The Regulation of Lipokines by Environmental Factors
Abstract
:1. Introduction
2. Adipose Tissue
3. Lipokines
3.1. Origin and Function of Lipokines
3.2. Palmitoleate (C16:1n7)
3.2.1. Discovery, Structure, and Synthesis of Palmitoleate
3.2.2. Endocrine Action of Palmitoleate
Palmitoleate Modulates De Novo Lipogenesis
Palmitoleate Improves Glucose Homeostasis and Insulin Sensitivity
Palmitoleate Decreases Cellular Stress and Inflammation
3.2.3. Exercise Regulation of Palmitoleate
3.3. Oxylipins
3.3.1. Discovery, Structure, and Synthesis of 12,13-diHOME
3.3.2. Exercise and Cold-Induced Adaptations are Mediated by the 12,13-Dihome
3.4. Fatty Acid Esters of Hydroxy Fatty Acids
3.4.1. Discovery, Structure, and Synthesis of FAHFAs
3.4.2. Methodological Identification of FAHFAs and PAHSAs
3.4.3. Endocrine Action of FAHFAs
4. Conclusions
Funding
Conflicts of Interest
References
- Efeyan, A.; Comb, W.C.; Sabatini, D.M. Nutrient-sensing mechanisms and pathways. Nature 2015, 517, 302–310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hardie, D.G. Energy sensing by the AMP-activated protein kinase and its effects on muscle metabolism. Proc. Nutr. Soc. 2011, 70, 92–99. [Google Scholar] [CrossRef] [PubMed]
- Steinberg, G.R. Role of the AMP-activated protein kinase in regulating fatty acid metabolism during exercise. Appl. Physiol. Nutr. Metab. 2009, 34, 315–322. [Google Scholar] [CrossRef] [PubMed]
- Rebelo-Marques, A.; De Sousa Lages, A.; Andrade, R.; Ribeiro, C.F.; Mota-Pinto, A.; Carrilho, F.; Espregueira-Mendes, J. Aging Hallmarks: The Benefits of Physical Exercise. Front. Endocrinol. (Lausanne) 2018, 9, 258. [Google Scholar] [CrossRef] [PubMed]
- Brychta, R.J.; Chen, K.Y. Cold-induced thermogenesis in humans. Eur. J. Clin. Nutr. 2017, 71, 345–352. [Google Scholar] [CrossRef] [PubMed]
- Stanford, K.I.; Goodyear, L.J. Exercise regulation of adipose tissue. Adipocyte 2016, 5, 153–162. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stanford, K.I.; Goodyear, L.J. Muscle-Adipose Tissue Cross Talk. Cold Spring Harb. Perspect. Med. 2018, 8. [Google Scholar] [CrossRef]
- Dewal, R.S.; Stanford, K.I. Effects of exercise on brown and beige adipocytes. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2018, 1864, 71–78. [Google Scholar] [CrossRef]
- Orava, J.; Nuutila, P.; Lidell, M.E.; Oikonen, V.; Noponen, T.; Viljanen, T.; Scheinin, M.; Taittonen, M.; Niemi, T.; Enerback, S.; et al. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 2011, 14, 272–279. [Google Scholar] [CrossRef]
- Lynes, M.D.; Tseng, Y.H. Deciphering adipose tissue heterogeneity. Ann. N. Y. Acad. Sci. 2018, 1411, 5–20. [Google Scholar] [CrossRef]
- Lynes, M.D.; Shamsi, F.; Sustarsic, E.G.; Leiria, L.O.; Wang, C.H.; Su, S.C.; Huang, T.L.; Gao, F.; Narain, N.R.; Chen, E.Y.; et al. Cold-Activated Lipid Dynamics in Adipose Tissue Highlights a Role for Cardiolipin in Thermogenic Metabolism. Cell Rep. 2018, 24, 781–790. [Google Scholar] [CrossRef] [PubMed] [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] [PubMed]
- Lehnig, A.C.; Dewal, R.S.; Baer, L.A.; Kitching, K.M.; Munoz, V.R.; Arts, P.J.; Sindeldecker, D.A.; May, F.J.; Lauritzen, H.; Goodyear, L.J.; et al. Exercise Training Induces Depot-Specific Adaptations to White and Brown Adipose Tissue. iScience 2019, 11, 425–439. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pischon, T.; Boeing, H.; Hoffmann, K.; Bergmann, M.; Schulze, M.B.; Overvad, K.; van der Schouw, Y.T.; Spencer, E.; Moons, K.G.; Tjonneland, A.; et al. General and abdominal adiposity and risk of death in Europe. N. Engl. J. Med. 2008, 359, 2105–2120. [Google Scholar] [CrossRef] [PubMed]
- Cohen, P.; Levy, J.D.; Zhang, Y.; Frontini, A.; Kolodin, D.P.; Svensson, K.J.; Lo, J.C.; Zeng, X.; Ye, L.; Khandekar, M.J.; et al. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell 2014, 156, 304–316. [Google Scholar] [CrossRef] [PubMed]
- Gesta, S.; Tseng, Y.H.; Kahn, C.R. Developmental origin of fat: Tracking obesity to its source. Cell 2007, 131, 242–256. [Google Scholar] [CrossRef] [PubMed]
- Hull, D. The structure and function of brown adipose tissue. Br. Med. Bull. 1966, 22, 92–96. [Google Scholar] [CrossRef] [PubMed]
- Arbuthnott, E. Brown adipose tissue: Structure and function. Proc. Nutr. Soc. 1989, 48, 177–182. [Google Scholar] [CrossRef]
- Cannon, B.; Nedergaard, J. Brown adipose tissue: Function and physiological significance. Physiol. Rev. 2004, 84, 277–359. [Google Scholar] [CrossRef]
- Cypess, A.M.; Lehman, S.; Williams, G.; Tal, I.; Rodman, D.; Goldfine, A.B.; Kuo, F.C.; Palmer, E.L.; Tseng, Y.H.; Doria, A.; et al. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 2009, 360, 1509–1517. [Google Scholar] [CrossRef]
- Leitner, B.P.; Huang, S.; Brychta, R.J.; Duckworth, C.J.; Baskin, A.S.; McGehee, S.; Tal, I.; Dieckmann, W.; Gupta, G.; Kolodny, G.M.; et al. Mapping of human brown adipose tissue in lean and obese young men. Proc. Natl. Acad. Sci. USA 2017, 114, 8649–8654. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Poekes, L.; Lanthier, N.; Leclercq, I.A. Brown adipose tissue: A potential target in the fight against obesity and the metabolic syndrome. Clin. Sci. (Lond.) 2015, 129, 933–949. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
- Kershaw, E.E.; Flier, J.S. Adipose tissue as an endocrine organ. J. Clin. Endocrinol. Metab. 2004, 89, 2548–2556. [Google Scholar] [CrossRef] [PubMed]
- Friedman, J.M. Leptin and the endocrine control of energy balance. Nat. Metab. 2019, 1, 754–764. [Google Scholar] [CrossRef]
- Lee, M.W.; Lee, M.; Oh, K.J. Adipose Tissue-Derived Signatures for Obesity and Type 2 Diabetes: Adipokines, Batokines and MicroRNAs. J. Clin. Med. 2019, 8. [Google Scholar] [CrossRef] [PubMed]
- MacDougald, O.A.; Burant, C.F. The rapidly expanding family of adipokines. Cell Metab. 2007, 6, 159–161. [Google Scholar] [CrossRef]
- Gross, R.W.; Han, X. Lipidomics at the interface of structure and function in systems biology. Chem. Biol. 2011, 18, 284–291. [Google Scholar] [CrossRef]
- Leiria, L.O.; Wang, C.H.; Lynes, M.D.; Yang, K.; Shamsi, F.; Sato, M.; Sugimoto, S.; Chen, E.Y.; Bussberg, V.; Narain, N.R.; et al. 12-Lipoxygenase Regulates Cold Adaptation and Glucose Metabolism by Producing the Omega-3 Lipid 12-HEPE from Brown Fat. Cell Metab. 2019, 30, 768–783. [Google Scholar] [CrossRef]
- Stanford, K.I.; Lynes, M.D.; Takahashi, H.; Baer, L.A.; Arts, P.J.; May, F.J.; Lehnig, A.C.; Middelbeek, R.J.W.; Richard, J.J.; So, K.; et al. 12,13-diHOME: An Exercise-Induced Lipokine that Increases Skeletal Muscle Fatty Acid Uptake. Cell Metab. 2018, 27, 1111–1120.e3. [Google Scholar] [CrossRef] [Green Version]
- Lynes, M.D.; Leiria, L.O.; Lundh, M.; Bartelt, A.; Shamsi, F.; Huang, T.L.; Takahashi, H.; Hirshman, M.F.; Schlein, C.; Lee, A.; et al. The cold-induced lipokine 12,13-diHOME promotes fatty acid transport into brown adipose tissue. Nat. Med. 2017, 23, 631–637. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cao, H.; Gerhold, K.; Mayers, J.R.; Wiest, M.M.; Watkins, S.M.; Hotamisligil, G.S. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 2008, 134, 933–944. [Google Scholar] [CrossRef] [PubMed]
- Yore, M.M.; Syed, I.; Moraes-Vieira, P.M.; Zhang, T.; Herman, M.A.; Homan, E.A.; Patel, R.T.; Lee, J.; Chen, S.; Peroni, O.D.; et al. Discovery of a class of endogenous mammalian lipids with anti-diabetic and anti-inflammatory effects. Cell 2014, 159, 318–332. [Google Scholar] [CrossRef] [PubMed]
- Yilmaz, M.; Claiborn, K.C.; Hotamisligil, G.S. De Novo Lipogenesis Products and Endogenous Lipokines. Diabetes 2016, 65, 1800–1807. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuda, O.; Brezinova, M.; Rombaldova, M.; Slavikova, B.; Posta, M.; Beier, P.; Janovska, P.; Veleba, J.; Kopecky, J., Jr.; Kudova, E.; et al. Docosahexaenoic Acid-Derived Fatty Acid Esters of Hydroxy Fatty Acids (FAHFAs) with Anti-inflammatory Properties. Diabetes 2016, 65, 2580–2590. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Burhans, M.S.; Flowers, M.T.; Ntambi, J.M. Hepatic oleate regulates liver stress response partially through PGC-1alpha during high-carbohydrate feeding. J. Hepatol. 2016, 65, 103–112. [Google Scholar] [CrossRef]
- Burhans, M.S.; Flowers, M.T.; Harrington, K.R.; Bond, L.M.; Guo, C.A.; Anderson, R.M.; Ntambi, J.M. Hepatic oleate regulates adipose tissue lipogenesis and fatty acid oxidation. J. Lipid Res. 2015, 56, 304–318. [Google Scholar] [CrossRef] [Green Version]
- ALJohani, A.M.; Syed, D.N.; Ntambi, J.M. Insights into Stearoyl-CoA Desaturase-1 Regulation of Systemic Metabolism. Trends Endocrinol. Metab. 2017, 28, 831–842. [Google Scholar] [CrossRef]
- Imamura, F.; Micha, R.; Wu, J.H.; de Oliveira Otto, M.C.; Otite, F.O.; Abioye, A.I.; Mozaffarian, D. Effects of Saturated Fat, Polyunsaturated Fat, Monounsaturated Fat, and Carbohydrate on Glucose-Insulin Homeostasis: A Systematic Review and Meta-analysis of Randomised Controlled Feeding Trials. PLoS Med. 2016, 13, e1002087. [Google Scholar] [CrossRef]
- Olefsky, J.M. Fat talks, liver and muscle listen. Cell 2008, 134, 914–916. [Google Scholar] [CrossRef]
- Maeda, K.; Cao, H.; Kono, K.; Gorgun, C.Z.; Furuhashi, M.; Uysal, K.T.; Cao, Q.; Atsumi, G.; Malone, H.; Krishnan, B.; et al. Adipocyte/macrophage fatty acid binding proteins control integrated metabolic responses in obesity and diabetes. Cell Metab. 2005, 1, 107–119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Newberry, E.P.; Xie, Y.; Kennedy, S.M.; Luo, J.; Davidson, N.O. Protection against Western diet-induced obesity and hepatic steatosis in liver fatty acid-binding protein knockout mice. Hepatology 2006, 44, 1191–1205. [Google Scholar] [CrossRef]
- Frigolet, M.E.; Gutierrez-Aguilar, R. The Role of the Novel Lipokine Palmitoleic Acid in Health and Disease. Adv. Nutr. 2017, 8, 173S–181S. [Google Scholar] [CrossRef] [PubMed]
- Guillocheau, E.; Garcia, C.; Drouin, G.; Richard, L.; Catheline, D.; Legrand, P.; Rioux, V. Retroconversion of dietary trans-vaccenic (trans-C18:1 n-7) acid to trans-palmitoleic acid (trans-C16:1 n-7): Proof of concept and quantification in both cultured rat hepatocytes and pregnant rats. J. Nutr. Biochem. 2018, 63, 19–26. [Google Scholar] [CrossRef]
- Senagolage, M.D.; Sommars, M.A.; Ramachandran, K.; Futtner, C.R.; Omura, Y.; Allred, A.L.; Wang, J.; Yang, C.; Procissi, D.; Evans, R.M.; et al. Loss of Transcriptional Repression by BCL6 Confers Insulin Sensitivity in the Setting of Obesity. Cell Rep. 2018, 25, 3283–3298.e6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fatima, T.; Snyder, C.L.; Schroeder, W.R.; Cram, D.; Datla, R.; Wishart, D.; Weselake, R.J.; Krishna, P. Fatty acid composition of developing sea buckthorn (Hippophae rhamnoides L.) berry and the transcriptome of the mature seed. PLoS ONE 2012, 7, e34099. [Google Scholar] [CrossRef] [PubMed]
- Sambanthamurthi, R.; Parman, S.H.; Noor, M.R.M. Oil palm (Elaeis guineensis) protoplasts: Isolation, culture and microcallus formation. Plant Cell Tissue Organ 1996, 46, 35–41. [Google Scholar] [CrossRef]
- Yakoob, M.Y.; Shi, P.; Hu, F.B.; Campos, H.; Rexrode, K.M.; Orav, E.J.; Willett, W.C.; Mozaffarian, D. Circulating biomarkers of dairy fat and risk of incident stroke in U.S. men and women in 2 large prospective cohorts. Am. J. Clin. Nutr. 2014, 100, 1437–1447. [Google Scholar] [CrossRef] [Green Version]
- Mozaffarian, D.; de Oliveira Otto, M.C.; Lemaitre, R.N.; Fretts, A.M.; Hotamisligil, G.; Tsai, M.Y.; Siscovick, D.S.; Nettleton, J.A. trans-Palmitoleic acid, other dairy fat biomarkers, and incident diabetes: The Multi-Ethnic Study of Atherosclerosis (MESA). Am. J. Clin. Nutr. 2013, 97, 854–861. [Google Scholar] [CrossRef]
- Micha, R.; King, I.B.; Lemaitre, R.N.; Rimm, E.B.; Sacks, F.; Song, X.; Siscovick, D.S.; Mozaffarian, D. Food sources of individual plasma phospholipid trans fatty acid isomers: The Cardiovascular Health Study. Am. J. Clin. Nutr. 2010, 91, 883–893. [Google Scholar] [CrossRef]
- Mozaffarian, D.; Cao, H.; King, I.B.; Lemaitre, R.N.; Song, X.; Siscovick, D.S.; Hotamisligil, G.S. Circulating palmitoleic acid and risk of metabolic abnormalities and new-onset diabetes. Am. J. Clin. Nutr. 2010, 92, 1350–1358. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McLaren, D.S.; Ajans, Z.A.; Awdeh, Z. Composition of human adipose tissue, with special reference to site and age differences. Am. J. Clin. Nutr. 1965, 17, 171–176. [Google Scholar] [CrossRef] [PubMed]
- Yli-Jama, P.; Haugen, T.S.; Rebnord, H.M.; Ringstad, J.; Pedersen, J.I. Selective mobilisation of fatty acids from human adipose tissue. Eur. J. Intern. Med. 2001, 12, 107–115. [Google Scholar] [CrossRef]
- Hirsch, J.; Farquhar, J.W.; Ahrens, E.H., Jr.; Peterson, M.L.; Stoffel, W. Studies of adipose tissue in man. A microtechnic for sampling and analysis. Am. J. Clin. Nutr. 1960, 8, 499–511. [Google Scholar] [CrossRef] [PubMed]
- Bolsoni-Lopes, A.; Festuccia, W.T.; Farias, T.S.; Chimin, P.; Torres-Leal, F.L.; Derogis, P.B.; de Andrade, P.B.; Miyamoto, S.; Lima, F.B.; Curi, R.; et al. Palmitoleic acid (n-7) increases white adipocyte lipolysis and lipase content in a PPARalpha-dependent manner. Am. J. Physiol. Endocrinol. Metab. 2013, 305, E1093–E1102. [Google Scholar] [CrossRef] [PubMed]
- Fernandez, C.; Schuhmann, K.; Herzog, R.; Fielding, B.; Frayn, K.; Shevchenko, A.; James, P.; Holm, C.; Strom, K. Altered desaturation and elongation of fatty acids in hormone-sensitive lipase null mice. PLoS ONE 2011, 6, e21603. [Google Scholar] [CrossRef]
- Yang, Z.H.; Miyahara, H.; Hatanaka, A. Chronic administration of palmitoleic acid reduces insulin resistance and hepatic lipid accumulation in KK-Ay Mice with genetic type 2 diabetes. Lipids Health Dis. 2011, 10, 120. [Google Scholar] [CrossRef]
- Diakogiannaki, E.; Dhayal, S.; Childs, C.E.; Calder, P.C.; Welters, H.J.; Morgan, N.G. Mechanisms involved in the cytotoxic and cytoprotective actions of saturated versus monounsaturated long-chain fatty acids in pancreatic beta-cells. J. Endocrinol. 2007, 194, 283–291. [Google Scholar] [CrossRef]
- Bolsoni-Lopes, A.; Festuccia, W.T.; Chimin, P.; Farias, T.S.; Torres-Leal, F.L.; Cruz, M.M.; Andrade, P.B.; Hirabara, S.M.; Lima, F.B.; Alonso-Vale, M.I. Palmitoleic acid (n-7) increases white adipocytes GLUT4 content and glucose uptake in association with AMPK activation. Lipids Health Dis. 2014, 13, 199. [Google Scholar] [CrossRef] [Green Version]
- Cruz, M.M.; Lopes, A.B.; Crisma, A.R.; de Sa, R.C.C.; Kuwabara, W.M.T.; Curi, R.; de Andrade, P.B.M.; Alonso-Vale, M.I.C. Palmitoleic acid (16:1n7) increases oxygen consumption, fatty acid oxidation and ATP content in white adipocytes. Lipids Health Dis. 2018, 17, 55. [Google Scholar] [CrossRef]
- Lehnig, A.C.; Stanford, K.I. Exercise-induced adaptations to white and brown adipose tissue. J. Exp. Biol. 2018, 221. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Snijder, M.B.; Dekker, J.M.; Visser, M.; Bouter, L.M.; Stehouwer, C.D.; Kostense, P.J.; Yudkin, J.S.; Heine, R.J.; Nijpels, G.; Seidell, J.C. Associations of hip and thigh circumferences independent of waist circumference with the incidence of type 2 diabetes: The Hoorn Study. Am. J. Clin. Nutr. 2003, 77, 1192–1197. [Google Scholar] [CrossRef] [PubMed]
- Misra, A.; Garg, A.; Abate, N.; Peshock, R.M.; Stray-Gundersen, J.; Grundy, S.M. Relationship of anterior and posterior subcutaneous abdominal fat to insulin sensitivity in nondiabetic men. Obes. Res. 1997, 5, 93–99. [Google Scholar] [CrossRef] [PubMed]
- Stanford, K.I.; Middelbeek, R.J.; Townsend, K.L.; Lee, M.Y.; Takahashi, H.; So, K.; Hitchcox, K.M.; Markan, K.R.; Hellbach, K.; Hirshman, M.F.; et al. A novel role for subcutaneous adipose tissue in exercise-induced improvements in glucose homeostasis. Diabetes 2015, 64, 2002–2014. [Google Scholar] [CrossRef] [PubMed]
- Pinnick, K.E.; Neville, M.J.; Fielding, B.A.; Frayn, K.N.; Karpe, F.; Hodson, L. Gluteofemoral adipose tissue plays a major role in production of the lipokine palmitoleate in humans. Diabetes 2012, 61, 1399–1403. [Google Scholar] [CrossRef] [PubMed]
- Stefan, N.; Kantartzis, K.; Celebi, N.; Staiger, H.; Machann, J.; Schick, F.; Cegan, A.; Elcnerova, M.; Schleicher, E.; Fritsche, A.; et al. Circulating palmitoleate strongly and independently predicts insulin sensitivity in humans. Diabetes Care 2010, 33, 405–407. [Google Scholar] [CrossRef] [PubMed]
- Gong, J.; Campos, H.; McGarvey, S.; Wu, Z.; Goldberg, R.; Baylin, A. Adipose tissue palmitoleic acid and obesity in humans: Does it behave as a lipokine? Am. J. Clin. Nutr. 2011, 93, 186–191. [Google Scholar] [CrossRef]
- Bergman, B.C.; Howard, D.; Schauer, I.E.; Maahs, D.M.; Snell-Bergeon, J.K.; Clement, T.W.; Eckel, R.H.; Perreault, L.; Rewers, M. The importance of palmitoleic acid to adipocyte insulin resistance and whole-body insulin sensitivity in type 1 diabetes. J. Clin. Endocrinol. Metab. 2013, 98, E40–E50. [Google Scholar] [CrossRef]
- Matsuzaka, T.; Shimano, H.; Yahagi, N.; Kato, T.; Atsumi, A.; Yamamoto, T.; Inoue, N.; Ishikawa, M.; Okada, S.; Ishigaki, N.; et al. Crucial role of a long-chain fatty acid elongase, Elovl6, in obesity-induced insulin resistance. Nat. Med. 2007, 13, 1193–1202. [Google Scholar] [CrossRef]
- de Souza, C.O.; Teixeira, A.A.S.; Biondo, L.A.; Lima Junior, E.A.; Batatinha, H.A.P.; Rosa Neto, J.C. Palmitoleic Acid Improves Metabolic Functions in Fatty Liver by PPARalpha-Dependent AMPK Activation. J. Cell. Physiol. 2017, 232, 2168–2177. [Google Scholar] [CrossRef]
- Kuda, O.; Stankova, B.; Tvrzicka, E.; Hensler, M.; Jelenik, T.; Rossmeisl, M.; Flachs, P.; Kopecky, J. Prominent role of liver in elevated plasma palmitoleate levels in response to rosiglitazone in mice fed high-fat diet. J. Physiol. Pharm. 2009, 60, 135–140. [Google Scholar]
- Mensink, R.P.; de Groot, M.J.; van den Broeke, L.T.; Severijnen-Nobels, A.P.; Demacker, P.N.; Katan, M.B. Effects of monounsaturated fatty acids v complex carbohydrates on serum lipoproteins and apoproteins in healthy men and women. Metabolism 1989, 38, 172–178. [Google Scholar] [CrossRef]
- Vessby, B.; Uusitupa, M.; Hermansen, K.; Riccardi, G.; Rivellese, A.A.; Tapsell, L.C.; Nalsen, C.; Berglund, L.; Louheranta, A.; Rasmussen, B.M.; et al. Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: The KANWU Study. Diabetologia 2001, 44, 312–319. [Google Scholar] [CrossRef] [PubMed]
- Baer, D.J.; Judd, J.T.; Clevidence, B.A.; Tracy, R.P. Dietary fatty acids affect plasma markers of inflammation in healthy men fed controlled diets: A randomized crossover study. Am. J. Clin. Nutr. 2004, 79, 969–973. [Google Scholar] [CrossRef] [PubMed]
- Esposito, K.; Marfella, R.; Ciotola, M.; Di Palo, C.; Giugliano, F.; Giugliano, G.; D’Armiento, M.; D’Andrea, F.; Giugliano, D. Effect of a mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: A randomized trial. JAMA 2004, 292, 1440–1446. [Google Scholar] [CrossRef] [PubMed]
- van Dijk, S.J.; Feskens, E.J.; Bos, M.B.; Hoelen, D.W.; Heijligenberg, R.; Bromhaar, M.G.; de Groot, L.C.; de Vries, J.H.; Muller, M.; Afman, L.A. A saturated fatty acid-rich diet induces an obesity-linked proinflammatory gene expression profile in adipose tissue of subjects at risk of metabolic syndrome. Am. J. Clin. Nutr. 2009, 90, 1656–1664. [Google Scholar] [CrossRef] [PubMed]
- Shaw, B.; Lambert, S.; Wong, M.H.; Ralston, J.C.; Stryjecki, C.; Mutch, D.M. Individual saturated and monounsaturated fatty acids trigger distinct transcriptional networks in differentiated 3T3-L1 preadipocytes. J. Nutr. Nutr. 2013, 6, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Kadotani, A.; Tsuchiya, Y.; Hatakeyama, H.; Katagiri, H.; Kanzaki, M. Different impacts of saturated and unsaturated free fatty acids on COX-2 expression in C(2)C(12) myotubes. Am. J. Physiol. Endocrinol. Metab. 2009, 297, E1291–E1303. [Google Scholar] [CrossRef] [PubMed]
- Talbot, N.A.; Wheeler-Jones, C.P.; Cleasby, M.E. Palmitoleic acid prevents palmitic acid-induced macrophage activation and consequent p38 MAPK-mediated skeletal muscle insulin resistance. Mol. Cell. Endocrinol. 2014, 393, 129–142. [Google Scholar] [CrossRef] [PubMed]
- Macrae, K.; Stretton, C.; Lipina, C.; Blachnio-Zabielska, A.; Baranowski, M.; Gorski, J.; Marley, A.; Hundal, H.S. Defining the role of DAG, mitochondrial function, and lipid deposition in palmitate-induced proinflammatory signaling and its counter-modulation by palmitoleate. J. Lipid Res. 2013, 54, 2366–2378. [Google Scholar] [CrossRef] [Green Version]
- Duckett, S.K.; Volpi-Lagreca, G.; Alende, M.; Long, N.M. Palmitoleic acid reduces intramuscular lipid and restores insulin sensitivity in obese sheep. Diabetes Metab. Syndr. Obes. 2014, 7, 553–563. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akazawa, Y.; Cazanave, S.; Mott, J.L.; Elmi, N.; Bronk, S.F.; Kohno, S.; Charlton, M.R.; Gores, G.J. Palmitoleate attenuates palmitate-induced Bim and PUMA up-regulation and hepatocyte lipoapoptosis. J. Hepatol. 2010, 52, 586–593. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Welters, H.J.; Tadayyon, M.; Scarpello, J.H.; Smith, S.A.; Morgan, N.G. Mono-unsaturated fatty acids protect against beta-cell apoptosis induced by saturated fatty acids, serum withdrawal or cytokine exposure. FEBS Lett. 2004, 560, 103–108. [Google Scholar] [CrossRef]
- Welters, H.J.; Diakogiannaki, E.; Mordue, J.M.; Tadayyon, M.; Smith, S.A.; Morgan, N.G. Differential protective effects of palmitoleic acid and cAMP on caspase activation and cell viability in pancreatic beta-cells exposed to palmitate. Apoptosis 2006, 11, 1231–1238. [Google Scholar] [CrossRef] [PubMed]
- Nemcova-Furstova, V.; James, R.F.; Kovar, J. Inhibitory effect of unsaturated fatty acids on saturated fatty acid-induced apoptosis in human pancreatic beta-cells: Activation of caspases and ER stress induction. Cell. Physiol. Biochem. 2011, 27, 525–538. [Google Scholar] [CrossRef]
- Cimen, I.; Kocaturk, B.; Koyuncu, S.; Tufanli, O.; Onat, U.I.; Yildirim, A.D.; Apaydin, O.; Demirsoy, S.; Aykut, Z.G.; Nguyen, U.T.; et al. Prevention of atherosclerosis by bioactive palmitoleate through suppression of organelle stress and inflammasome activation. Sci. Transl. Med. 2016, 8, 358ra126. [Google Scholar] [CrossRef] [PubMed]
- Cimen, I.; Yildirim, Z.; Dogan, A.E.; Yildirim, A.D.; Tufanlı, Ö.; Onat, U.I.; Nguyen, U.; Watkins, S.M.; Weber, C.; Erbay, E. Double Bond Configuration of Palmitoleate is Critical For Atheroprotection. Mol. Metab. 2019, 28, 58–72. [Google Scholar] [CrossRef]
- Rohm, M.; Savic, D.; Ball, V.; Curtis, M.K.; Bonham, S.; Fischer, R.; Legrave, N.; MacRae, J.I.; Tyler, D.J.; Ashcroft, F.M. Cardiac Dysfunction and Metabolic Inflexibility in a Mouse Model of Diabetes without Dyslipidemia. Diabetes 2018, 67, 1057–1067. [Google Scholar] [CrossRef]
- de Souza, C.O.; Valenzuela, C.A.; Baker, E.J.; Miles, E.A.; Rosa Neto, J.C.; Calder, P.C. Palmitoleic Acid has Stronger Anti-Inflammatory Potential in Human Endothelial Cells Compared to Oleic and Palmitic Acids. Mol. Nutr. Food Res. 2018, 62, e1800322. [Google Scholar] [CrossRef]
- Da Silva, M.S.; Julien, P.; Bilodeau, J.F.; Barbier, O.; Rudkowska, I. Trans Fatty Acids Suppress TNF-alpha-Induced Inflammatory Gene Expression in Endothelial (HUVEC) and Hepatocellular Carcinoma (HepG2) Cells. Lipids 2017, 52, 315–325. [Google Scholar] [CrossRef]
- Da Silva, M.S.; Bilodeau, J.F.; Larose, J.; Greffard, K.; Julien, P.; Barbier, O.; Rudkowska, I. Modulation of the biomarkers of inflammation and oxidative stress by ruminant trans fatty acids and dairy proteins in vascular endothelial cells (HUVEC). Prostaglandins Leukot. Essent. Fat. Acids 2017, 126, 64–71. [Google Scholar] [CrossRef] [PubMed]
- Staiger, K.; Staiger, H.; Weigert, C.; Haas, C.; Haring, H.U.; Kellerer, M. Saturated, but not unsaturated, fatty acids induce apoptosis of human coronary artery endothelial cells via nuclear factor-kappaB activation. Diabetes 2006, 55, 3121–3126. [Google Scholar] [CrossRef] [PubMed]
- Pedersen, B.K.; Febbraio, M.A. Muscles, exercise and obesity: Skeletal muscle as a secretory organ. Nat. Rev. Endocrinol. 2012, 8, 457–465. [Google Scholar] [CrossRef] [PubMed]
- Febbraio, M.A. Exercise metabolism in 2016: Health benefits of exercise-more than meets the eye! Nat. Rev. Endocrinol. 2017, 13, 72–74. [Google Scholar] [CrossRef] [PubMed]
- Mul, J.D.; Stanford, K.I.; Hirshman, M.F.; Goodyear, L.J. Exercise and Regulation of Carbohydrate Metabolism. Prog. Mol. Biol. Transl. Sci. 2015, 135, 17–37. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hayashi, T.; Wojtaszewski, J.F.; Goodyear, L.J. Exercise regulation of glucose transport in skeletal muscle. Am. J. Physiol. 1997, 273, E1039–E1051. [Google Scholar] [CrossRef] [PubMed]
- Stanford, K.I.; Middelbeek, R.J.; Goodyear, L.J. Exercise Effects on White Adipose Tissue: Beiging and Metabolic Adaptations. Diabetes 2015, 64, 2361–2368. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Foryst-Ludwig, A.; Kreissl, M.C.; Benz, V.; Brix, S.; Smeir, E.; Ban, Z.; Januszewicz, E.; Salatzki, J.; Grune, J.; Schwanstecher, A.K.; et al. Adipose Tissue Lipolysis Promotes Exercise-induced Cardiac Hypertrophy Involving the Lipokine C16:1n7-Palmitoleate. J. Biol. Chem. 2015, 290, 23603–23615. [Google Scholar] [CrossRef] [Green Version]
- Rocha-Rodrigues, S.; Rodriguez, A.; Goncalves, I.O.; Moreira, A.; Maciel, E.; Santos, S.; Domingues, M.R.; Fruhbeck, G.; Ascensao, A.; Magalhaes, J. Impact of physical exercise on visceral adipose tissue fatty acid profile and inflammation in response to a high-fat diet regimen. Int. J. Biochem. Cell Biol. 2017, 87, 114–124. [Google Scholar] [CrossRef]
- Kawanishi, N.; Takagi, K.; Lee, H.C.; Nakano, D.; Okuno, T.; Yokomizo, T.; Machida, S. Endurance exercise training and high-fat diet differentially affect composition of diacylglycerol molecular species in rat skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2018, 314, R892–R901. [Google Scholar] [CrossRef] [Green Version]
- Mukwevho, E.; Joseph, J.S. Calmodulin dependent protein kinase II activation by exercise regulates saturated & unsaturated fatty acids and improves some metabolic syndrome markers. Life Sci. 2014, 111, 53–61. [Google Scholar] [CrossRef] [PubMed]
- de Souza, C.O.; Vannice, G.K.; Rosa Neto, J.C.; Calder, P.C. Is Palmitoleic Acid a Plausible Nonpharmacological Strategy to Prevent or Control Chronic Metabolic and Inflammatory Disorders? Mol. Nutr. Food Res. 2018, 62. [Google Scholar] [CrossRef] [PubMed]
- Diakogiannaki, E.; Welters, H.J.; Morgan, N.G. Differential regulation of the endoplasmic reticulum stress response in pancreatic beta-cells exposed to long-chain saturated and monounsaturated fatty acids. J. Endocrinol. 2008, 197, 553–563. [Google Scholar] [CrossRef] [PubMed]
- Diakogiannaki, E.; Morgan, N.G. Differential regulation of the ER stress response by long-chain fatty acids in the pancreatic beta-cell. Biochem. Soc. Trans. 2008, 36, 959–962. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Yang, J.; Qi, W.; Yang, H.; Wang, C.; Tan, B.; Hammock, B.D.; Park, Y.; Kim, D.; Zhang, G. Lipidomic profiling of high-fat diet-induced obesity in mice: Importance of cytochrome P450-derived fatty acid epoxides. Obesity (Silver Spring) 2017, 25, 132–140. [Google Scholar] [CrossRef] [PubMed]
- Schuchardt, J.P.; Schmidt, S.; Kressel, G.; Dong, H.; Willenberg, I.; Hammock, B.D.; Hahn, A.; Schebb, N.H. Comparison of free serum oxylipin concentrations in hyper- vs. normolipidemic men. Prostaglandins Leukot. Essent. Fat. Acids 2013, 89, 19–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nieman, D.C.; Shanely, R.A.; Luo, B.; Meaney, M.P.; Dew, D.A.; Pappan, K.L. Metabolomics approach to assessing plasma 13- and 9-hydroxy-octadecadienoic acid and linoleic acid metabolite responses to 75-km cycling. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2014, 307, R68–R74. [Google Scholar] [CrossRef] [PubMed]
- Pauls, S.D.; Rodway, L.A.; Winter, T.; Taylor, C.G.; Zahradka, P.; Aukema, H.M. Anti-inflammatory effects of alpha-linolenic acid in M1-like macrophages are associated with enhanced production of oxylipins from alpha-linolenic and linoleic acid. J. Nutr. Biochem. 2018, 57, 121–129. [Google Scholar] [CrossRef]
- Wang, Y.M.; Liu, H.X.; Fang, N.Y. 9-PAHSA promotes browning of white fat via activating G-protein-coupled receptor 120 and inhibiting lipopolysaccharide/NF-kappa B pathway. Biochem. Biophys. Res. Commun. 2018, 506, 153–160. [Google Scholar] [CrossRef]
- Tan, D.; Ertunc, M.E.; Konduri, S.; Zhang, J.; Pinto, A.M.; Chu, Q.; Kahn, B.B.; Siegel, D.; Saghatelian, A. Discovery of FAHFA-Containing Triacylglycerols and Their Metabolic Regulation. J. Am. Chem. Soc. 2019, 141, 8798–8806. [Google Scholar] [CrossRef]
- Moraes-Vieira, P.M.; Saghatelian, A.; Kahn, B.B. GLUT4 Expression in Adipocytes Regulates De Novo Lipogenesis and Levels of a Novel Class of Lipids with Antidiabetic and Anti-inflammatory Effects. Diabetes 2016, 65, 1808–1815. [Google Scholar] [CrossRef] [PubMed]
- Herman, M.A.; Peroni, O.D.; Villoria, J.; Schon, M.R.; Abumrad, N.A.; Bluher, M.; Klein, S.; Kahn, B.B. A novel ChREBP isoform in adipose tissue regulates systemic glucose metabolism. Nature 2012, 484, 333–338. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hammarstedt, A.; Syed, I.; Vijayakumar, A.; Eliasson, B.; Gogg, S.; Kahn, B.B.; Smith, U. Adipose tissue dysfunction is associated with low levels of the novel Palmitic Acid Hydroxystearic Acids. Sci. Rep. 2018, 8, 15757. [Google Scholar] [CrossRef] [PubMed]
- Vijayakumar, A.; Aryal, P.; Wen, J.; Syed, I.; Vazirani, R.P.; Moraes-Vieira, P.M.; Camporez, J.P.; Gallop, M.R.; Perry, R.J.; Peroni, O.D.; et al. Absence of Carbohydrate Response Element Binding Protein in Adipocytes Causes Systemic Insulin Resistance and Impairs Glucose Transport. Cell Rep. 2017, 21, 1021–1035. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Syed, I.; de Celis, M.F.R.; Mohan, J.F.; Moraes-Vieira, P.M.; Vijayakumar, A.; Nelson, A.T.; Siegel, D.; Saghatelian, A.; Mathis, D.; Kahn, B.B. PAHSAs attenuate immune responses and promote beta cell survival in autoimmune diabetic mice. J. Clin. Investig. 2019, 129, 3717–3731. [Google Scholar] [CrossRef] [PubMed]
- Syed, I.; Lee, J.; Moraes-Vieira, P.M.; Donaldson, C.J.; Sontheimer, A.; Aryal, P.; Wellenstein, K.; Kolar, M.J.; Nelson, A.T.; Siegel, D.; et al. Palmitic Acid Hydroxystearic Acids Activate GPR40, Which Is Involved in Their Beneficial Effects on Glucose Homeostasis. Cell Metab. 2018, 27, 419–427.e4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, P.; Santoro, A.; Peroni, O.D.; Nelson, A.T.; Saghatelian, A.; Siegel, D.; Kahn, B.B. PAHSAs enhance hepatic and systemic insulin sensitivity through direct and indirect mechanisms. J. Clin. Investig. 2019, 129, 4138–4150. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.; Moraes-Vieira, P.M.; Castoldi, A.; Aryal, P.; Yee, E.U.; Vickers, C.; Parnas, O.; Donaldson, C.J.; Saghatelian, A.; Kahn, B.B. Branched Fatty Acid Esters of Hydroxy Fatty Acids (FAHFAs) Protect against Colitis by Regulating Gut Innate and Adaptive Immune Responses. J. Biol. Chem. 2016, 291, 22207–22217. [Google Scholar] [CrossRef] [Green Version]
- Gabbs, M.; Leng, S.; Devassy, J.G.; Monirujjaman, M.; Aukema, H.M. Advances in Our Understanding of Oxylipins Derived from Dietary PUFAs. Adv. Nutr. 2015, 6, 513–540. [Google Scholar] [CrossRef] [Green Version]
- Nayeem, M.A. Role of oxylipins in cardiovascular diseases. Acta Pharm. Sin. 2018, 39, 1142–1154. [Google Scholar] [CrossRef]
- Barnard, N.D. Trends in food availability, 1909–2007. Am. J. Clin. Nutr. 2010, 91, 1530S–1536S. [Google Scholar] [CrossRef] [PubMed]
- Itoh, T.; Fairall, L.; Amin, K.; Inaba, Y.; Szanto, A.; Balint, B.L.; Nagy, L.; Yamamoto, K.; Schwabe, J.W. Structural basis for the activation of PPARgamma by oxidized fatty acids. Nat. Struct. Mol. Biol. 2008, 15, 924–931. [Google Scholar] [CrossRef] [PubMed]
- Wu, M.V.; Bikopoulos, G.; Hung, S.; Ceddia, R.B. Thermogenic capacity is antagonistically regulated in classical brown and white subcutaneous fat depots by high fat diet and endurance training in rats: Impact on whole-body energy expenditure. J. Biol. Chem. 2014, 289, 34129–34140. [Google Scholar] [CrossRef] [PubMed]
- Vosselman, M.J.; Hoeks, J.; Brans, B.; Pallubinsky, H.; Nascimento, E.B.; van der Lans, A.A.; Broeders, E.P.; Mottaghy, F.M.; Schrauwen, P.; van Marken Lichtenbelt, W.D. Low brown adipose tissue activity in endurance-trained compared with lean sedentary men. Int. J. Obes. (Lond) 2015, 39, 1696–1702. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Motiani, P.; Virtanen, K.A.; Motiani, K.K.; Eskelinen, J.J.; Middelbeek, R.J.; Goodyear, L.J.; Savolainen, A.M.; Kemppainen, J.; Jensen, J.; Din, M.U.; et al. Decreased insulin-stimulated brown adipose tissue glucose uptake after short-term exercise training in healthy middle-aged men. Diabetes Obes. Metab. 2017, 19, 1379–1388. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kolar, M.J.; Kamat, S.S.; Parsons, W.H.; Homan, E.A.; Maher, T.; Peroni, O.D.; Syed, I.; Fjeld, K.; Molven, A.; Kahn, B.B.; et al. Branched Fatty Acid Esters of Hydroxy Fatty Acids Are Preferred Substrates of the MODY8 Protein Carboxyl Ester Lipase. Biochemistry 2016, 55, 4636–4641. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuda, O.; Brezinova, M.; Silhavy, J.; Landa, V.; Zidek, V.; Dodia, C.; Kreuchwig, F.; Vrbacky, M.; Balas, L.; Durand, T.; et al. Nrf2-Mediated Antioxidant Defense and Peroxiredoxin 6 Are Linked to Biosynthesis of Palmitic Acid Ester of 9-Hydroxystearic Acid. Diabetes 2018, 67, 1190–1199. [Google Scholar] [CrossRef] [Green Version]
- Abel, E.D.; Peroni, O.; Kim, J.K.; Kim, Y.B.; Boss, O.; Hadro, E.; Minnemann, T.; Shulman, G.I.; Kahn, B.B. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 2001, 409, 729–733. [Google Scholar] [CrossRef]
- Pflimlin, E.; Bielohuby, M.; Korn, M.; Breitschopf, K.; Lohn, M.; Wohlfart, P.; Konkar, A.; Podeschwa, M.; Barenz, F.; Pfenninger, A.; et al. Acute and Repeated Treatment with 5-PAHSA or 9-PAHSA Isomers Does Not Improve Glucose Control in Mice. Cell Metab. 2018, 28, 217–227.e13. [Google Scholar] [CrossRef] [Green Version]
- Kuda, O. On the Complexity of PAHSA Research. Cell Metab. 2018, 28, 541–542. [Google Scholar] [CrossRef] [Green Version]
- Syed, I.; Lee, J.; Peroni, O.D.; Yore, M.M.; Moraes-Vieira, P.M.; Santoro, A.; Wellenstein, K.; Smith, U.; McGraw, T.E.; Saghatelian, A.; et al. Methodological Issues in Studying PAHSA Biology: Masking PAHSA Effects. Cell Metab. 2018, 28, 543–546. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kolar, M.J.; Nelson, A.T.; Chang, T.; Ertunc, M.E.; Christy, M.P.; Ohlsson, L.; Harrod, M.; Kahn, B.B.; Siegel, D.; Saghatelian, A. Faster Protocol for Endogenous Fatty Acid Esters of Hydroxy Fatty Acid (FAHFA) Measurements. Anal. Chem. 2018, 90, 5358–5365. [Google Scholar] [CrossRef] [PubMed]
- Brezinova, M.; Kuda, O.; Hansikova, J.; Rombaldova, M.; Balas, L.; Bardova, K.; Durand, T.; Rossmeisl, M.; Cerna, M.; Stranak, Z.; et al. Levels of palmitic acid ester of hydroxystearic acid (PAHSA) are reduced in the breast milk of obese mothers. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2018, 1863, 126–131. [Google Scholar] [CrossRef]
- Ma, Y.; Kind, T.; Vaniya, A.; Gennity, I.; Fahrmann, J.F.; Fiehn, O. An in silico MS/MS library for automatic annotation of novel FAHFA lipids. J. Cheminform. 2015, 7, 53. [Google Scholar] [CrossRef] [PubMed]
- Zhang, T.; Chen, S.; Syed, I.; Stahlman, M.; Kolar, M.J.; Homan, E.A.; Chu, Q.; Smith, U.; Boren, J.; Kahn, B.B.; et al. A LC-MS-based workflow for measurement of branched fatty acid esters of hydroxy fatty acids. Nat. Protoc. 2016, 11, 747–763. [Google Scholar] [CrossRef]
- Zhu, Q.F.; Yan, J.W.; Zhang, T.Y.; Xiao, H.M.; Feng, Y.Q. Comprehensive Screening and Identification of Fatty Acid Esters of Hydroxy Fatty Acids in Plant Tissues by Chemical Isotope Labeling-Assisted Liquid Chromatography-Mass Spectrometry. Anal. Chem. 2018, 90, 10056–10063. [Google Scholar] [CrossRef]
- Hirasawa, A.; Tsumaya, K.; Awaji, T.; Katsuma, S.; Adachi, T.; Yamada, M.; Sugimoto, Y.; Miyazaki, S.; Tsujimoto, G. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat. Med. 2005, 11, 90–94. [Google Scholar] [CrossRef] [PubMed]
- Bandak, B.; Yi, L.; Roper, M.G. Microfluidic-enabled quantitative measurements of insulin release dynamics from single islets of Langerhans in response to 5-palmitic acid hydroxy stearic acid. Lab Chip 2018, 18, 2873–2882. [Google Scholar] [CrossRef]
Lipokine | Source | Target Tissue | References |
---|---|---|---|
Palmitoleate | Dietary (salmon, cod liver oil, dairy products, and macadamia oil) Endogenous synthesis (mainly WAT) | WAT | [32,43,45,52,53,55,56,59,60,65,77,98,99] |
Liver | [32,57,70,71,82,102] | ||
Pancreas | [58,83,84,85,103,104] | ||
Endothelial cells | [80,85,87,89,90,91,92,98,102] | ||
Immune cells | [79,85,87] | ||
Muscle | [32,78,81,100,101] | ||
12,13-diHOME | Dietary (sunflower, safflower, soybean, corn, and canola oils as well as nuts and seeds) Endogenous synthesis (mainly BAT) | BAT | [30,31,105] |
Muscle | [30,106,107] | ||
Immune cells | [108] | ||
FAHFAs | Dietary (olive oil, Arabidopsis thaliana, rice) Endogenous synthesis (mainly WAT and BAT) | WAT | [33,35,109,110,111,112,113,114] |
Pancreas | [115,116] | ||
Liver | [117] | ||
Intestine (colon) | [118] | ||
Immune cells | [35] |
© 2019 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
Hernández-Saavedra, D.; Stanford, K.I. The Regulation of Lipokines by Environmental Factors. Nutrients 2019, 11, 2422. https://doi.org/10.3390/nu11102422
Hernández-Saavedra D, Stanford KI. The Regulation of Lipokines by Environmental Factors. Nutrients. 2019; 11(10):2422. https://doi.org/10.3390/nu11102422
Chicago/Turabian StyleHernández-Saavedra, Diego, and Kristin I. Stanford. 2019. "The Regulation of Lipokines by Environmental Factors" Nutrients 11, no. 10: 2422. https://doi.org/10.3390/nu11102422