Resveratrol attenuates intermittent hypoxia-induced macrophage migration to visceral white adipose tissue and insulin resistance in male mice

Endocrinology (United States)

Volumn 156, Issue 2, 2015, Pages 437-443

  Carreras, Alba ^a   Zhang, Shelley X L ^a   Almendros, Isaac ^a   Wang, Yang ^a   Peris, Eduard ^a   Qiao, Zhuanhong ^a   Gozal, David ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN; LEPTIN; OXYGEN; PROTEIN KINASE B; RESVERATROL; ANTIOBESITY AGENT; STILBENE DERIVATIVE;

ADIPOCYTE; ADIPOSE TISSUE; ADULT; AMBIENT AIR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CELL INFILTRATION; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; DRUG EFFICACY; DRUG MEGADOSE; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; EPIDIDYMIS FAT; FLOW CYTOMETRY; FOOD INTAKE; GLUCOSE BLOOD LEVEL; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTRAABDOMINAL FAT; MACROPHAGE; MACROPHAGE MIGRATION; MALE; MOUSE; NONHUMAN; OXYGEN CONCENTRATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; WEIGHT GAIN; WHITE ADIPOCYTE; WHITE ADIPOSE TISSUE; ANIMAL; ANOXIA; BLOOD; C57BL MOUSE; DRUG EFFECTS; DRUG SCREENING; EATING; IMMUNOLOGY; RANDOMIZATION;

ANIMALS; ANOXIA; ANTI-OBESITY AGENTS; DRUG EVALUATION, PRECLINICAL; EATING; INSULIN; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; LEPTIN; MACROPHAGES; MALE; MICE, INBRED C57BL; RANDOM ALLOCATION; STILBENES; WEIGHT GAIN;

EID: 84921634220     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1706     Document Type: Article

References (56)

1. Li RC, Row BW, Kheirandish L, et al. Nitric oxiDe synthase and intermittent hypoxia-induced spatial learning Deficits in the rat. Neurobiol Dis. 2004;17(1):44-53
2. Veasey SC, Davis CW, Fenik P, et al. Long-term intermittent hypoxia in mice: protracted hypersomnolence with oxidative injury to sleep-wake brain regions. Sleep. 2004;27(2):194-201
3. Nair D, Dayyat EA, Zhang SX, Wang Y, Gozal D. Intermittent hypoxia-induced cognitive Deficits are mediated byNADPHoxidase activity in a murine moDel of sleep apnea. PLoS One. 2011;6(5): e19847
4. Kheirandish L, Row BW, Li RC, Brittian KR, Gozal D. Apolipoprotein E-Deficient mice exhibit increased vulnerability to intermittent hypoxia-induced spatial learning Deficits. Sleep. 2005;28(11): 1412-1417
5. Davis EM, ODonnell CP. RoDent moDels of sleep apnea. Respir Physiol Neurobiol. 2013;188(3):355-361
6. Chou YT, Zhan G, Zhu Y, et al. C/EBP homologous binding protein (CHOP) unDerlies neural injury in sleep apnea moDel. Sleep. 2013; 36(4):481-492
7. Fang G, Song D, Ye X, Mao SZ, Liu G, Liu SF. Chronic intermittent hypoxia exposure induces atherosclerosis in ApoE knockout mice: role of NF-B p50. Am J Pathol. 2012;181(5):1530-1539
8. Schulz R, Murzabekova G, Egemnazarov B, et al. Arterial hypertension in a murine moDel of sleep apnea: role of NADPH oxidase 2. J Hypertens. 2014;32(2):300-305
9. Chalacheva P, Thum J, Yokoe T, ODonnell CP, Khoo MC. Development of autonomic dysfunction with intermittent hypoxia in a lean murine moDel. Respir Physiol Neurobiol. 2013;188(2):143-151
10. Gautier-Veyret E, Arnaud C, Bck M, et al. Intermittent hypoxiaactivated cyclooxygenase pathway: role in atherosclerosis. Eur Respir J. 2013;42(2):404-413
11. Iiyori N, Alonso LC, Li J, et al. Intermittent hypoxia causes insulin resistance in lean mice inDepenDent of autonomic activity. Am J Respir Crit Care Med. 2007;175(8):851-857
12. Li J, Savransky V, Nanayakkara A, Smith PL, ODonnell CP, Polotsky VY. HyperlipiDemia and lipid peroxidation are DepenDent on the severity of chronic intermittent hypoxia. J Appl Physiol (1985). 2007;102(2):557-563
13. Drager LF, Li J, Reinke C, BeVans-Fonti S, Jun JC, Polotsky VY. Intermittent hypoxia exacerbates metabolic effects of diet-induced obesity. Obesity (Silver Spring). 2011;19(11):2167-2174
14. Gharib SA, Khalyfa A, AbDelkarim A, et al. Intermittent hypoxia activates temporally coordinated transcriptional programs in visceral adipose tissue. J Mol Med (Berl). 2012;90(4):435-445
15. Carreras A, Kayali F, Zhang J, Hirotsu C, Wang Y, Gozal D. Metabolic effects of intermittent hypoxia in mice: steady versus highfrequency applied hypoxia daily during the rest period.AmJ Physiol Regul Integr Comp Physiol. 2012;303(7):R700-R709
16. Lee EJ, Alonso LC, Stefanovski D, et al. Time-DepenDent changes in glucose and insulin regulation during intermittent hypoxia and continuous hypoxia. Eur J Appl Physiol. 2013;113(2):467-478
17. Jun JC, Shin MK, Yao Q, et al. Acute hypoxia induces hypertriglyceriDemia by Decreasing plasma triglyceriDe clearance in mice. Am J Physiol Endocrinol Metab. 2012;303(3):E377-E388
18. Poulain L,ThomasA, Rieusset J, et al. Visceral white fat remoDelling contributes to intermittent hypoxia-induced atherogenesis. Eur Respir J. 2014;43(2):513-522
19. Gozal D, CapDevila OS, Kheirandish-Gozal L. Metabolic alterations and systemic inflammation in obstructive sleep apnea among nonobese and obese prepubertal children. Am J Respir Crit Care Med. 2008;177(10):1142-1149
20. Kendzerska T, Gershon AS, Hawker G, Tomlinson G, Leung RS. Obstructive sleep apnea and inciDent diabetes. A historical cohort study. Am J Respir Crit Care Med. 2014;190(2):218-225
21. Guest JF, Panca M, Sladkevicius E, Taheri S, Stradling J. Clinical outcomes and cost-effectiveness of continuous positive airway pressure to manage obstructive sleep apnea in patients with type 2 diabetes in the U.K. Diabetes Care. 2014;37(5):1263-1271
22. Zhong W, Tang YG, Zhao X, Go FY, Harper RM, Hui H. Treating benefits type 2 diabetes management. Pancreas. 2014;43(3):325-330
23. Grimaldi D, Beccuti G, Touma C, Van Cauter E, Mokhlesi B. Association of obstructive sleep apnea in rapid eye movement sleep with reduced glycemic control in type 2 diabetes: therapeutic implications. Diabetes Care. 2014;37(2):355-363
24. Louis M, Punjabi NM. Effects of acute intermittent hypoxia on glucose metabolism in awake healthy volunteers. J Appl Physiol (1985). 2009;106(5):1538-1544
25. Yokoe T, Alonso LC, Romano LC, et al. Intermittent hypoxia reverses the diurnal glucose rhythm and causes pancreatic-cell replication in mice. J Physiol. 2008;586(3):899-911
26. Xu J, Long YS, Gozal D, Epstein PN.-Cell Death and proliferation after intermittent hypoxia: role of oxidative stress. Free Radic Biol Med. 2009;46(6):783-790
27. Fang Y, Zhang Q, Tan J, Li L, An X, Lei P. Intermittent hypoxiainduced rat pancreatic-cell apoptosis and protective effects of antioxidant intervention. Nutr Diabetes. 2014;4:e131
28. Zhang SX, Qiao Z, Gozal D,WangY. Intermittent hypoxia-induced metabolic dysfunction in visceral fat is associated with immune Deregulation and inflammation. Am J Respir Crit Care Med 2013; 187:2013:A2383
29. Eguchi J, Kong X, Tenta M, Wang X, Kang S, Rosen ED. Interferon regulatory factor 4 regulates obesity-induced inflammation through regulation of adipose tissue macrophage polarization. Diabetes. 2013;62(10):3394-403
30. Polak J, Shimoda LA, Drager LF, et al. Intermittent hypoxia impairs glucose homeostasis in C57BL6/J mice: partial improvement with cessation of the exposure. Sleep. 2013;36(10):1483-1490; 1490A-1490B
31. He Q, Yang QC, Zhou Q, et al. Effects of varying Degrees of intermittent hypoxia on proinflammatory cytokines and adipokines in rats and 3T3-L1 adipocytes. PLoS One. 2014;9(1):e86326
32. Olea E, Agapito MT, Gallego-Martin T, et al. Intermittent hypoxia and diet-induced obesity: effects on oxidative status, sympathetic tone, plasma glucose and insulin levels and arterial pressure. J Appl Physiol (1985). 2014;117(7):706-719
33. Pearson KJ, Baur JA, Lewis KN, et al. Resveratrol Delays age-related Deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell Metab. 2008;8:157-168
34. Baur JA, Pearson KJ, Price NL, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature. 2006;444:337-342
35. Lagouge M, Argmann C, Gerhart-Hines Z, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1. Cell. 2006;127:1109-1122
36. Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo eviDence. Nat Rev Drug Discov. 2006;5:493-506
37. Um JH, Park SJ, Kang H, et al. AMP-Activated protein kinase-Deficient mice are resistant to the metabolic effects of resveratrol. Diabetes. 2010;59(3):554-563
38. Price NL, Gomes AP, Ling AJ, et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012;15(5):675-690
39. Nwachukwu JC, Srinivasan S, Bruno NE, et al. Resveratrol modulates the inflammatory response via an estrogen receptor-signal integration network. Elife. 2014;3:e02057
40. Gozal D, Daniel JM, Dohanich GP. Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J Neurosci. 2001;21:2442-2450
41. SargisRM,Neel BA, Brock CO, et al. The novel endocrine disruptor tolylfluanid impairs insulin signaling in primary roDent and human adipocytes through a reduction in insulin receptor substrate-1 levels. Biochim Biophys Acta. 2012;1822:952-960
42. Van Den Borst B, Schols AM, De Theije C, et al. Characterization of the inflammatory and metabolic profile of adipose tissue in a mouse moDel of chronic hypoxia. J Appl Physiol (1985). 2013;114(11): 1619-1628
43. Zhang H, Zhang G, Gonzalez FJ, Park SM, Cai D. Hypoxia-inducible factor directs POMC gene to mediate hypothalamic glucose sensing and energy balance regulation. PLoS Biol. 2011;9(7): e1001112
44. SchneiDer Y, Duranton B, Goss F, Schleiffer R, Seiler N, Raul F. Resveratrol inhibits intestinal tumorigenesis and modulates hostDefense-related gene expression in an animal moDel of human familial aDenomatous polyposis. Nutr Cancer. 2001;39:102-107
45. Norata GD, Marchesi P, Passamonti S, Pirillo A, Violi F, Catapano AL. Anti-inflammatory and anti-Atherogenic effects of cathechin, caffeic acid and trans-resveratrol in apolipoprotein E Deficient mice. Atherosclerosis. 2007;191:265-271
46. Qureshi AA, Guan XQ, Reis JC, et al. Inhibition of nitric oxiDe and inflammatory cytokines in LPS-stimulated murine macrophages by resveratrol, a potent proteasome inhibitor. Lipids Health Dis. 2012; 11:76
47. Cho SJ, Jung UJ, Choi MS. Differential effects of low-dose resveratrol on adiposity and hepatic steatosis in diet-induced obese mice. Br J Nutr. 2012;108:2166-2175
48. Taylor CT, Kent BD, Crinion SJ, McNicholas WT, Ryan S. Human adipocytes are highly sensitive to intermittent hypoxia induced NF-B activity and subsequent inflammatory gene expression. Biochem Biophys Res Commun. 2014;447(4):660-665
49. Reinke C, BeVans-Fonti S, Drager LF, Shin MK, Polotsky VY. Effects of different acute hypoxic regimens on tissue oxygen profiles and metabolic outcomes. J Appl Physiol (1985). 2011;111(3):881-890
50. Vieira-Potter VJ. Inflammation and macrophage modulation in adipose tissues. Cell Microbiol. 2014;16(10):1484-1492
51. Charo IF. Macrophage polarization and insulin resistance: PPAR in control. Cell Metab. 2007;6(2):96-98
52. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest. 2003;112:1796-1808
53. Di Gregorio GB, Yao-Borengasser A, Rasouli N, et al. Expression of CD68 and macrophage chemoattractant protein-1 genes in human adipose and muscle tissues: association with cytokine expression, insulin resistance, and reduction by pioglitazone. Diabetes. 2005; 54:2305-2313
54. Oh DY, Morinaga H, Talukdar S, Bae EJ, Olefsky JM. Increased macrophage migration into adipose tissue in obese mice. Diabetes. 2012;61(2):346-354
55. HernanDez ED, Lee SJ, Kim JY, et al Macrophage NBR1-MEKK3 complex triggers JNK-mediated adipose tissue inflammation in obesity. Cell Metab. 2014;20(3):499-511
56. Fujisaka S, Usui I, Ikutani M, et al. Adipose tissue hypoxia induces inflammatoryM1polarity of macrophages in an HIF-1-DepenDent and HIF-1-inDepenDent manner in obese mice. Diabetologia. 2013;56(6):1403-1412.