Gene Expression of Sirtuin-1 and Endogenous Secretory Receptor for Advanced Glycation End Products in Healthy and Slightly Overweight Subjects after Caloric Restriction and Resveratrol Administration
Abstract
1. Introduction
2. Materials and Methods
2.1. Interventions
2.2. Laboratory Tests
2.3. Sirt-1 and RAGE Expression
2.4. Statistical Analysis
3. Results
4. Discussion
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Haigis, M.C.; Sinclair, D.A. Mammalian sirtuins: Biological insights and disease relevance. Annu. Rev. Pathol. 2010, 5, 253–295. [Google Scholar] [CrossRef] [PubMed]
- Ristow, M.; Zarse, K. How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis). Exp. Gerontol. 2010, 45, 410–418. [Google Scholar] [CrossRef] [PubMed]
- Nisoli, E.; Tonello, C.; Cardile, A.; Cozzi, V.; Bracale, R.; Tedesco, L.; Falcone, S.; Valerio, A.; Cantoni, O.; Clementi, E.; et al. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 2005, 310, 314–317. [Google Scholar] [CrossRef] [PubMed]
- Nemoto, S.; Fergusson, M.M.; Finkel, T. Nutrient availability regulates SIRT1 through a fork head dependent pathway. Science 2004, 306, 2105–2108. [Google Scholar] [CrossRef] [PubMed]
- Lagouge, M.; Argmann, C.; Gerhart-Hines, Z.; Meziane, H.; Lerin, C.; Daussin, F.; Messadeq, N.; Milne, J.; Lambert, P.; Elliott, P.; et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α. Cell 2006, 127, 1109–1122. [Google Scholar] [CrossRef] [PubMed]
- Mariani, S.; Fiore, D.; Persichetti, A.; Basciani, S.; Lubrano, C.; Poggiogalle, E.; Genco, A.; Donini, L.M.; Gnessi, L. Circulating SIRT1 Increases After Intragastric Balloon Fat Loss in Obese Patients. Obes. Surg. 2016, 26, 1215–1220. [Google Scholar] [CrossRef] [PubMed]
- Mansur, A.P.; Roggerio, A.; Goes, M.F.; Avakian, S.D.; Leal, D.P.; Maranhão, R.C.; Strunz, C.M. Serum concentrations and gene expression of sirtuin 1 in healthy and slightly overweight subjects after caloric restriction or resveratrol supplementation: A randomized trial. Int. J. Cardiol. 2017, 15, 788–794. [Google Scholar] [CrossRef] [PubMed]
- Kitada, M.; Kume, S.; Takeda-Watanabe, A.; Tsuda, S.; Kanasaki, K.; Koya, D. Calorie restriction in overweight males ameliorates obesity-related metabolic alterations and cellular adaptations through anti-aging effects, possibly including AMPK and SIRT1 activation. Biochim. Biophys. Acta 2013, 1830, 4820–4827. [Google Scholar] [CrossRef] [PubMed]
- Ota, H.; Akishita, M.; Eto, M.; Iijima, K.; Kaneki, M.; Ouchi, Y. Sirt1 modulates premature senescence-like phenotype in human endothelial cells. J. Mol. Cell. Cardiol. 2007, 43, 571–579. [Google Scholar] [CrossRef] [PubMed]
- Brett, J.; Schmidt, A.M.; Yan, S.D.; Zou, Y.S.; Weidman, E.; Pinsky, D.; Nowygrod, R.; Neeper, M.; Przysiecki, C.; Shaw, A.; et al. Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am. J. Pathol. 1993, 143, 1699–1712. [Google Scholar] [PubMed]
- Vlassara, H.; Cai, W.; Crandall, J.; Goldberg, T.; Oberstein, R.; Dardaine, V.; Peppa, M.; Rayfield, E.J. Inflammatory mediators are induced by dietary glycotoxins, a major risk factor for diabetic angiopathy. Proc. Natl. Acad. Sci. USA 2002, 99, 15596–15601. [Google Scholar] [CrossRef] [PubMed]
- Uribarri, J.; Woodruff, S.; Goodman, S.; Cai, W.; Chen, X.; Pyzik, R.; Yong, A.; Striker, G.E.; Vlassara, H. Advanced glycation end products in foods and a practical guide to their reduction in the diet. J. Am. Diet. Assoc. 2010, 110, 911–916. [Google Scholar] [CrossRef] [PubMed]
- Schmidt, A.M.; Yan, S.D.; Wautier, J.L.; Stern, D. Activation of receptor for advanced glycation end products: A mechanism for chronic vascular dysfunction in diabetic vasculopathy and atherosclerosis. Circ. Res. 1999, 84, 489–497. [Google Scholar] [CrossRef] [PubMed]
- De Kreutzenberg, S.V.; Ceolotto, G.; Papparella, I.; Bortoluzzi, A.; Semplicini, A.; Dalla Man, C.; Cobelli, C.; Fadini, G.P.; Avogaro, A. Downregulation of the longevity-associated protein SIRT1 in insulin resistance and metabolic syndrome. Potential biochemical mechanisms. Diabetes 2010, 59, 1006–1015. [Google Scholar] [CrossRef] [PubMed]
- Hudson, B.I.; Carter, A.M.; Harja, E.; Kalea, A.Z.; Arriero, M.; Yang, H.; Grant, P.J.; Schmidt, A.M. Identification, classification, and expression of RAGE gene splice variants. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2008, 22, 1572–1580. [Google Scholar] [CrossRef] [PubMed]
- Falcone, C.; Emanuele, E.; D’Angelo, A.; Buzzi, M.P.; Belvito, C.; Cuccia, M.; Geroldi, D. Plasma levels of soluble receptor for advanced glycation end products and coronary artery disease in non-diabetic men. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 1032–1037. [Google Scholar] [CrossRef] [PubMed]
- Selvin, E.; Halushka, M.K.; Rawlings, A.M.; Hoogeveen, R.C.; Ballantyne, C.M.; Coresh, J.; Astor, B.C. sRAGE and risk of diabetes, cardiovascular disease, and death. Diabetes 2013, 62, 2116–2121. [Google Scholar] [CrossRef] [PubMed]
- Mulrennan, S.; Baltic, S.; Aggarwal, S.; Wood, J.; Miranda, A.; Frost, F.; Kaye, J.; Thompson, P.J. The role of receptor for advanced glycation end products in airway inflammation in CF and CF related diabetes. Sci. Rep. 2015, 10, 8931. [Google Scholar] [CrossRef] [PubMed]
- Lan, Y.Y.; Peterson, C.M.; Ravussin, E. Resveratrol vs. calorie restriction: Data from rodents to humans. Exp. Gerontol. 2013, 48, 1018–1024. [Google Scholar] [CrossRef]
- Howitz, K.T.; Bitterman, K.J.; Cohen, H.Y.; Lamming, D.W.; Lavu, S.; Wood, J.G.; Zipkin, R.E.; Chung, P.; Kisielewski, A.; Zhang, L.L.; et al. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 425, 191–196. [Google Scholar] [CrossRef] [PubMed]
- Barger, J.L. An adipocentric perspective of resveratrol as a calorie restriction mimetic. Ann. N. Y. Acad. Sci. 2013, 1290, 122–129. [Google Scholar] [CrossRef] [PubMed]
- Park, S.; Yoon, S.J.; Tae, H.J.; Shin, C.Y. RAGE and cardiovascular disease. Front. Biosci. 2001, 16, 486–497. [Google Scholar]
- Basta, G. Receptor of advanced glycation end products and atherosclerosis: From basis mechanisms to clinal implications. Atherosclerosis 2008, 196, 9–21. [Google Scholar] [CrossRef] [PubMed]
- Kalea, A.Z.; See, F.; Harja, E.; Arriero, M.; Schmidt, A.M.; Hudson, B.I. Alternatively spliced RAGEv1 inhibits tumorigenesis through suppression of JNK signaling. Cancer Res. 2010, 70, 5628–5638. [Google Scholar] [CrossRef] [PubMed]
- Bierhaus, A.; Humpert, P.M.; Morcos, M.; Wendt, T.; Chavakis, T.; Arnold, B.; Stern, D.M.; Nawroth, P.P. Understanding RAGE, the receptor for advanced glycation end products. J. Mol. Med. 2005, 83, 876–886. [Google Scholar] [CrossRef] [PubMed]
- Yonekura, H.; Yamamoto, Y.; Sakurai, S.; Petrova, R.G.; Abedin, M.J.; Li, H.; Yasui, K.; Takeuchi, M.; Makita, Z.; Takasawa, S.; et al. Novel splice variants of the receptor for advanced glycation end-products expressed in human vascular endothelial cells and pericytes, and their putative roles in diabetes-induced vascular injury. Biochem. J. 2003, 15, 1097–1109. [Google Scholar] [CrossRef] [PubMed]
- Kierdof, K.; Fritz, G. RAGE regulation and signaling in inflammation and beyond. J. Leukoc. Biol. 2013, 94, 55–68. [Google Scholar] [CrossRef] [PubMed]
- Di Pino, A.; Urbano, F.; Zagami, R.M.; Filippello, A.; Di Mauro, S.; Piro, S.; Purrello, F.; Rabuazzo, A.M. Low endogenous secretory receptor for advanced glycation end-products levels are associated with inflammation and carotid atherosclerosis in prediabetes. J. Clin. Endocrinol. Metab. 2016, 101, 1701–1709. [Google Scholar] [CrossRef] [PubMed]
- Di Pino, A.; Mangiafico, S.; Urbano, F.; Scicali, R.; Scandura, S.; D’Agate, V.; Piro, S.; Tamburino, C.; Purrello, F.; Rabuazzo, A.M. HbA1c Identifies Subjects with Prediabetes and Subclinical Left Ventricular Diastolic Dysfunction. J. Clin. Endocrinol. Metab. 2017, 102, 3756–3764. [Google Scholar] [CrossRef] [PubMed]
- Aris, J.P.; Elios, M.C.; Bimstein, E.; Wallet, S.M.; Cha, S.; Lakshmyya, K.N.; Katz, J. Gingival RAGE expression in calorie-restricted versus ad libitum-fed rats. J. Periodontol. 2010, 81, 1481–1487. [Google Scholar] [CrossRef] [PubMed]
- Moridi, H.; Karimi, J.; Sheikh, N.; Goodarzi, M.T.; Saidijam, M.; Yadegarazari, R.; Khazaei, M.; Khodadadi, I.; Tavilani, H.; Piri, H.; et al. Resveratrol-dependent down-regulation of receptor for advanced glycation end-products and oxidative stress in kidney of rats with diabetes. Int. J. Endocrinol. Metab. 2015, 13, e23542. [Google Scholar] [CrossRef] [PubMed]
- Busch, A.; Hertel, K.J. Evolution of SR protein and hnRNP splicing regulatory factors. Wiley Interdiscip. Rev. RNA 2012, 3, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.Y.; Li, H.L.; Su, J.B.; Ding, F.H.; Zhao, J.J.; Chai, F.; Li, Y.X.; Cui, S.C.; Sun, F.Y.; Wu, Z.Y.; et al. Regulation of RAGE splicing by hnRNP A1 and Tra2β-1 and its potential role in AD pathogenesis. J. Neurochem. 2015, 133, 187–198. [Google Scholar] [CrossRef] [PubMed]
- Holly, A.C.; Melzer, D.; Pilling, L.C.; Fellows, A.C.; Tanaka, T.; Ferrucci, L.; Harries, L.W. Changes in splicing factor expression are associated with advancing age in man. Mech. Ageing Dev. 2013, 134, 356–366. [Google Scholar] [CrossRef] [PubMed]
- Baker, D.J.; Childs, B.G.; Durik, M.; Wijers, M.E.; Sieben, C.J.; Zhong, J.; Saltness, R.A.; Jeganathan, K.B.; Verzosa, G.C.; Pezeshki, A.; et al. Naturally occurring p16(Ink4a)-positive cells shorten healthy lifespan. Nature 2016, 530, 184–189. [Google Scholar] [CrossRef] [PubMed]
- Markus, M.A.; Marques, F.Z.; Morris, B.J. Resveratrol, by modulating RNA processing factor levels, can influence the alternative splicing of pre-mRNAs. PLoS ONE 2011, 6, e28926. [Google Scholar] [CrossRef] [PubMed]
- Evankovich, J.; Lear, T.; Mckelvey, A.; Dunn, S.; Londino, J.; Liu, Y.; Chen, B.B.; Mallampalli, R.K. Receptor for advanced glycation end products is targeted by FBXO10 for ubiquitination and degradation. FASEB J. 2017, 31, 3894–3903. [Google Scholar] [CrossRef] [PubMed]
- Quade-Lyssy, P.; Kanarek, A.M.; Baiersdörfer, M.; Postina, R.; Kojro, E. Statins stimulate the production of a soluble form of the receptor for advanced glycation end products. J. Lipid Res. 2013, 54, 3052–3061. [Google Scholar] [CrossRef] [PubMed]
- Pullerits, R.; Bokarewa, M.; Dahlberg, L.; Tarkowski, A. Decreased levels of soluble receptor for advanced glycation end products in patients with rheumatoid arthritis indicating deficient inflammatory control. Arthritis Res. Ther. 2005, 7, R817–R824. [Google Scholar] [CrossRef] [PubMed]
- Haddad, M.; Knani, I.; Bouzidi, H.; Berriche, O.; Hammami, M.; Kerkeni, M. Plasma Levels of Pentosidine, Carboxymethyl-Lysine, Soluble Receptor for Advanced Glycation End Products, and Metabolic Syndrome: The Metformin Effect. Dis. Markers 2016, 2016, 6248264. [Google Scholar] [CrossRef] [PubMed]
- Koyama, H.; Tanaka, S.; Monden, M.; Shoji, T.; Morioka, T.; Fukumoto, S.; Mori, K.; Emoto, M.; Shoji, T.; Fukui, M.; et al. Comparison of effects of pioglitazone and glimepiride on plasma soluble RAGE and RAGE expression in peripheral mononuclear cells in type 2 diabetes: Randomized controlled trial (PioRAGE). Atherosclerosis 2014, 234, 329–334. [Google Scholar] [CrossRef] [PubMed]
Resveratrol | Caloric Restriction | |||||
---|---|---|---|---|---|---|
Baseline n = 24 | 30 days n = 24 | p | Baseline n = 24 | 30 days n = 24 | p | |
Age, years | 58.46 ± 3.44 | 58.63 ± 3.65 | ||||
Weight, kg | 83.01 ± 21.88 | 91.14 ± 17.77 | 0.328 | 69.13 ± 7.99 | 64.60 ± 7.30 | 0.002 |
Body mass index, kg/m2 | 27.61 ± 4.24 | 27.79 ± 4.38 | 0.370 | 25.84 ± 3.22 | 25.50 ± 3.21 | 0.083 |
Waist circumference, cm | 96.82 ± 12.08 | 96.90 ± 11.36 | 0.457 | 94.27 ± 7.50 | 91.82 ± 7.12 | 0.011 |
Heart rate, bpm | 64.61 ± 8.46 | 65.65 ± 8.22 | 0.269 | 62.50 ± 9.60 | 62.32 ± 10.51 | 0.902 |
Systolic BP, mmHg | 131.46 ± 15.48 | 128.95 ± 15.44 | 0.660 | 129.73 ± 15.65 | 124.23 ± 12.81 | 0.109 |
Diastolic BP, mmHg | 81.21 ± 10.81 | 81.95 ± 9.22 | 0.612 | 82.86 ± 10.96 | 79.36 ± 9.92 | 0.070 |
Total cholesterol, mmol/L | 5.38 ± 0.85 | 5.64 ± 1.14 | 0.030 | 5.60 ± 1.12 | 5.25 ± 1.01 | 0.007 |
HDL-cholesterol, mmol/L | 1.27 ± 0.35 | 1,25 ± 0.35 | 0.260 | 1.43 ± 0.47 | 1.35 ± 0.42 | 0.008 |
LDL-cholesterol, mmol/L | 3.43 ± 0.68 | 3.61 ± 1.03 | 0.089 | 3.59 ± 0.93 | 3.37 ± 0.85 | 0.031 |
Non-HDL cholesterol mmol/L | 4.11 ± 0.77 | 4.39 ± 1.07 | 0.010 | 4.17 ± 1.04 | 3.90 ± 0.98 | 0.025 |
Triglycerides, mmol/L | 1.40 ± 0.73 | 1.68 ± 1.03 | 0.075 | 1.26 ± 0.70 | 1.15 ± 0.67 | 0.234 |
Glucose, mmol/L | 5.26 ± 0.74 | 5.41 ± 0.79 | 0.165 | 5.20 ± 0.58 | 5.03 ± 0.32 | 0.118 |
Insulin, µUI/mL | 7.85 ± 5.57 | 8.52 ± 5.67 | 0.066 | 6.71 ± 4.37 | 6.13 ± 3.16 | 0.428 |
HOMA-IR | 1.66 ± 1.55 | 1.87 ± 1.70 | 0.038 | 1.49 ± 1.27 | 1.25 ± 0.74 | 0.275 |
Sirtuin1, ng/mL | 1.06 ± 0.71 | 5.75 ± 2.98 | <0.001 | 1.65 ± 1.81 | 5.80 ± 2.23 | <0.001 |
esRAGE, pg/mL | 255.78 ± 128.87 | 246.96 ± 115.32 | 0.800 | 246.67 ± 111.62 | 253.33 ± 116.81 | 0.857 |
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Roggerio, A.; Strunz, C.M.C.; Pacanaro, A.P.; Leal, D.P.; Takada, J.Y.; Avakian, S.D.; Mansur, A.D.P. Gene Expression of Sirtuin-1 and Endogenous Secretory Receptor for Advanced Glycation End Products in Healthy and Slightly Overweight Subjects after Caloric Restriction and Resveratrol Administration. Nutrients 2018, 10, 937. https://doi.org/10.3390/nu10070937
Roggerio A, Strunz CMC, Pacanaro AP, Leal DP, Takada JY, Avakian SD, Mansur ADP. Gene Expression of Sirtuin-1 and Endogenous Secretory Receptor for Advanced Glycation End Products in Healthy and Slightly Overweight Subjects after Caloric Restriction and Resveratrol Administration. Nutrients. 2018; 10(7):937. https://doi.org/10.3390/nu10070937
Chicago/Turabian StyleRoggerio, Alessandra, Célia M. Cassaro Strunz, Ana Paula Pacanaro, Dalila Pinheiro Leal, Julio Y. Takada, Solange D. Avakian, and Antonio De Padua Mansur. 2018. "Gene Expression of Sirtuin-1 and Endogenous Secretory Receptor for Advanced Glycation End Products in Healthy and Slightly Overweight Subjects after Caloric Restriction and Resveratrol Administration" Nutrients 10, no. 7: 937. https://doi.org/10.3390/nu10070937
APA StyleRoggerio, A., Strunz, C. M. C., Pacanaro, A. P., Leal, D. P., Takada, J. Y., Avakian, S. D., & Mansur, A. D. P. (2018). Gene Expression of Sirtuin-1 and Endogenous Secretory Receptor for Advanced Glycation End Products in Healthy and Slightly Overweight Subjects after Caloric Restriction and Resveratrol Administration. Nutrients, 10(7), 937. https://doi.org/10.3390/nu10070937