Circadian Rhythm in Adipose Tissue: Novel Antioxidant Target for Metabolic and Cardiovascular Diseases
Abstract
:1. Introduction
2. Role of Adipose Tissue in Metabolic and Cardiovascular Health
2.1. White Adipose Tissue
2.2. Brown Adipose Tissue
2.3. Beige Cells and Browning
2.4. Perivascular Adipose Tissue
2.5. Adipokines
3. Circadian Rhythm in Adipose Tissue
3.1. The Molecular Clock Mechanism in Adipose Tissue
3.2. Clock Genes in Adipose Function
4. Oxidative Stress and Circadian Rhythm
4.1. Effects of Time-Restricted Feeding and Intermittent Fasting on Circadian Rhythm and Metabolism
4.2. Clock-Controlled Pathways in Adipose Tissue
4.2.1. Peroxisome Proliferator–Activated Receptors
4.2.2. PPARγ Coactivator 1
4.2.3. SIRT1
4.2.4. BCAA Metabolism and mTOR Signaling
4.2.5. GLP-1 and DPP-IV
4.2.6. AMPK
4.2.7. eNOS
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Collaborators, G.O. Health effects of overweight and obesity in 195 countries over 25 years. N. Engl. J. Med. 2017, 377, 13–27. [Google Scholar] [CrossRef]
- Lavie, C.J.; Milani, R.V.; Ventura, H.O. Obesity and cardiovascular disease: Risk factor, paradox, and impact of weight loss. J. Am. Coll. Cardiol. 2009, 53, 1925–1932. [Google Scholar] [CrossRef] [Green Version]
- Bass, J.; Lazar, M.A. Circadian time signatures of fitness and disease. Science 2016, 354, 994–999. [Google Scholar] [CrossRef] [Green Version]
- Fasshauer, M.; Bluher, M. Adipokines in health and disease. Trends Pharm. Sci. 2015, 36, 461–470. [Google Scholar] [CrossRef]
- Shostak, A.; Meyer-Kovac, J.; Oster, H. Circadian regulation of lipid mobilization in white adipose tissues. Diabetes 2013, 62, 2195–2203. [Google Scholar] [CrossRef] [Green Version]
- Kalsbeek, A.; Fliers, E.; Romijn, J.A.; La Fleur, S.E.; Wortel, J.; Bakker, O.; Endert, E.; Buijs, R.M. The suprachiasmatic nucleus generates the diurnal changes in plasma leptin levels. Endocrinology 2001, 142, 2677–2685. [Google Scholar] [CrossRef]
- Rudic, R.D.; McNamara, P.; Curtis, A.M.; Boston, R.C.; Panda, S.; Hogenesch, J.B.; Fitzgerald, G.A. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol. 2004, 2, e377. [Google Scholar] [CrossRef] [Green Version]
- Sena, C.M.; Leandro, A.; Azul, L.; Seica, R.; Perry, G. Vascular Oxidative Stress: Impact and Therapeutic Approaches. Front. Physiol. 2018, 9, 1668. [Google Scholar] [CrossRef] [Green Version]
- Hancock, J.T.; Desikan, R.; Neill, S.J. Role of reactive oxygen species in cell signalling pathways. Biochem. Soc. Trans. 2001, 29, 345–350. [Google Scholar] [CrossRef]
- Sies, H. Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: Oxidative eustress. Redox Biol. 2017, 11, 613–619. [Google Scholar] [CrossRef]
- Horvath, T.L.; Andrews, Z.B.; Diano, S. Fuel utilization by hypothalamic neurons: Roles for ROS. Trends Endocrinol. Metab. TEM 2009, 20, 78–87. [Google Scholar] [CrossRef] [PubMed]
- Furukawa, S.; Fujita, T.; Shimabukuro, M.; Iwaki, M.; Yamada, Y.; Nakajima, Y.; Nakayama, O.; Makishima, M.; Matsuda, M.; Shimomura, I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Investig. 2004, 114, 1752–1761. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Forstermann, U. Uncoupling of endothelial NO synthase in atherosclerosis and vascular disease. Curr Opin Pharm. 2013, 13, 161–167. [Google Scholar] [CrossRef] [PubMed]
- Chrysohoou, C.; Panagiotakos, D.B.; Pitsavos, C.; Skoumas, I.; Papademetriou, L.; Economou, M.; Stefanadis, C. The implication of obesity on total antioxidant capacity in apparently healthy men and women: The ATTICA study. Nutr. Metab. Cardiovasc. Dis. 2007, 17, 590–597. [Google Scholar] [CrossRef]
- Wilking, M.; Ndiaye, M.; Mukhtar, H.; Ahmad, N. Circadian rhythm connections to oxidative stress: Implications for human health. Antioxid. Redox Signal. 2013, 19, 192–208. [Google Scholar] [CrossRef] [Green Version]
- Bass, J.; Takahashi, J.S. Circadian integration of metabolism and energetics. Science 2010, 330, 1349–1354. [Google Scholar] [CrossRef] [Green Version]
- Reppert, S.M.; Weaver, D.R. Coordination of circadian timing in mammals. Nature 2002, 418, 935. [Google Scholar] [CrossRef]
- Potter, G.D.; Cade, J.E.; Grant, P.J.; Hardie, L.J. Nutrition and the circadian system. Br. J. Nutr. 2016, 116, 434–442. [Google Scholar] [CrossRef] [Green Version]
- Monk, T.H. Enhancing circadian zeitgebers. Sleep 2010, 33, 421–422. [Google Scholar] [CrossRef] [Green Version]
- Mukherji, A.; Kobiita, A.; Damara, M.; Misra, N.; Meziane, H.; Champy, M.-F.; Chambon, P. Shifting eating to the circadian rest phase misaligns the peripheral clocks with the master SCN clock and leads to a metabolic syndrome. Proc. Natl. Acad. Sci. USA 2015, 112, E6691–E6698. [Google Scholar] [CrossRef] [Green Version]
- Froy, O.; Garaulet, M. The Circadian Clock in White and Brown Adipose Tissue: Mechanistic, Endocrine, and Clinical Aspects. Endocr Rev. 2018, 39, 261–273. [Google Scholar] [CrossRef] [PubMed]
- Zhang, R.; Lahens, N.F.; Ballance, H.I.; Hughes, M.E.; Hogenesch, J.B. A circadian gene expression atlas in mammals: Implications for biology and medicine. Proc. Natl. Acad. Sci. USA 2014, 111, 16219–16224. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Christou, S.; Wehrens, S.M.T.; Isherwood, C.; Moller-Levet, C.S.; Wu, H.; Revell, V.L.; Bucca, G.; Skene, D.J.; Laing, E.E.; Archer, S.N.; et al. Circadian regulation in human white adipose tissue revealed by transcriptome and metabolic network analysis. Sci. Rep. 2019, 9, 2641. [Google Scholar] [CrossRef]
- Chen, Y.; Pan, R.; Pfeifer, A. Fat tissues, the brite and the dark sides. Pflug. Arch. Eur. J. Physiol. 2016, 468, 1803–1807. [Google Scholar] [CrossRef] [Green Version]
- Ahmadian, M.; Duncan, R.E.; Jaworski, K.; Sarkadi-Nagy, E.; Sul, H.S. Triacylglycerol metabolism in adipose tissue. Future Lipidol. 2007, 2, 229–237. [Google Scholar] [CrossRef] [Green Version]
- Aldhahi, W.; Hamdy, O. Adipokines, inflammation, and the endothelium in diabetes. Curr. Diabetes Rep. 2003, 3, 293–298. [Google Scholar] [CrossRef] [Green Version]
- Vitali, A.; Murano, I.; Zingaretti, M.C.; Frontini, A.; Ricquier, D.; Cinti, S. The adipose organ of obesity-prone C57BL/6J mice is composed of mixed white and brown adipocytes. J. Lipid Res. 2012, 53, 619–629. [Google Scholar] [CrossRef] [Green Version]
- Lafontan, M. Advances in adipose tissue metabolism. Int. J. Obes. 2008, 32 (Suppl. 7), S39–S51. [Google Scholar] [CrossRef] [Green Version]
- Cannon, B.; Nedergaard, J. Brown adipose tissue: Function and physiological significance. Physiol. Rev. 2004, 84, 277–359. [Google Scholar] [CrossRef]
- Lepper, C.; Fan, C.M. Inducible lineage tracing of Pax7-descendant cells reveals embryonic origin of adult satellite cells. Genesis 2010, 48, 424–436. [Google Scholar] [CrossRef]
- An, Y.; Wang, G.; Diao, Y.; Long, Y.; Fu, X.; Weng, M.; Zhou, L.; Sun, K.; Cheung, T.H.; Ip, N.Y.; et al. A Molecular Switch Regulating Cell Fate Choice between Muscle Progenitor Cells and Brown Adipocytes. Dev. Cell 2017, 41, 382–391 e385. [Google Scholar] [CrossRef] [Green Version]
- Virtanen, K.A.; Lidell, M.E.; Orava, J.; Heglind, M.; Westergren, R.; Niemi, T.; Taittonen, M.; Laine, J.; Savisto, N.J.; Enerback, S.; et al. Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 2009, 360, 1518–1525. [Google Scholar] [CrossRef]
- Yoneshiro, T.; Aita, S.; Matsushita, M.; Kayahara, T.; Kameya, T.; Kawai, Y.; Iwanaga, T.; Saito, M. Recruited brown adipose tissue as an antiobesity agent in humans. J. Clin. Investig. 2013, 123, 3404–3408. [Google Scholar] [CrossRef] [Green Version]
- Stanford, K.I.; Middelbeek, R.J.; Townsend, K.L.; An, D.; Nygaard, E.B.; Hitchcox, K.M.; Markan, K.R.; Nakano, K.; Hirshman, M.F.; Tseng, Y.H.; et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J. Clin. Investig. 2013, 123, 215–223. [Google Scholar] [CrossRef] [Green Version]
- Lizcano, F. The Beige Adipocyte as a Therapy for Metabolic Diseases. Int. J. Mol. Sci. 2019, 20, 58. [Google Scholar] [CrossRef] [Green Version]
- Dewal, R.S.; Stanford, K.I. Effects of exercise on brown and beige adipocytes. Biochim. Biophys. Acta. Mol. Cell Biol. Lipids 2019, 1864, 71–78. [Google Scholar] [CrossRef]
- Min, S.Y.; Kady, J.; Nam, M.; Rojas-Rodriguez, R.; Berkenwald, A.; Kim, J.H.; Noh, H.L.; Kim, J.K.; Cooper, M.P.; Fitzgibbons, T.; et al. Human ‘brite/beige’ adipocytes develop from capillary networks, and their implantation improves metabolic homeostasis in mice. Nat. Med. 2016, 22, 312–318. [Google Scholar] [CrossRef] [Green Version]
- Wu, J.; Bostrom, P.; Sparks, L.M.; Ye, L.; Choi, J.H.; Giang, A.H.; Khandekar, M.; Virtanen, K.A.; Nuutila, P.; Schaart, G.; et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012, 150, 366–376. [Google Scholar] [CrossRef] [Green Version]
- Altshuler-Keylin, S.; Shinoda, K.; Hasegawa, Y.; Ikeda, K.; Hong, H.; Kang, Q.; Yang, Y.; Perera, R.M.; Debnath, J.; Kajimura, S. Beige Adipocyte Maintenance Is Regulated by Autophagy-Induced Mitochondrial Clearance. Cell Metab. 2016, 24, 402–419. [Google Scholar] [CrossRef] [Green Version]
- Roh, H.C.; Tsai, L.T.Y.; Shao, M.; Tenen, D.; Shen, Y.; Kumari, M.; Lyubetskaya, A.; Jacobs, C.; Dawes, B.; Gupta, R.K.; et al. Warming Induces Significant Reprogramming of Beige, but Not Brown, Adipocyte Cellular Identity. Cell Metab. 2018, 27, 1121–1137 e1125. [Google Scholar] [CrossRef] [PubMed]
- Kleiner, S.; Douris, N.; Fox, E.C.; Mepani, R.J.; Verdeguer, F.; Wu, J.; Kharitonenkov, A.; Flier, J.S.; Maratos-Flier, E.; Spiegelman, B.M. FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis. Genes Dev. 2012, 26, 271–281. [Google Scholar]
- Bordicchia, M.; Liu, D.; Amri, E.Z.; Ailhaud, G.; Dessi-Fulgheri, P.; Zhang, C.; Takahashi, N.; Sarzani, R.; Collins, S. Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. J. Clin. Investig. 2012, 122, 1022–1036. [Google Scholar] [CrossRef] [Green Version]
- Schulz, T.J.; Huang, P.; Huang, T.L.; Xue, R.D.; McDougall, L.E.; Townsend, K.L.; Cypess, A.M.; Mishina, Y.; Gussoni, E.; Tseng, Y.H. Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat. Nature 2013, 495, 379–383. [Google Scholar] [CrossRef] [Green Version]
- Aldiss, P.; Davies, G.; Woods, R.; Budge, H.; Sacks, H.S.; Symonds, M.E. ‘Browning’ the cardiac and peri-vascular adipose tissues to modulate cardiovascular risk. Int. J. Cardiol. 2017, 228, 265–274. [Google Scholar] [CrossRef] [Green Version]
- Saito, M.; Okamatsu-Ogura, Y.; Matsushita, M.; Watanabe, K.; Yoneshiro, T.; Nio-Kobayashi, J.; Iwanaga, T.; Miyagawa, M.; Kameya, T.; Nakada, K.; et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: Effects of cold exposure and adiposity. Diabetes 2009, 58, 1526–1531. [Google Scholar] [CrossRef] [Green Version]
- Bartelt, A.; Bruns, O.T.; Reimer, R.; Hohenberg, H.; Ittrich, H.; Peldschus, K.; Kaul, M.G.; Tromsdorf, U.I.; Weller, H.; Waurisch, C.; et al. Brown adipose tissue activity controls triglyceride clearance. Nat. Med. 2011, 17, 200–205. [Google Scholar] [CrossRef]
- Planavila, A.; Redondo, I.; Hondares, E.; Vinciguerra, M.; Munts, C.; Iglesias, R.; Gabrielli, L.A.; Sitges, M.; Giralt, M.; van Bilsen, M.; et al. Fibroblast growth factor 21 protects against cardiac hypertrophy in mice. Nat. Commun. 2013, 4, 2019. [Google Scholar] [CrossRef]
- Liu, S.Q.; Roberts, D.; Kharitonenkov, A.; Zhang, B.; Hanson, S.M.; Li, Y.C.; Zhang, L.Q.; Wu, Y.H. Endocrine protection of ischemic myocardium by FGF21 from the liver and adipose tissue. Sci. Rep. 2013, 3, 2767. [Google Scholar] [CrossRef] [Green Version]
- Gimeno, R.E.; Moller, D.E. FGF21-based pharmacotherapy--potential utility for metabolic disorders. Trends Endocrinol. Metab. TEM 2014, 25, 303–311. [Google Scholar] [CrossRef]
- Bookout, A.L.; de Groot, M.H.; Owen, B.M.; Lee, S.; Gautron, L.; Lawrence, H.L.; Ding, X.; Elmquist, J.K.; Takahashi, J.S.; Mangelsdorf, D.J.; et al. FGF21 regulates metabolism and circadian behavior by acting on the nervous system. Nat. Med. 2013, 19, 1147–1152. [Google Scholar] [CrossRef]
- Man, A.W.C.; Zhou, Y.; Xia, N.; Li, H. Perivascular Adipose Tissue as a Target for Antioxidant Therapy for Cardiovascular Complications. Antioxidants 2020, 9, 574. [Google Scholar] [CrossRef]
- Xia, N.; Li, H.G. The role of perivascular adipose tissue in obesity-induced vascular dysfunction. Br. J. Pharmacol. 2017, 174, 3425–3442. [Google Scholar] [CrossRef] [Green Version]
- Chang, L.; Milton, H.; Eitzman, D.T.; Chen, Y.E. Paradoxical roles of perivascular adipose tissue in atherosclerosis and hypertension. Circ. J. 2012, CJ-12-1393. [Google Scholar] [CrossRef] [Green Version]
- Gao, Y.J.; Zeng, Z.H.; Teoh, K.; Sharma, A.M.; Abouzahr, L.; Cybulsky, I.; Lamy, A.; Semelhago, L.; Lee, R.M. Perivascular adipose tissue modulates vascular function in the human internal thoracic artery. J. Thorac. Cardiovasc. Surg. 2005, 130, 1130–1136. [Google Scholar] [CrossRef] [Green Version]
- Greenstein, A.S.; Khavandi, K.; Withers, S.B.; Sonoyama, K.; Clancy, O.; Jeziorska, M.; Laing, I.; Yates, A.P.; Pemberton, P.W.; Malik, R.A.; et al. Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 2009, 119, 1661–1670. [Google Scholar] [CrossRef] [Green Version]
- Brown, N.K.; Zhou, Z.; Zhang, J.; Zeng, R.; Wu, J.; Eitzman, D.T.; Chen, Y.E.; Chang, L. Perivascular adipose tissue in vascular function and disease: A review of current research and animal models. Arterioscler. Thromb. Vasc. Biol. 2014, 34, 1621–1630. [Google Scholar] [CrossRef] [Green Version]
- Omar, A.; Chatterjee, T.K.; Tang, Y.; Hui, D.Y.; Weintraub, N.L. Proinflammatory phenotype of perivascular adipocytes. Arterioscler. Thromb. Vasc. Biol. 2014, 34, 1631–1636. [Google Scholar] [CrossRef] [Green Version]
- Gil-Ortega, M.; Somoza, B.; Huang, Y.; Gollasch, M.; Fernandez-Alfonso, M.S. Regional differences in perivascular adipose tissue impacting vascular homeostasis. Trends Endocrinol. Metab. TEM 2015, 26, 367–375. [Google Scholar] [CrossRef]
- Drosos, I.; Chalikias, G.; Pavlaki, M.; Kareli, D.; Epitropou, G.; Bougioukas, G.; Mikroulis, D.; Konstantinou, F.; Giatromanolaki, A.; Ritis, K.; et al. Differences between perivascular adipose tissue surrounding the heart and the internal mammary artery: Possible role for the leptin-inflammation-fibrosis-hypoxia axis. Clin. Res. Cardiol. 2016, 105, 887–900. [Google Scholar] [CrossRef]
- Victorio, J.A.; Fontes, M.T.; Rossoni, L.V.; Davel, A.P. Different Anti-Contractile Function and Nitric Oxide Production of Thoracic and Abdominal Perivascular Adipose Tissues. Front. Physiol. 2016, 7, 295. [Google Scholar] [CrossRef] [Green Version]
- Chang, L.; Garcia-Barrio, M.T.; Chen, Y.E. Perivascular Adipose Tissue Regulates Vascular Function by Targeting Vascular Smooth Muscle Cells. Arterioscler. Thromb. Vasc. Biol. 2020, 40. [Google Scholar] [CrossRef] [PubMed]
- Bailey-Downs, L.C.; Tucsek, Z.; Toth, P.; Sosnowska, D.; Gautam, T.; Sonntag, W.E.; Csiszar, A.; Ungvari, Z. Aging exacerbates obesity-induced oxidative stress and inflammation in perivascular adipose tissue in mice: A paracrine mechanism contributing to vascular redox dysregulation and inflammation. J. Gerontol. Ser. A Biomed. Sci. Med. Sci. 2013, 68, 780–792. [Google Scholar] [CrossRef] [Green Version]
- Gil-Ortega, M.; Condezo-Hoyos, L.; Garcia-Prieto, C.F.; Arribas, S.M.; Gonzalez, M.C.; Aranguez, I.; Ruiz-Gayo, M.; Somoza, B.; Fernandez-Alfonso, M.S. Imbalance between Pro and Anti-Oxidant Mechanisms in Perivascular Adipose Tissue Aggravates Long-Term High-Fat Diet-Derived Endothelial Dysfunction. PLoS ONE 2014, 9, e95312. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aldiss, P.; Lewis, J.E.; Lupini, I.; Boocock, D.J.; Miles, A.K.; Ebling, F.J.; Budge, H.; Symonds, M.E. Exercise does not induce browning of WAT at thermoneutrality and induces an oxidative, myogenic signature in BAT. bioRxiv 2019, 649061. [Google Scholar]
- Dutheil, F.; Gordon, B.A.; Naughton, G.; Crendal, E.; Courteix, D.; Chaplais, E.; Thivel, D.; Lac, G.; Benson, A.C. Cardiovascular risk of adipokines: A review. J. Int. Med Res. 2018, 46, 2082–2095. [Google Scholar] [CrossRef]
- Deng, Y.; Scherer, P.E. Adipokines as novel biomarkers and regulators of the metabolic syndrome. Ann. N. Y. Acad. Sci. 2010, 1212, E1–E19. [Google Scholar] [CrossRef]
- Lafontan, M. Historical perspectives in fat cell biology: The fat cell as a model for the investigation of hormonal and metabolic pathways. Am. J. Physiol. Cell Physiol. 2012, 302, C327–C359. [Google Scholar] [CrossRef] [Green Version]
- Sena, C.M.; Pereira, A.; Fernandes, R.; Letra, L.; Seica, R.M. Adiponectin improves endothelial function in mesenteric arteries of rats fed a high-fat diet: Role of perivascular adipose tissue. Br. J. Pharmacol. 2017, 174, 3514–3526. [Google Scholar] [CrossRef] [Green Version]
- Challet, E. Circadian aspects of adipokine regulation in rodents. Best Pract. Res. Clin. Endocrinol. Metab. 2017, 31, 573–582. [Google Scholar] [CrossRef]
- Mohawk, J.A.; Green, C.B.; Takahashi, J.S. Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 2012, 35, 445–462. [Google Scholar] [CrossRef] [Green Version]
- Kawano, H.; Motoyama, T.; Yasue, H.; Hirai, N.; Waly, H.M.; Kugiyama, K.; Ogawa, H. Endothelial function fluctuates with diurnal variation in the frequency of ischemic episodes in patients with variant angina. J. Am. Coll. Cardiol. 2002, 40, 266–270. [Google Scholar] [PubMed] [Green Version]
- Otto, M.E.; Svatikova, A.; de Mattos Barretto, R.B.; Santos, S.; Hoffmann, M.; Khandheria, B.; Somers, V. Early morning attenuation of endothelial function in healthy humans. Circulation 2004, 109, 2507–2510. [Google Scholar] [PubMed] [Green Version]
- Walters, J.F.; Skene, D.J.; Hampton, S.M.; Ferns, G.A. Biological rhythms, endothelial health and cardiovascular disease. Med Sci. Monit. 2003, 9, RA1–RA8. [Google Scholar] [PubMed]
- Singh, R.B.; Cornélissen, G.; Weydahl, A.; Schwartzkopff, O.; Katinas, G.; Otsuka, K.; Watanabe, Y.; Yano, S.; Mori, H.; Ichimaru, Y. Circadian heart rate and blood pressure variability considered for research and patient care. Int. J. Cardiol. 2003, 87, 9–28. [Google Scholar]
- Panza, J.A.; Epstein, S.E.; Quyyumi, A.A. Circadian variation in vascular tone and its relation to α-sympathetic vasoconstrictor activity. N. Engl. J. Med. 1991, 325, 986–990. [Google Scholar]
- Lee, C.; Etchegaray, J.P.; Cagampang, F.R.; Loudon, A.S.; Reppert, S.M. Posttranslational mechanisms regulate the mammalian circadian clock. Cell 2001, 107, 855–867. [Google Scholar] [CrossRef]
- Young, M.E. The circadian clock within the heart: Potential influence on myocardial gene expression, metabolism, and function. Am. J. Physiol. Heart Circ. Physiol. 2006, 290, H1–H16. [Google Scholar] [CrossRef] [Green Version]
- Reppert, S.M.; Weaver, D.R. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 2001, 63, 647–676. [Google Scholar] [CrossRef]
- Kraves, S.; Weitz, C.J. A role for cardiotrophin-like cytokine in the circadian control of mammalian locomotor activity. Nat. Neurosci. 2006, 9, 212–219. [Google Scholar] [CrossRef]
- Cheng, M.Y.; Bullock, C.M.; Li, C.; Lee, A.G.; Bermak, J.C.; Belluzzi, J.; Weaver, D.R.; Leslie, F.M.; Zhou, Q.Y. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 2002, 417, 405–410. [Google Scholar] [CrossRef]
- Kiehn, J.-T.; Koch, C.E.; Walter, M.; Brod, A.; Oster, H. Circadian rhythms and clocks in adipose tissues: Current Insights. ChronoPhysiology Ther. 2017, 7, 7–17. [Google Scholar]
- Ando, H.; Yanagihara, H.; Hayashi, Y.; Obi, Y.; Tsuruoka, S.; Takamura, T.; Kaneko, S.; Fujimura, A. Rhythmic messenger ribonucleic acid expression of clock genes and adipocytokines in mouse visceral adipose tissue. Endocrinology 2005, 146, 5631–5636. [Google Scholar] [CrossRef] [PubMed]
- Zvonic, S.; Ptitsyn, A.A.; Conrad, S.A.; Scott, L.K.; Floyd, Z.E.; Kilroy, G.; Wu, X.; Goh, B.C.; Mynatt, R.L.; Gimble, J.M. Characterization of peripheral circadian clocks in adipose tissues. Diabetes 2006, 55, 962–970. [Google Scholar] [CrossRef] [Green Version]
- Wu, X.; Zvonic, S.; Floyd, Z.E.; Kilroy, G.; Goh, B.C.; Hernandez, T.L.; Eckel, R.H.; Mynatt, R.L.; Gimble, J.M. Induction of circadian gene expression in human subcutaneous adipose-derived stem cells. Obesity 2007, 15, 2560–2570. [Google Scholar] [CrossRef] [PubMed]
- Otway, D.T.; Mantele, S.; Bretschneider, S.; Wright, J.; Trayhurn, P.; Skene, D.J.; Robertson, M.D.; Johnston, J.D. Rhythmic diurnal gene expression in human adipose tissue from individuals who are lean, overweight, and type 2 diabetic. Diabetes 2011, 60, 1577–1581. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gomez-Santos, C.; Gomez-Abellan, P.; Madrid, J.A.; Hernandez-Morante, J.J.; Lujan, J.A.; Ordovas, J.M.; Garaulet, M. Circadian rhythm of clock genes in human adipose explants. Obesity 2009, 17, 1481–1485. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buhr, E.D.; Takahashi, J.S. Molecular components of the Mammalian circadian clock. Handb. Exp. Pharmacol. 2013, 3–27. [Google Scholar] [CrossRef] [Green Version]
- Schibler, U.; Ripperger, J.; Brown, S.A. Peripheral circadian oscillators in mammals: Time and food. J. Biol. Rhythm. 2003, 18, 250–260. [Google Scholar] [CrossRef]
- Froy, O.; Chang, D.C.; Reppert, S.M. Redox potential: Differential roles in dCRY and mCRY1 functions. Curr. Biol. CB 2002, 12, 147–152. [Google Scholar] [CrossRef] [Green Version]
- Preitner, N.; Damiola, F.; Lopez-Molina, L.; Zakany, J.; Duboule, D.; Albrecht, U.; Schibler, U. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002, 110, 251–260. [Google Scholar] [CrossRef]
- Ueda, H.R.; Hayashi, S.; Chen, W.; Sano, M.; Machida, M.; Shigeyoshi, Y.; Iino, M.; Hashimoto, S. System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat. Genet. 2005, 37, 187–192. [Google Scholar] [CrossRef]
- Sato, T.K.; Panda, S.; Miraglia, L.J.; Reyes, T.M.; Rudic, R.D.; McNamara, P.; Naik, K.A.; FitzGerald, G.A.; Kay, S.A.; Hogenesch, J.B. A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 2004, 43, 527–537. [Google Scholar] [CrossRef] [Green Version]
- Dunlap, J.C. Molecular bases for circadian clocks. Cell 1999, 96, 271–290. [Google Scholar] [CrossRef] [Green Version]
- Onder, Y.; Green, C.B. Rhythms of metabolism in adipose tissue and mitochondria. Neurobiol. Sleep Circadian Rhythm. 2018, 4, 57–63. [Google Scholar] [CrossRef]
- Bray, M.; Young, M. The role of cell-specific circadian clocks in metabolism and disease. Obes. Rev. 2009, 10, 6–13. [Google Scholar] [CrossRef]
- Antoch, M.P.; Gorbacheva, V.Y.; Vykhovanets, O.; Toshkov, I.A.; Kondratov, R.V.; Kondratova, A.A.; Lee, C.; Nikitin, A.Y. Disruption of the circadian clock due to the Clock mutation has discrete effects on aging and carcinogenesis. Cell Cycle 2008, 7, 1197–1204. [Google Scholar] [CrossRef] [Green Version]
- Kondratov, R.V.; Kondratova, A.A.; Gorbacheva, V.Y.; Vykhovanets, O.V.; Antoch, M.P. Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev. 2006, 20, 1868–1873. [Google Scholar] [CrossRef] [Green Version]
- Turek, F.W.; Joshu, C.; Kohsaka, A.; Lin, E.; Ivanova, G.; McDearmon, E.; Laposky, A.; Losee-Olson, S.; Easton, A.; Jensen, D.R. Obesity and metabolic syndrome in circadian Clock mutant mice. Science 2005, 308, 1043–1045. [Google Scholar] [CrossRef] [Green Version]
- Anea, C.B.; Zhang, M.; Stepp, D.W.; Simkins, G.B.; Reed, G.; Fulton, D.J.; Rudic, R.D. Vascular disease in mice with a dysfunctional circadian clock. Circulation 2009, 119, 1510–1517. [Google Scholar] [CrossRef] [Green Version]
- Shimba, S.; Ishii, N.; Ohta, Y.; Ohno, T.; Watabe, Y.; Hayashi, M.; Wada, T.; Aoyagi, T.; Tezuka, M. Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc. Natl. Acad. Sci. USA 2005, 102, 12071–12076. [Google Scholar] [CrossRef] [Green Version]
- Guo, B.; Chatterjee, S.; Li, L.; Kim, J.M.; Lee, J.; Yechoor, V.K.; Minze, L.J.; Hsueh, W.; Ma, K. The clock gene, brain and muscle Arnt-like 1, regulates adipogenesis via Wnt signaling pathway. FASEB J. 2012, 26, 3453–3463. [Google Scholar] [CrossRef]
- Nam, D.; Guo, B.; Chatterjee, S.; Chen, M.H.; Nelson, D.; Yechoor, V.K.; Ma, K. The adipocyte clock controls brown adipogenesis through the TGF-beta and BMP signaling pathways. J. Cell Sci. 2015, 128, 1835–1847. [Google Scholar] [CrossRef] [Green Version]
- Fournier, B.; Murray, B.; Gutzwiller, S.; Marcaletti, S.; Marcellin, D.; Bergling, S.; Brachat, S.; Persohn, E.; Pierrel, E.; Bombard, F.; et al. Blockade of the activin receptor IIb activates functional brown adipogenesis and thermogenesis by inducing mitochondrial oxidative metabolism. Mol. Cell. Biol. 2012, 32, 2871–2879. [Google Scholar] [CrossRef] [Green Version]
- Kuo, M.M.; Kim, S.; Tseng, C.Y.; Jeon, Y.H.; Choe, S.; Lee, D.K. BMP-9 as a potent brown adipogenic inducer with anti-obesity capacity. Biomaterials 2014, 35, 3172–3179. [Google Scholar] [CrossRef]
- Kondratov, R.V.; Vykhovanets, O.; Kondratova, A.A.; Antoch, M.P. Antioxidant N-acetyl-L-cysteine ameliorates symptoms of premature aging associated with the deficiency of the circadian protein BMAL1. Aging 2009, 1, 979–987. [Google Scholar] [CrossRef] [Green Version]
- Chawla, A.; Lazar, M.A. Induction of Rev-ErbA alpha, an orphan receptor encoded on the opposite strand of the alpha-thyroid hormone receptor gene, during adipocyte differentiation. J. Biol. Chem. 1993, 268, 16265–16269. [Google Scholar]
- Bray, M.S.; Young, M.E. Circadian rhythms in the development of obesity: Potential role for the circadian clock within the adipocyte. Obes. Rev. Off. J. Int. Assoc. Study Obes. 2007, 8, 169–181. [Google Scholar] [CrossRef] [PubMed]
- Torra, I.P.; Tsibulsky, V.; Delaunay, F.; Saladin, R.; Laudet, V.; Fruchart, J.C.; Kosykh, V.; Staels, B. Circadian and glucocorticoid regulation of Rev-erbalpha expression in liver. Endocrinology 2000, 141, 3799–3806. [Google Scholar] [CrossRef]
- Delezie, J.; Dumont, S.; Dardente, H.; Oudart, H.; Grechez-Cassiau, A.; Klosen, P.; Teboul, M.; Delaunay, F.; Pevet, P.; Challet, E. The nuclear receptor REV-ERBalpha is required for the daily balance of carbohydrate and lipid metabolism. FASEB J. 2012, 26, 3321–3335. [Google Scholar] [CrossRef] [Green Version]
- Solt, L.A.; Wang, Y.; Banerjee, S.; Hughes, T.; Kojetin, D.J.; Lundasen, T.; Shin, Y.; Liu, J.; Cameron, M.D.; Noel, R.; et al. Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 2012, 485, 62–68. [Google Scholar] [CrossRef]
- Amador, A.; Wang, Y.; Banerjee, S.; Kameneka, T.M.; Solt, L.A.; Burris, T.P. Pharmacological and Genetic Modulation of REV-ERB Activity and Expression Affects Orexigenic Gene Expression. PLoS ONE 2016, 11, e0151014. [Google Scholar] [CrossRef]
- Gerhart-Hines, Z.; Feng, D.; Emmett, M.J.; Everett, L.J.; Loro, E.; Briggs, E.R.; Bugge, A.; Hou, C.; Ferrara, C.; Seale, P.; et al. The nuclear receptor Rev-erbalpha controls circadian thermogenic plasticity. Nature 2013, 503, 410–413. [Google Scholar] [CrossRef] [PubMed]
- Nam, D.; Chatterjee, S.; Yin, H.; Liu, R.; Lee, J.; Yechoor, V.K.; Ma, K. Novel Function of Rev-erbalpha in Promoting Brown Adipogenesis. Sci. Rep. 2015, 5, 11239. [Google Scholar] [CrossRef] [Green Version]
- Grimaldi, B.; Bellet, M.M.; Katada, S.; Astarita, G.; Hirayama, J.; Amin, R.H.; Granneman, J.G.; Piomelli, D.; Leff, T.; Sassone-Corsi, P. PER2 controls lipid metabolism by direct regulation of PPARgamma. Cell Metab. 2010, 12, 509–520. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aggarwal, A.; Costa, M.J.; Rivero-Gutierrez, B.; Ji, L.; Morgan, S.L.; Feldman, B.J. The Circadian Clock Regulates Adipogenesis by a Per3 Crosstalk Pathway to Klf15. Cell Rep. 2017, 21, 2367–2375. [Google Scholar] [CrossRef] [Green Version]
- Ikeda, H.; Yong, Q.; Kurose, T.; Todo, T.; Mizunoya, W.; Fushiki, T.; Seino, Y.; Yamada, Y. Clock gene defect disrupts light-dependency of autonomic nerve activity. Biochem. Biophys. Res. Commun. 2007, 364, 457–463. [Google Scholar] [CrossRef] [Green Version]
- Barclay, J.L.; Shostak, A.; Leliavski, A.; Tsang, A.H.; Johren, O.; Muller-Fielitz, H.; Landgraf, D.; Naujokat, N.; van der Horst, G.T.; Oster, H. High-fat diet-induced hyperinsulinemia and tissue-specific insulin resistance in Cry-deficient mice. Am. J. Physiol. Endocrinol. Metab. 2013, 304, E1053–E1063. [Google Scholar] [CrossRef] [Green Version]
- Narasimamurthy, R.; Hatori, M.; Nayak, S.K.; Liu, F.; Panda, S.; Verma, I.M. Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc. Natl. Acad. Sci. USA 2012, 109, 12662–12667. [Google Scholar] [CrossRef] [Green Version]
- Dashti, H.S.; Smith, C.E.; Lee, Y.C.; Parnell, L.D.; Lai, C.Q.; Arnett, D.K.; Ordovas, J.M.; Garaulet, M. CRY1 circadian gene variant interacts with carbohydrate intake for insulin resistance in two independent populations: Mediterranean and North American. Chronobiol. Int. 2014, 31, 660–667. [Google Scholar] [CrossRef] [Green Version]
- Paschos, G.K.; Ibrahim, S.; Song, W.L.; Kunieda, T.; Grant, G.; Reyes, T.M.; Bradfield, C.A.; Vaughan, C.H.; Eiden, M.; Masoodi, M.; et al. Obesity in mice with adipocyte-specific deletion of clock component Arntl. Nat. Med. 2012, 18, 1768–1777. [Google Scholar] [CrossRef] [Green Version]
- Birky, T.L.; Bray, M.S. Understanding circadian gene function: Animal models of tissue-specific circadian disruption. IUBMB Life 2014, 66, 34–41. [Google Scholar] [CrossRef] [PubMed]
- Chang, L.; Xiong, W.; Zhao, X.; Fan, Y.; Guo, Y.; Garcia-Barrio, M.; Zhang, J.; Jiang, Z.; Lin, J.D.; Chen, Y.E. Bmal1 in Perivascular Adipose Tissue Regulates Resting-Phase Blood Pressure Through Transcriptional Regulation of Angiotensinogen. Circulation 2018, 138, 67–79. [Google Scholar] [CrossRef] [PubMed]
- Stadtman, E.R. Metal ion-catalyzed oxidation of proteins: Biochemical mechanism and biological consequences. Free Radic. Biol. Med. 1990, 9, 315–325. [Google Scholar] [CrossRef] [Green Version]
- Frohnert, B.I.; Sinaiko, A.R.; Serrot, F.J.; Foncea, R.E.; Moran, A.; Ikramuddin, S.; Choudry, U.; Bernlohr, D.A. Increased adipose protein carbonylation in human obesity. Obesity 2011, 19, 1735–1741. [Google Scholar] [CrossRef] [PubMed]
- Forstermann, U.; Xia, N.; Li, H. Roles of Vascular Oxidative Stress and Nitric Oxide in the Pathogenesis of Atherosclerosis. Circ. Res. 2017, 120, 713–735. [Google Scholar] [CrossRef]
- Li, H.; Horke, S.; Forstermann, U. Vascular oxidative stress, nitric oxide and atherosclerosis. Atherosclerosis 2014, 237, 208–219. [Google Scholar] [CrossRef]
- Cancello, R.; Henegar, C.; Viguerie, N.; Taleb, S.; Poitou, C.; Rouault, C.; Coupaye, M.; Pelloux, V.; Hugol, D.; Bouillot, J.-L. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 2005, 54, 2277–2286. [Google Scholar] [CrossRef] [Green Version]
- Chen, B.; Lam, K.S.; Wang, Y.; Wu, D.; Lam, M.C.; Shen, J.; Wong, L.; Hoo, R.L.; Zhang, J.; Xu, A. Hypoxia dysregulates the production of adiponectin and plasminogen activator inhibitor-1 independent of reactive oxygen species in adipocytes. Biochem. Biophys. Res. Commun. 2006, 341, 549–556. [Google Scholar] [CrossRef]
- Peek, C.B.; Levine, D.C.; Cedernaes, J.; Taguchi, A.; Kobayashi, Y.; Tsai, S.J.; Bonar, N.A.; McNulty, M.R.; Ramsey, K.M.; Bass, J. Circadian Clock Interaction with HIF1alpha Mediates Oxygenic Metabolism and Anaerobic Glycolysis in Skeletal Muscle. Cell Metab. 2017, 25, 86–92. [Google Scholar] [CrossRef] [Green Version]
- Egg, M.; Koblitz, L.; Hirayama, J.; Schwerte, T.; Folterbauer, C.; Kurz, A.; Fiechtner, B.; Most, M.; Salvenmoser, W.; Sassone-Corsi, P.; et al. Linking Oxygen to Time: The Bidirectional Interaction Between the Hypoxic Signaling Pathway and the Circadian Clock. Chronobiol. Int. 2013, 30, 510–529. [Google Scholar] [CrossRef]
- Kusminski, C.M.; Bickel, P.E.; Scherer, P.E. Targeting adipose tissue in the treatment of obesity-associated diabetes. Nat. Rev. Drug Discov. 2016, 15, 639–660. [Google Scholar] [CrossRef] [PubMed]
- Alzamendi, A.; Giovambattista, A.; Raschia, A.; Madrid, V.; Gaillard, R.C.; Rebolledo, O.; Gagliardino, J.J.; Spinedi, E. Fructose-rich diet-induced abdominal adipose tissue endocrine dysfunction in normal male rats. Endocrine 2009, 35, 227–232. [Google Scholar] [CrossRef] [PubMed]
- Rosen, E.D.; Spiegelman, B.M. What we talk about when we talk about fat. Cell 2014, 156, 20–44. [Google Scholar] [CrossRef] [Green Version]
- Masschelin, P.M.; Cox, A.R.; Chernis, N.; Hartig, S.M. The Impact of Oxidative Stress on Adipose Tissue Energy Balance. Front. Physiol. 2019, 10, 1638. [Google Scholar] [CrossRef] [PubMed]
- Vgontzas, A.N.; Pejovic, S.; Zoumakis, E.; Lin, H.M.; Bixler, E.O.; Basta, M.; Fang, J.; Sarrigiannidis, A.; Chrousos, G.P. Daytime napping after a night of sleep loss decreases sleepiness, improves performance, and causes beneficial changes in cortisol and interleukin-6 secretion. Am. J. Physiol. Endocrinol. Metab. 2007, 292, E253–E261. [Google Scholar] [CrossRef] [PubMed]
- Vgontzas, A.N. Does obesity play a major role in the pathogenesis of sleep apnoea and its associated manifestations via inflammation, visceral adiposity, and insulin resistance? Arch. Physiol. Biochem. 2008, 114, 211–223. [Google Scholar] [CrossRef] [PubMed]
- Bray, M.S.; Tsai, J.Y.; Villegas-Montoya, C.; Boland, B.B.; Blasier, Z.; Egbejimi, O.; Kueht, M.; Young, M.E. Time-of-day-dependent dietary fat consumption influences multiple cardiometabolic syndrome parameters in mice. Int. J. Obes. 2010, 34, 1589–1598. [Google Scholar] [CrossRef] [Green Version]
- Hardeland, R.; Coto-Montes, A.; Poeggeler, B. Circadian rhythms, oxidative stress, and antioxidative defense mechanisms. Chronobiol. Int. 2003, 20, 921–962. [Google Scholar] [CrossRef]
- Teixeira, K.R.C.; Dos Santos, C.P.; de Medeiros, L.A.; Mendes, J.A.; Cunha, T.M.; De Angelis, K.; Penha-Silva, N.; de Oliveira, E.P.; Crispim, C.A. Night workers have lower levels of antioxidant defenses and higher levels of oxidative stress damage when compared to day workers. Sci. Rep. 2019, 9, 4455. [Google Scholar] [CrossRef] [Green Version]
- Punjabi, N.M.; Beamer, B.A. C-reactive protein is associated with sleep disordered breathing independent of adiposity. Sleep 2007, 30, 29–34. [Google Scholar] [CrossRef] [Green Version]
- Lananna, B.V.; Musiek, E.S. The wrinkling of time: Aging, inflammation, oxidative stress, and the circadian clock in neurodegeneration. Neurobiol. Dis. 2020, 139, 104832. [Google Scholar] [CrossRef] [PubMed]
- Sengupta, S.; Yang, G.; O’Donnell, J.C.; Hinson, M.D.; McCormack, S.E.; Falk, M.J.; La, P.; Robinson, M.B.; Williams, M.L.; Yohannes, M.T.; et al. The circadian gene Rev-erbalpha improves cellular bioenergetics and provides preconditioning for protection against oxidative stress. Free Radic. Biol. Med. 2016, 93, 177–189. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pei, J.F.; Li, X.K.; Li, W.Q.; Gao, Q.; Zhang, Y.; Wang, X.M.; Fu, J.Q.; Cui, S.S.; Qu, J.H.; Zhao, X.; et al. Diurnal oscillations of endogenous H2O2 sustained by p66(Shc) regulate circadian clocks. Nat. Cell Biol. 2019, 21, 1553–1564. [Google Scholar] [CrossRef] [PubMed]
- Imai, S.-i. “Clocks” in the NAD World: NAD as a metabolic oscillator for the regulation of metabolism and aging. Biochim. Biophys. Acta Proteins Proteom. 2010, 1804, 1584–1590. [Google Scholar] [CrossRef] [Green Version]
- Froy, O. Circadian rhythms and obesity in mammals. ISRN Obes. 2012, 2012. [Google Scholar] [CrossRef] [Green Version]
- Froy, O. Circadian rhythms, aging, and life span in mammals. Physiology 2011, 26, 225–235. [Google Scholar] [CrossRef] [Green Version]
- Sandbichler, A.M.; Jansen, B.; Peer, B.A.; Paulitsch, M.; Pelster, B.; Egg, M. Metabolic Plasticity Enables Circadian Adaptation to Acute Hypoxia in Zebrafish Cells. Cell. Physiol. Biochem. Int. J. Exp. Cell. Physiol. Biochem. Pharmacol. 2018, 46, 1159–1174. [Google Scholar] [CrossRef]
- Rutter, J.; Reick, M.; Wu, L.C.; McKnight, S.L. Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 2001, 293, 510–514. [Google Scholar] [CrossRef] [Green Version]
- Rey, G.; Valekunja, U.K.; Feeney, K.A.; Wulund, L.; Milev, N.B.; Stangherlin, A.; Ansel-Bollepalli, L.; Velagapudi, V.; O’Neill, J.S.; Reddy, A.B. The Pentose Phosphate Pathway Regulates the Circadian Clock. Cell Metab. 2016, 24, 462–473. [Google Scholar] [CrossRef] [Green Version]
- Wible, R.S.; Ramanathan, C.; Sutter, C.H.; Olesen, K.M.; Kensler, T.W.; Liu, A.C.; Sutter, T.R. NRF2 regulates core and stabilizing circadian clock loops, coupling redox and timekeeping in Mus musculus. eLife 2018, 7. [Google Scholar] [CrossRef] [Green Version]
- Mills, E.L.; Pierce, K.A.; Jedrychowski, M.P.; Garrity, R.; Winther, S.; Vidoni, S.; Yoneshiro, T.; Spinelli, J.B.; Lu, G.Z.; Kazak, L.; et al. Accumulation of succinate controls activation of adipose tissue thermogenesis. Nature 2018, 560, 102–106. [Google Scholar] [CrossRef] [PubMed]
- Chouchani, E.T.; Kazak, L.; Jedrychowski, M.P.; Lu, G.Z.; Erickson, B.K.; Szpyt, J.; Pierce, K.A.; Laznik-Bogoslavski, D.; Vetrivelan, R.; Clish, C.B.; et al. Mitochondrial ROS regulate thermogenic energy expenditure and sulfenylation of UCP1. Nature 2016, 532, 112–116. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rong, B.; Wu, Q.; Sun, C. Melatonin: A novel strategy for prevention of obesity and fat accumulation in peripheral organs through the improvements of circadian rhythms and antioxidative capacity. Melatonin Res. 2020, 3, 58–76. [Google Scholar] [CrossRef]
- Hacışevki, A.; Baba, B. An overview of melatonin as an antioxidant molecule: A biochemical approach. Melatonin Mol. Biol. Clin. Pharm. Approaches 2018, 59–85. [Google Scholar] [CrossRef] [Green Version]
- Tarocco, A.; Caroccia, N.; Morciano, G.; Wieckowski, M.R.; Ancora, G.; Garani, G.; Pinton, P. Melatonin as a master regulator of cell death and inflammation: Molecular mechanisms and clinical implications for newborn care. Cell Death Dis. 2019, 10, 317. [Google Scholar] [CrossRef] [Green Version]
- Fernandez Vazquez, G.; Reiter, R.J.; Agil, A. Melatonin increases brown adipose tissue mass and function in Zucker diabetic fatty rats: Implications for obesity control. J. Pineal Res. 2018, 64, e12472. [Google Scholar] [CrossRef]
- Jimenez-Aranda, A.; Fernandez-Vazquez, G.; Campos, D.; Tassi, M.; Velasco-Perez, L.; Tan, D.X.; Reiter, R.J.; Agil, A. Melatonin induces browning of inguinal white adipose tissue in Zucker diabetic fatty rats. J. Pineal Res. 2013, 55, 416–423. [Google Scholar] [CrossRef]
- Hatori, M.; Vollmers, C.; Zarrinpar, A.; DiTacchio, L.; Bushong, E.A.; Gill, S.; Leblanc, M.; Chaix, A.; Joens, M.; Fitzpatrick, J.A.; et al. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab. 2012, 15, 848–860. [Google Scholar] [CrossRef] [Green Version]
- Vollmers, C.; Gill, S.; DiTacchio, L.; Pulivarthy, S.R.; Le, H.D.; Panda, S. Time of feeding and the intrinsic circadian clock drive rhythms in hepatic gene expression. Proc. Natl. Acad. Sci. USA 2009, 106, 21453–21458. [Google Scholar] [CrossRef] [Green Version]
- Yamamuro, D.; Takahashi, M.; Nagashima, S.; Wakabayashi, T.; Yamazaki, H.; Takei, A.; Takei, S.; Sakai, K.; Ebihara, K.; Iwasaki, Y.; et al. Peripheral circadian rhythms in the liver and white adipose tissue of mice are attenuated by constant light and restored by time-restricted feeding. PLoS ONE 2020, 15, e0234439. [Google Scholar] [CrossRef]
- Oishi, K.; Kasamatsu, M.; Ishida, N. Gene- and tissue-specific alterations of circadian clock gene expression in streptozotocin-induced diabetic mice under restricted feeding. Biochem. Biophys. Res. Commun. 2004, 317, 330–334. [Google Scholar] [CrossRef] [PubMed]
- Damiola, F.; Le Minh, N.; Preitner, N.; Kornmann, B.; Fleury-Olela, F.; Schibler, U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000, 14, 2950–2961. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de Goede, P.; Sen, S.; Oosterman, J.E.; Foppen, E.; Jansen, R.; la Fleur, S.E.; Challet, E.; Kalsbeek, A. Differential effects of diet composition and timing of feeding behavior on rat brown adipose tissue and skeletal muscle peripheral clocks. Neurobiol. Sleep Circadian Rhythm. 2018, 4, 24–33. [Google Scholar] [CrossRef] [PubMed]
- Chaix, A.; Lin, T.; Le, H.D.; Chang, M.W.; Panda, S. Time-Restricted Feeding Prevents Obesity and Metabolic Syndrome in Mice Lacking a Circadian Clock. Cell Metab. 2019, 29, 303–319 e304. [Google Scholar] [CrossRef]
- Heilbronn, L.K.; Panda, S. Alternate-Day Fasting Gets a Safe Bill of Health. Cell Metab. 2019, 30, 411–413. [Google Scholar] [CrossRef]
- Heilbronn, L.K.; Civitarese, A.E.; Bogacka, I.; Smith, S.R.; Hulver, M.; Ravussin, E. Glucose tolerance and skeletal muscle gene expression in response to alternate day fasting. Obes. Res. 2005, 13, 574–581. [Google Scholar] [CrossRef]
- Hoddy, K.K.; Kroeger, C.M.; Trepanowski, J.F.; Barnosky, A.; Bhutani, S.; Varady, K.A. Meal timing during alternate day fasting: Impact on body weight and cardiovascular disease risk in obese adults. Obesity 2014, 22, 2524–2531. [Google Scholar] [CrossRef]
- Varady, K.A.; Bhutani, S.; Klempel, M.C.; Kroeger, C.M.; Trepanowski, J.F.; Haus, J.M.; Hoddy, K.K.; Calvo, Y. Alternate day fasting for weight loss in normal weight and overweight subjects: A randomized controlled trial. Nutr. J. 2013, 12, 146. [Google Scholar] [CrossRef] [Green Version]
- Liu, B.; Page, A.J.; Hatzinikolas, G.; Chen, M.; Wittert, G.A.; Heilbronn, L.K. Intermittent Fasting Improves Glucose Tolerance and Promotes Adipose Tissue Remodeling in Male Mice Fed a High-Fat Diet. Endocrinology 2019, 160, 169–180. [Google Scholar] [CrossRef] [Green Version]
- Móez Al-Islam, E.F.; Jahrami, H.A.; Obaideen, A.A.; Madkour, M.I. Impact of diurnal intermittent fasting during Ramadan on inflammatory and oxidative stress markers in healthy people: Systematic review and meta-analysis. J. Nutr. Intermed. Metab. 2019, 15, 18–26. [Google Scholar]
- BaHammam, A.; Alrajeh, M.; Albabtain, M.; Bahammam, S.; Sharif, M. Circadian pattern of sleep, energy expenditure, and body temperature of young healthy men during the intermittent fasting of Ramadan. Appetite 2010, 54, 426–429. [Google Scholar] [CrossRef] [PubMed]
- Madkour, M.I.; El-Serafi, A.T.; Jahrami, H.A.; Sherif, N.M.; Hassan, R.E.; Awadallah, S.; Faris, M.A.E. Ramadan diurnal intermittent fasting modulates SOD2, TFAM, Nrf2, and sirtuins (SIRT1, SIRT3) gene expressions in subjects with overweight and obesity. Diabetes Res. Clin. Pract. 2019, 155, 107801. [Google Scholar] [CrossRef] [PubMed]
- Zhao, L.; Hutchison, A.T.; Wittert, G.A.; Thompson, C.H.; Lange, K.; Liu, B.; Heilbronn, L.K. Intermittent Fasting Does Not Uniformly Impact Genes Involved in Circadian Regulation in Women with Obesity. Obesity 2020, 28 (Suppl. 1), S63–S67. [Google Scholar] [CrossRef] [PubMed]
- Desvergne, B.; Wahli, W. Peroxisome proliferator-activated receptors: Nuclear control of metabolism. Endocr. Rev. 1999, 20, 649–688. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kersten, S.; Desvergne, B.; Wahli, W. Roles of PPARs in health and disease. Nature 2000, 405, 421–424. [Google Scholar] [CrossRef] [PubMed]
- Lefebvre, P.; Chinetti, G.; Fruchart, J.C.; Staels, B. Sorting out the roles of PPAR alpha in energy metabolism and vascular homeostasis. J. Clin. Investig. 2006, 116, 571–580. [Google Scholar] [CrossRef] [Green Version]
- Braissant, O.; Foufelle, F.; Scotto, C.; Dauca, M.; Wahli, W. Differential expression of peroxisome proliferator-activated receptors (PPARs): Tissue distribution of PPAR-alpha, -beta, and -gamma in the adult rat. Endocrinology 1996, 137, 354–366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, X.; Downes, M.; Yu, R.T.; Bookout, A.L.; He, W.; Straume, M.; Mangelsdorf, D.J.; Evans, R.M. Nuclear receptor expression links the circadian clock to metabolism. Cell 2006, 126, 801–810. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.X.; Lee, C.H.; Tiep, S.; Yu, R.T.; Ham, J.; Kang, H.; Evans, R.M. Peroxisome-proliferator-activated receptor delta activates fat metabolism to prevent obesity. Cell 2003, 113, 159–170. [Google Scholar] [CrossRef] [Green Version]
- Kroon, T.; Harms, M.; Maurer, S.; Bonnet, L.; Alexandersson, I.; Lindblom, A.; Ahnmark, A.; Nilsson, D.; Gennemark, P.; O’Mahony, G.; et al. PPARgamma and PPARalpha synergize to induce robust browning of white fat in vivo. Mol. Metab. 2020, 36, 100964. [Google Scholar] [CrossRef]
- Chen, L.; Yang, G. PPARs Integrate the Mammalian Clock and Energy Metabolism. PPAR Res. 2014, 2014, 653017. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beltowski, J. Endogenous hydrogen sulfide in perivascular adipose tissue: Role in the regulation of vascular tone in physiology and pathology. Can. J. Physiol. Pharm. 2013, 91, 889–898. [Google Scholar] [CrossRef] [PubMed]
- Cai, J.; Shi, X.; Wang, H.; Fan, J.; Feng, Y.; Lin, X.; Yang, J.; Cui, Q.; Tang, C.; Xu, G.; et al. Cystathionine gamma lyase-hydrogen sulfide increases peroxisome proliferator-activated receptor gamma activity by sulfhydration at C139 site thereby promoting glucose uptake and lipid storage in adipocytes. Biochim. Biophys. Acta 2016, 1861, 419–429. [Google Scholar] [CrossRef] [PubMed]
- Charoensuksai, P.; Xu, W. PPARs in Rhythmic Metabolic Regulation and Implications in Health and Disease. PPAR Res 2010, 2010. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oishi, K.; Shirai, H.; Ishida, N. CLOCK is involved in the circadian transactivation of peroxisome-proliferator-activated receptor alpha (PPARalpha) in mice. Biochem. J. 2005, 386, 575–581. [Google Scholar] [CrossRef] [Green Version]
- Canaple, L.; Rambaud, J.; Dkhissi-Benyahya, O.; Rayet, B.; Tan, N.S.; Michalik, L.; Delaunay, F.; Wahli, W.; Laudet, V. Reciprocal regulation of brain and muscle Arnt-like protein 1 and peroxisome proliferator-activated receptor alpha defines a novel positive feedback loop in the rodent liver circadian clock. Mol. Endocrinol. 2006, 20, 1715–1727. [Google Scholar] [CrossRef] [Green Version]
- Kaneko, K.; Yamada, T.; Tsukita, S.; Takahashi, K.; Ishigaki, Y.; Oka, Y.; Katagiri, H. Obesity alters circadian expressions of molecular clock genes in the brainstem. Brain Res. 2009, 1263, 58–68. [Google Scholar] [CrossRef]
- Yang, G.; Jia, Z.; Aoyagi, T.; McClain, D.; Mortensen, R.M.; Yang, T. Systemic PPARgamma deletion impairs circadian rhythms of behavior and metabolism. PLoS ONE 2012, 7, e38117. [Google Scholar] [CrossRef] [Green Version]
- Gutman, R.; Barnea, M.; Haviv, L.; Chapnik, N.; Froy, O. Peroxisome proliferator-activated receptor alpha (PPARalpha) activation advances locomotor activity and feeding daily rhythms in mice. Int. J. Obes. 2012, 36, 1131–1134. [Google Scholar] [CrossRef] [Green Version]
- Shirai, H.; Oishi, K.; Kudo, T.; Shibata, S.; Ishida, N. PPARalpha is a potential therapeutic target of drugs to treat circadian rhythm sleep disorders. Biochem. Biophys. Res. Commun. 2007, 357, 679–682. [Google Scholar] [CrossRef]
- Wang, X.; Wang, Z.; Liu, J.Z.; Hu, J.X.; Chen, H.L.; Li, W.L.; Hai, C.X. Double antioxidant activities of rosiglitazone against high glucose-induced oxidative stress in hepatocyte. Toxicol. Vitr. Int. J. Publ. Assoc. BIBRA 2011, 25, 839–847. [Google Scholar] [CrossRef] [PubMed]
- Cheng, C.F.; Ku, H.C.; Lin, H. PGC-1alpha as a Pivotal Factor in Lipid and Metabolic Regulation. Int. J. Mol. Sci. 2018, 19, 3447. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, S.; Lin, J.D. Transcriptional control of circadian metabolic rhythms in the liver. Diabetes Obes. Metab. 2015, 17, 33–38. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, C.; Li, S.; Liu, T.; Borjigin, J.; Lin, J.D. Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 2007, 447, 477–481. [Google Scholar] [CrossRef]
- Grimaldi, B.; Sassone-Corsi, P. Circadian rhythms: Metabolic clockwork. Nature 2007, 447, 386–387. [Google Scholar] [CrossRef]
- Sonoda, J.; Mehl, I.R.; Chong, L.W.; Nofsinger, R.R.; Evans, R.M. PGC-1beta controls mitochondrial metabolism to modulate circadian activity, adaptive thermogenesis, and hepatic steatosis. Proc. Natl. Acad. Sci. USA 2007, 104, 5223–5228. [Google Scholar] [CrossRef] [Green Version]
- Tanno, M.; Sakamoto, J.; Miura, T.; Shimamoto, K.; Horio, Y. Nucleocytoplasmic shuttling of the NAD+-dependent histone deacetylase SIRT1. J. Biol. Chem. 2007, 282, 6823–6832. [Google Scholar] [CrossRef] [Green Version]
- Wood, J.G.; Rogina, B.; Lavu, S.; Howitz, K.; Helfand, S.L.; Tatar, M.; Sinclair, D. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 2004, 430, 686–689. [Google Scholar] [CrossRef]
- Donmez, G.; Guarente, L. Aging and disease: Connections to sirtuins. Aging Cell 2010, 9, 285–290. [Google Scholar] [CrossRef]
- Man, A.W.C.; Li, H.; Xia, N. The Role of Sirtuin1 in Regulating Endothelial Function, Arterial Remodeling and Vascular Aging. Front. Physiol. 2019, 10, 1173. [Google Scholar] [CrossRef] [Green Version]
- Gu, P.; Hui, H.; Vanhoutte, P.; Lam, K.; Xu, A. Deletion of SIRT1 in perivascular adipose tissue accelerates obesity-induced endothelial dysfunction. In Proceedings of the 1st ASCEPT-BPS Joint Scientific Meeting, Hong Kong, China, 19–21 May 2015. [Google Scholar]
- Minor, R.K.; Baur, J.A.; Gomes, A.P.; Ward, T.M.; Csiszar, A.; Mercken, E.M.; Abdelmohsen, K.; Shin, Y.K.; Canto, C.; Scheibye-Knudsen, M.; et al. SRT1720 improves survival and healthspan of obese mice. Sci. Rep. 2011, 1, 70. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, Y.; Li, J.; Xiao, N.; Wang, M.; Kou, J.; Qi, L.; Huang, F.; Liu, B.; Liu, K. Pharmacological activation of AMPK ameliorates perivascular adipose/endothelial dysfunction in a manner interdependent on AMPK and SIRT1. Pharm. Res. 2014, 89, 19–28. [Google Scholar] [CrossRef] [PubMed]
- Fleenor, B.S.; Eng, J.S.; Sindler, A.L.; Pham, B.T.; Kloor, J.D.; Seals, D.R. Superoxide signaling in perivascular adipose tissue promotes age-related artery stiffness. Aging Cell 2014, 13, 576–578. [Google Scholar] [CrossRef] [PubMed]
- Yoo, J.K.; Hwang, M.H.; Luttrell, M.J.; Kim, H.K.; Meade, T.H.; English, M.; Segal, M.S.; Christou, D.D. Higher levels of adiponectin in vascular endothelial cells are associated with greater brachial artery flow-mediated dilation in older adults. Exp. Gerontol. 2015, 63, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Qiao, L.; Shao, J. SIRT1 regulates adiponectin gene expression through Foxo1-C/enhancer-binding protein alpha transcriptional complex. J. Biol. Chem. 2006, 281, 39915–39924. [Google Scholar] [CrossRef] [Green Version]
- Masri, S.; Orozco-Solis, R.; Aguilar-Arnal, L.; Cervantes, M.; Sassone-Corsi, P. Coupling circadian rhythms of metabolism and chromatin remodelling. Diabetes Obes. Metab. 2015, 17, 17–22. [Google Scholar] [CrossRef] [Green Version]
- Asher, G.; Gatfield, D.; Stratmann, M.; Reinke, H.; Dibner, C.; Kreppel, F.; Mostoslavsky, R.; Alt, F.W.; Schibler, U. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 2008, 134, 317–328. [Google Scholar] [CrossRef] [Green Version]
- Bellet, M.M.; Nakahata, Y.; Boudjelal, M.; Watts, E.; Mossakowska, D.E.; Edwards, K.A.; Cervantes, M.; Astarita, G.; Loh, C.; Ellis, J.L. Pharmacological modulation of circadian rhythms by synthetic activators of the deacetylase SIRT1. Proc. Natl. Acad. Sci. USA 2013, 110, 3333–3338. [Google Scholar] [CrossRef] [Green Version]
- Belden, W.J.; Dunlap, J.C. SIRT1 is a circadian deacetylase for core clock components. Cell 2008, 134, 212–214. [Google Scholar] [CrossRef] [Green Version]
- Wang, R.H.; Zhao, T.; Cui, K.; Hu, G.; Chen, Q.; Chen, W.; Wang, X.W.; Soto-Gutierrez, A.; Zhao, K.; Deng, C.X. Negative reciprocal regulation between Sirt1 and Per2 modulates the circadian clock and aging. Sci. Rep. 2016, 6, 28633. [Google Scholar] [CrossRef]
- Ramsey, K.M.; Yoshino, J.; Brace, C.S.; Abrassart, D.; Kobayashi, Y.; Marcheva, B.; Hong, H.-K.; Chong, J.L.; Buhr, E.D.; Lee, C. Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 2009, 324, 651–654. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nakahata, Y.; Sahar, S.; Astarita, G.; Kaluzova, M.; Sassone-Corsi, P. Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 2009, 324, 654–657. [Google Scholar] [CrossRef] [PubMed]
- Sahar, S.; Masubuchi, S.; Eckel-Mahan, K.; Vollmer, S.; Galla, L.; Ceglia, N.; Masri, S.; Barth, T.K.; Grimaldi, B.; Oluyemi, O. Circadian control of fatty acid elongation by SIRT1 protein-mediated deacetylation of acetyl-coenzyme A synthetase 1. J. Biol. Chem. 2014, 289, 6091–6097. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galdieri, L.; Zhang, M.; Vancura, A. Regulation of acetyl-CoA homeostasis and global histone acetylation (942.1). FASEB J. 2014, 28, 942-1. [Google Scholar]
- Drazic, A.; Myklebust, L.M.; Ree, R.; Arnesen, T. The world of protein acetylation. Biochim. Biophys. Acta (BBA)-Proteins Proteom. 2016, 1864, 1372–1401. [Google Scholar] [CrossRef] [Green Version]
- Arany, Z.; Neinast, M. Branched Chain Amino Acids in Metabolic Disease. Curr. Diabetes Rep. 2018, 18, 76. [Google Scholar] [CrossRef]
- Drummond, G.R.; Selemidis, S.; Griendling, K.K.; Sobey, C.G. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 2011, 10, 453–471. [Google Scholar] [CrossRef] [Green Version]
- Li, F.; Yin, Y.; Tan, B.; Kong, X.; Wu, G. Leucine nutrition in animals and humans: mTOR signaling and beyond. Amino Acids 2011, 41, 1185–1193. [Google Scholar] [CrossRef]
- Saxton, R.A.; Sabatini, D.M. mTOR Signaling in Growth, Metabolism, and Disease. Cell 2017, 168, 960–976. [Google Scholar] [CrossRef] [Green Version]
- Zhenyukh, O.; Civantos, E.; Ruiz-Ortega, M.; Sanchez, M.S.; Vazquez, C.; Peiro, C.; Egido, J.; Mas, S. High concentration of branched-chain amino acids promotes oxidative stress, inflammation and migration of human peripheral blood mononuclear cells via mTORC1 activation. Free Radic. Biol. Med. 2017, 104, 165–177. [Google Scholar] [CrossRef]
- Cao, R.; Lee, B.; Cho, H.Y.; Saklayen, S.; Obrietan, K. Photic regulation of the mTOR signaling pathway in the suprachiasmatic circadian clock. Mol. Cell. Neurosci. 2008, 38, 312–324. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lipton, J.O.; Yuan, E.D.; Boyle, L.M.; Ebrahimi-Fakhari, D.; Kwiatkowski, E.; Nathan, A.; Guttler, T.; Davis, F.; Asara, J.M.; Sahin, M. The Circadian Protein BMAL1 Regulates Translation in Response to S6K1-Mediated Phosphorylation. Cell 2015, 161, 1138–1151. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dragert, K.; Bhattacharya, I.; Hall, M.N.; Humar, R.; Battegay, E.; Haas, E. Basal mTORC2 activity and expression of its components display diurnal variation in mouse perivascular adipose tissue. Biochem. Biophys. Res. Commun. 2016, 473, 317–322. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dragert, K.; Bhattacharya, I.; Pellegrini, G.; Seebeck, P.; Azzi, A.; Brown, S.A.; Georgiopoulou, S.; Held, U.; Blyszczuk, P.; Arras, M.; et al. Deletion of Rictor in brain and fat alters peripheral clock gene expression and increases blood pressure. Hypertension 2015, 66, 332–339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Y.; Dong, W.; Shao, J.; Wang, Y.; Zhou, M.; Sun, H. Branched-Chain Amino Acid Negatively Regulates KLF15 Expression via PI3K-AKT Pathway. Front. Physiol. 2017, 8, 853. [Google Scholar] [CrossRef] [Green Version]
- Matoba, K.; Lu, Y.; Zhang, R.; Chen, E.R.; Sangwung, P.; Wang, B.; Prosdocimo, D.A.; Jain, M.K. Adipose KLF15 Controls Lipid Handling to Adapt to Nutrient Availability. Cell Rep. 2017, 21, 3129–3140. [Google Scholar] [CrossRef]
- Standl, E. GLP-1 receptor agonists and cardiovascular outcomes: An updated synthesis. Lancet Diabetes Endocrinol. 2019, 7, 741–743. [Google Scholar] [CrossRef]
- Han, L.; Yu, Y.; Sun, X.; Wang, B. Exendin-4 directly improves endothelial dysfunction in isolated aortas from obese rats through the cAMP or AMPK–eNOS pathways. Diabetes Res. Clin. Pract. 2012, 97, 453–460. [Google Scholar] [CrossRef]
- Gil-Lozano, M.; Mingomataj, E.L.; Wu, W.K.; Ridout, S.A.; Brubaker, P.L. Circadian secretion of the intestinal hormone GLP-1 by the rodent L cell. Diabetes 2014, 63, 3674–3685. [Google Scholar] [CrossRef] [Green Version]
- Gil-Lozano, M.; Hunter, P.M.; Behan, L.A.; Gladanac, B.; Casper, R.F.; Brubaker, P.L. Short-term sleep deprivation with nocturnal light exposure alters time-dependent glucagon-like peptide-1 and insulin secretion in male volunteers. Am. J. Physiol. Endocrinol. Metab. 2016, 310, E41–E50. [Google Scholar] [CrossRef] [Green Version]
- Cantini, G.; Mannucci, E.; Luconi, M. Perspectives in GLP-1 Research: New Targets, New Receptors. Trends Endocrinol. Metab. 2016, 27, 427–438. [Google Scholar] [CrossRef]
- Han, F.; Hou, N.; Liu, Y.; Huang, N.; Pan, R.; Zhang, X.; Mao, E.; Sun, X. Liraglutide improves vascular dysfunction by regulating a cAMP-independent PKA-AMPK pathway in perivascular adipose tissue in obese mice. Biomed. Pharmacother. 2019, 120, 109537. [Google Scholar] [CrossRef] [PubMed]
- Trzaskalski, N.A.; Fadzeyeva, E.; Mulvihill, E.E. Dipeptidyl Peptidase-4 at the Interface Between Inflammation and Metabolism. Clin. Med. Insights Endocrinol Diabetes 2020, 13, 1179551420912972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alam, M.A.; Chowdhury, M.R.H.; Jain, P.; Sagor, M.A.T.; Reza, H.M. DPP-4 inhibitor sitagliptin prevents inflammation and oxidative stress of heart and kidney in two kidney and one clip (2K1C) rats. Diabetol. Metab. Syndr. 2015, 7, 107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, L.; Liu, J.; Tian, X.Y.; Wong, W.T.; Lau, C.W.; Xu, A.; Xu, G.; Ng, C.F.; Yao, X.; Gao, Y. Uncoupling protein-2 mediates DPP-4 inhibitor-induced restoration of endothelial function in hypertension through reducing oxidative stress. Antioxid. Redox Signal. 2014, 21, 1571–1581. [Google Scholar] [CrossRef] [Green Version]
- Kothny, W.; Foley, J.; Kozlovski, P.; Shao, Q.; Gallwitz, B.; Lukashevich, V. Improved glycaemic control with vildagliptin added to insulin, with or without metformin, in patients with type 2 diabetes mellitus. Diabetes Obes. Metab. 2013, 15, 252–257. [Google Scholar] [CrossRef]
- Salim, H.M.; Fukuda, D.; Higashikuni, Y.; Tanaka, K.; Hirata, Y.; Yagi, S.; Soeki, T.; Shimabukuro, M.; Sata, M. Teneligliptin, a dipeptidyl peptidase-4 inhibitor, attenuated pro-inflammatory phenotype of perivascular adipose tissue and inhibited atherogenesis in normoglycemic apolipoprotein-E-deficient mice. Vasc. Pharmacol. 2017, 96, 19–25. [Google Scholar] [CrossRef]
- Ahren, B. Dipeptidyl peptidase-4 inhibitors: Clinical data and clinical implications. Diabetes Care 2007, 30, 1344–1350. [Google Scholar] [CrossRef] [Green Version]
- Sufiun, A.; Rafiq, K.; Fujisawa, Y.; Rahman, A.; Mori, H.; Nakano, D.; Kobori, H.; Ohmori, K.; Masaki, T.; Kohno, M.; et al. Effect of dipeptidyl peptidase-4 inhibition on circadian blood pressure during the development of salt-dependent hypertension in rats. Hypertens Res. 2015, 38, 237–243. [Google Scholar] [CrossRef] [Green Version]
- Mihaylova, M.M.; Shaw, R.J. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell. Biol. 2011, 13, 1016–1023. [Google Scholar] [CrossRef]
- Um, J.H.; Pendergast, J.S.; Springer, D.A.; Foretz, M.; Viollet, B.; Brown, A.; Kim, M.K.; Yamazaki, S.; Chung, J.H. AMPK regulates circadian rhythms in a tissue- and isoform-specific manner. PLoS ONE 2011, 6, e18450. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, L.; Zhang, L.; Li, B.; Jiang, H.; Duan, Y.; Xie, Z.; Shuai, L.; Li, J.; Li, J. AMP-Activated Protein Kinase (AMPK) Regulates Energy Metabolism through Modulating Thermogenesis in Adipose Tissue. Front. Physiol. 2018, 9, 122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Almabrouk, T.A.; White, A.D.; Ugusman, A.B.; Skiba, D.S.; Katwan, O.J.; Alganga, H.; Guzik, T.J.; Touyz, R.M.; Salt, I.P.; Kennedy, S. High fat diet attenuates the anticontractile activity of aortic PVAT via a mechanism involving AMPK and reduced adiponectin secretion. Front. Physiol. 2018, 9, 51. [Google Scholar] [CrossRef] [PubMed]
- Jordan, S.D.; Lamia, K.A. AMPK at the crossroads of circadian clocks and metabolism. Mol. Cell Endocrinol. 2013, 366, 163–169. [Google Scholar] [CrossRef] [Green Version]
- Davies, S.P.; Carling, D.; Munday, M.R.; Hardie, D.G. Diurnal rhythm of phosphorylation of rat liver acetyl-CoA carboxylase by the AMP-activated protein kinase, demonstrated using freeze-clamping. Effects of high fat diets. Eur. J. Biochem. 1992, 203, 615–623. [Google Scholar] [CrossRef]
- Busino, L.; Bassermann, F.; Maiolica, A.; Lee, C.; Nolan, P.M.; Godinho, S.I.; Draetta, G.F.; Pagano, M. SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science 2007, 316, 900–904. [Google Scholar] [CrossRef] [Green Version]
- Eng, G.W.L.; Edison; Virshup, D.M. Site-specific phosphorylation of casein kinase 1 delta (CK1delta) regulates its activity towards the circadian regulator PER2. PLoS ONE 2017, 12, e0177834. [Google Scholar] [CrossRef] [Green Version]
- Barnea, M.; Haviv, L.; Gutman, R.; Chapnik, N.; Madar, Z.; Froy, O. Metformin affects the circadian clock and metabolic rhythms in a tissue-specific manner. Biochim. Biophys. Acta 2012, 1822, 1796–1806. [Google Scholar] [CrossRef] [Green Version]
- Vieira, E.; Nilsson, E.C.; Nerstedt, A.; Ormestad, M.; Long, Y.C.; Garcia-Roves, P.M.; Zierath, J.R.; Mahlapuu, M. Relationship between AMPK and the transcriptional balance of clock-related genes in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2008, 295, E1032–E1037. [Google Scholar] [CrossRef]
- Lamia, K.A.; Sachdeva, U.M.; DiTacchio, L.; Williams, E.C.; Alvarez, J.G.; Egan, D.F.; Vasquez, D.S.; Juguilon, H.; Panda, S.; Shaw, R.J.; et al. AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 2009, 326, 437–440. [Google Scholar] [CrossRef] [Green Version]
- Guo, Y.; Wang, Y. Targeting Endothelial SIRT1 for the Prevention of Arterial Aging. In Endothelial Dysfunction-Old Concepts and New Challenges; IntechOpen: London, UK, 2018. [Google Scholar]
- Förstermann, U.; Sessa, W.C. Nitric oxide synthases: Regulation and function. Eur. Heart J. 2011, 33, 829–837. [Google Scholar] [CrossRef] [Green Version]
- Fukai, T.; Siegfried, M.R.; Ushio-Fukai, M.; Cheng, Y.; Kojda, G.; Harrison, D.G. Regulation of the vascular extracellular superoxide dismutase by nitric oxide and exercise training. J. Clin. Investig. 2000, 105, 1631–1639. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wallerath, T.; Deckert, G.; Ternes, T.; Anderson, H.; Li, H.; Witte, K.; Förstermann, U. Resveratrol, a polyphenolic phytoalexin present in red wine, enhances expression and activity of endothelial nitric oxide synthase. Circulation 2002, 106, 1652–1658. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xia, N.; Strand, S.; Schlufter, F.; Siuda, D.; Reifenberg, G.; Kleinert, H.; Förstermann, U.; Li, H. Role of SIRT1 and FOXO factors in eNOS transcriptional activation by resveratrol. Nitric Oxide 2013, 32, 29–35. [Google Scholar] [CrossRef] [PubMed]
- Dimmeler, S.; Fleming, I.; Fisslthaler, B.; Hermann, C.; Busse, R.; Zeiher, A.M. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999, 399, 601–605. [Google Scholar] [CrossRef]
- Paschos, G.K.; FitzGerald, G.A. Circadian clocks and vascular function. Circ. Res. 2010, 106, 833–841. [Google Scholar] [CrossRef]
- Nernpermpisooth, N.; Qiu, S.; Mintz, J.D.; Suvitayavat, W.; Thirawarapan, S.; Rudic, D.R.; Fulton, D.J.; Stepp, D.W. Obesity alters the peripheral circadian clock in the aorta and microcirculation. Microcirculation 2015, 22, 257–266. [Google Scholar] [CrossRef] [Green Version]
- Kunieda, T.; Minamino, T.; Miura, K.; Katsuno, T.; Tateno, K.; Miyauchi, H.; Kaneko, S.; Bradfield, C.A.; FitzGerald, G.A.; Komuro, I. Reduced nitric oxide causes age-associated impairment of circadian rhythmicity. Circ. Res. 2008, 102, 607–614. [Google Scholar] [CrossRef] [Green Version]
- Viswambharan, H.; Carvas, J.M.; Antic, V.; Marecic, A.; Jud, C.; Zaugg, C.E.; Ming, X.F.; Montani, J.P.; Albrecht, U.; Yang, Z. Mutation of the circadian clock gene Per2 alters vascular endothelial function. Circulation 2007, 115, 2188–2195. [Google Scholar] [CrossRef] [Green Version]
- Tunctan, B.; Weigl, Y.; Dotan, A.; Peleg, L.; Zengil, H.; Ashkenazi, I.; Abacioglu, N. Circadian variation of nitric oxide synthase activity in mouse tissue. Chronobiol. Int. 2002, 19, 393–404. [Google Scholar] [CrossRef]
- Anea, C.B.; Cheng, B.; Sharma, S.; Kumar, S.; Caldwell, R.W.; Yao, L.; Ali, M.I.; Merloiu, A.M.; Stepp, D.W.; Black, S.M.; et al. Increased superoxide and endothelial NO synthase uncoupling in blood vessels of Bmal1-knockout mice. Circ. Res. 2012, 111, 1157–1165. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mastronardi, C.A.; Yu, W.H.; McCann, S.M. Resting and circadian release of nitric oxide is controlled by leptin in male rats. Proc. Natl. Acad. Sci. USA 2002, 99, 5721–5726. [Google Scholar] [CrossRef] [Green Version]
- Kriegsfeld, L.J.; Drazen, D.L.; Nelson, R.J. Circadian organization in male mice lacking the gene for endothelial nitric oxide synthase (eNOS-/-). J. Biol. Rhythm. 2001, 16, 142–148. [Google Scholar] [CrossRef] [PubMed]
- Arraj, M.; Lemmer, B. Endothelial nitric oxide is not involved in circadian rhythm generation of blood pressure: Experiments in wild-type C57 and eNOS knock-out mice under light-dark and free-run conditions. Chronobiol. Int. 2007, 24, 1231–1240. [Google Scholar] [CrossRef] [PubMed]
- Xia, N.; Förstermann, U.; Li, H. Effects of resveratrol on eNOS in the endothelium and the perivascular adipose tissue. Ann. N. Y. Acad. Sci. 2017, 1403, 132–141. [Google Scholar] [CrossRef] [Green Version]
- Galvin, V.B.; Barakat, H.; Kemeny, G.; Macdonald, K.G.; Pories, W.J.; Hickner, R.C. Endothelial nitric oxide synthase content in adipose tissue from obese and lean African American and white American women. Metabolism 2005, 54, 1368–1373. [Google Scholar] [CrossRef]
- Virdis, A.; Duranti, E.; Rossi, C.; Dell’Agnello, U.; Santini, E.; Anselmino, M.; Chiarugi, M.; Taddei, S.; Solini, A. Tumour necrosis factor-alpha participates on the endothelin-1/nitric oxide imbalance in small arteries from obese patients: Role of perivascular adipose tissue. Eur. Heart J. 2015, 36, 784–794. [Google Scholar] [CrossRef] [Green Version]
- Xia, N.; Weisenburger, S.; Koch, E.; Burkart, M.; Reifenberg, G.; Forstermann, U.; Li, H.G. Restoration of perivascular adipose tissue function in diet-induced obese mice without changing bodyweight. Br. J. Pharmacol. 2017, 174, 3443–3453. [Google Scholar] [CrossRef] [Green Version]
- Xia, N.; Horke, S.; Habermeier, A.; Closs, E.I.; Reifenberg, G.; Gericke, A.; Mikhed, Y.; Munzel, T.; Daiber, A.; Forstermann, U.; et al. Uncoupling of Endothelial Nitric Oxide Synthase in Perivascular Adipose Tissue of Diet-Induced Obese Mice. Arterioscler. Thromb. Vasc. Biol. 2016, 36, 78–85. [Google Scholar] [CrossRef] [Green Version]
- Kikuchi-Utsumi, K.; Gao, B.; Ohinata, H.; Hashimoto, M.; Yamamoto, N.; Kuroshima, A. Enhanced gene expression of endothelial nitric oxide synthase in brown adipose tissue during cold exposure. Am. J. Physiol. -Regul. Integr. Comp. Physiol. 2002, 282, R623–R626. [Google Scholar] [CrossRef] [Green Version]
- Csiszar, A.; Labinskyy, N.; Pinto, J.T.; Ballabh, P.; Zhang, H.; Losonczy, G.; Pearson, K.; De Cabo, R.; Pacher, P.; Zhang, C. Resveratrol induces mitochondrial biogenesis in endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 2009, 297, H13–H20. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gil-Ortega, M.; Stucchi, P.; Guzmán-Ruiz, R.; Cano, V.; Arribas, S.; González, M.C.; Ruiz-Gayo, M.; Fernández-Alfonso, M.S.; Somoza, B. Adaptative nitric oxide overproduction in perivascular adipose tissue during early diet-induced obesity. Endocrinology 2010, 151, 3299–3306. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, Y.; Li, L.; Shao, Y.; Bai, X.; Bai, T.; Huang, X. Methotrexate improves perivascular adipose tissue/endothelial dysfunction via activation of AMPK/eNOS pathway. Mol. Med. Rep. 2017, 15, 2353–2359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Gene Mutation/Knockout | Mice Phenotype | Effect on Circadian Rhythm and Oxidative Stress | Refs |
---|---|---|---|
Bmal1−/− driven by aP2 promoter | ↑ HFD-induced obesity ↑ HFD-induced adiposity ↑ plasma leptin level ↓ leptin signaling ↓ energy expenditure ↓ polysaturated fatty acids |
| [120] |
ClockΔ19 driven by aP2 promoter | ↑ young mortality rate ↓ rate of glucose tolerance | Not mentioned | [121] |
Bmal1−/− driven by UCP1 | ↓ PVAT-induced vasoconstriction | ↓ blood pressure during resting phase ↓ angiotensin and angiotensinogen levels in PVAT | [122] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Man, A.W.C.; Xia, N.; Li, H. Circadian Rhythm in Adipose Tissue: Novel Antioxidant Target for Metabolic and Cardiovascular Diseases. Antioxidants 2020, 9, 968. https://doi.org/10.3390/antiox9100968
Man AWC, Xia N, Li H. Circadian Rhythm in Adipose Tissue: Novel Antioxidant Target for Metabolic and Cardiovascular Diseases. Antioxidants. 2020; 9(10):968. https://doi.org/10.3390/antiox9100968
Chicago/Turabian StyleMan, Andy W. C., Ning Xia, and Huige Li. 2020. "Circadian Rhythm in Adipose Tissue: Novel Antioxidant Target for Metabolic and Cardiovascular Diseases" Antioxidants 9, no. 10: 968. https://doi.org/10.3390/antiox9100968
APA StyleMan, A. W. C., Xia, N., & Li, H. (2020). Circadian Rhythm in Adipose Tissue: Novel Antioxidant Target for Metabolic and Cardiovascular Diseases. Antioxidants, 9(10), 968. https://doi.org/10.3390/antiox9100968