Loss of regulator of G protein signaling 5 exacerbates obesity, hepatic steatosis, inflammation and insulin resistance

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Deng, Wei ^a   Wang, Xinan ^a   Xiao, Jinfeng ^a   Chen, Kuoju ^a   Zhou, Heng ^a   Shen, Difei ^a   Li, Hongliang ^a   Tang, Qizhu ^a  

^a RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; CYCLIN D1; DIACYLGLYCEROL ACYLTRANSFERASE 1; DIACYLGLYCEROL ACYLTRANSFERASE 2; FATTY ACID; FATTY ACID BINDING PROTEIN 4; GLUCOSE; GLYCEROL 3 PHOSPHATE ACYLTRANSFERASE; GLYCOGEN SYNTHASE KINASE 3BETA; GUANINE NUCLEOTIDE BINDING PROTEIN; HIGH DENSITY LIPOPROTEIN; I KAPPA B ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; JANUS KINASE; LEPTIN; LOW DENSITY LIPOPROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE B; RESISTIN; RGS PROTEIN; RGS5 PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRANSCRIPTION FACTOR RELA; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; I KAPPA B KINASE; RELA PROTEIN, MOUSE; RGS5 PROTEIN, MOUSE; STRESS ACTIVATED PROTEIN KINASE;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ARTICLE; BODY MASS; BODY WEIGHT; CONTROLLED STUDY; DISEASE EXACERBATION; ENZYME ACTIVATION; FATTY ACID OXIDATION; FATTY LIVER; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HEPATITIS; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTRAABDOMINAL FAT; LIPID DIET; LIPID STORAGE; LIPOLYSIS; LIVER; LIVER WEIGHT; MACROPHAGE; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; ANIMAL; C57BL MOUSE; CELL SIZE; DRUG EFFECT; GENETICS; HYPERINSULINISM; INFLAMMATION; METABOLISM; MOUSE MUTANT; OXIDATION REDUCTION REACTION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; WESTERN BLOTTING;

MUS;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; BLOTTING, WESTERN; BODY WEIGHT; CELL SIZE; DIET, HIGH-FAT; FATTY ACIDS; FATTY LIVER; HYPERINSULINISM; I-KAPPA B KINASE; INFLAMMATION; INSULIN RESISTANCE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SKELETAL; OBESITY; OXIDATION-REDUCTION; RGS PROTEINS; TRANSCRIPTION FACTOR RELA;

EID: 84855858769     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030256     Document Type: Article

References (53)

1. Flegal KM, Carroll MD, Ogden CL, Curtin LR, (2010) Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303: 235-241.
2. Gregor MF, Hotamisligil GS, (2011) Inflammatory mechanisms in obesity. Annu Rev Immunol 29: 415-445.
3. Wang Y, Mi J, Shan XY, Wang QJ, Ge KY, (2007) Is China facing an obesity epidemic and the consequences? The trends in obesity and chronic disease in China. Int J Obes (Lond) 31: 177-188.
4. Yang W, Lu J, Weng J, Jia W, Ji L, et al. (2010) Prevalence of diabetes among men and women in China. N Engl J Med 362: 1090-1101.
5. Wei H, Ahn S, Shenoy SK, Karnik SS, Hunyady L, et al. (2003) Independent beta-arrestin 2 and G protein-mediated pathways for angiotensin II activation of extracellular signal-regulated kinases 1 and 2. Proc Natl Acad Sci U S A 100: 10782-10787.
6. Moxham CM, Malbon CC, (1996) Insulin action impaired by deficiency of the G-protein subunit G ialpha2. Nature 379: 840-844.
7. Huang XP, Song X, Wang HY, Malbon CC, (2002) Targeted expression of activated Q227L G(alpha)(s) in vivo. Am J Physiol Cell Physiol 283: C386-395.
8. Huang X, Charbeneau RA, Fu Y, Kaur K, Gerin I, et al. (2008) Resistance to diet-induced obesity and improved insulin sensitivity in mice with a regulator of G protein signaling-insensitive G184S Gnai2 allele. Diabetes 57: 77-85.
9. Nunn C, Zhao P, Zou MX, Summers K, Guglielmo CG, et al. (2011) Resistance to age-related, normal body weight gain in RGS2 deficient mice. Cell Signal 23: 1375-1386.
10. Li H, He C, Feng J, Zhang Y, Tang Q, et al. (2010) Regulator of G protein signaling 5 protects against cardiac hypertrophy and fibrosis during biomechanical stress of pressure overload. Proc Natl Acad Sci U S A 107: 13818-13823.
11. Takata Y, Liu J, Yin F, Collins AR, Lyon CJ, et al. (2008) PPARdelta-mediated antiinflammatory mechanisms inhibit angiotensin II-accelerated atherosclerosis. Proc Natl Acad Sci U S A 105: 4277-4282.
12. Hamzah J, Jugold M, Kiessling F, Rigby P, Manzur M, et al. (2008) Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 453: 410-414.
13. Gunaje JJ, Bahrami AJ, Schwartz SM, Daum G, Mahoney WM Jr, (2011) PDGF-dependent regulation of regulator of G protein signaling-5 expression and vascular smooth muscle cell functionality. Am J Physiol Cell Physiol 301: C478-489.
14. Hajer GR, van HTW, Visseren FL, (2008) Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Eur Heart J 29: 2959-2971.
15. Stumvoll M, Goldstein BJ, van HTW, (2005) Type 2 diabetes: principles of pathogenesis and therapy. Lancet 365: 1333-1346.
16. Tunaru S, Kero J, Schaub A, Wufka C, Blaukat A, et al. (2003) PUMA-G and HM74 are receptors for nicotinic acid and mediate its anti-lipolytic effect. Nat Med 9: 352-355.
17. Kather H, Bieger W, Michel G, Aktories K, Jakobs KH, (1985) Human fat cell lipolysis is primarily regulated by inhibitory modulators acting through distinct mechanisms. J Clin Invest 76: 1559-1565.
18. Holm C, (2003) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans 31: 1120-1124.
19. Zimmermann R, Strauss JG, Haemmerle G, Schoiswohl G, Birner-Gruenberger R, et al. (2004) Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306: 1383-1386.
20. Karpe F, Tan GD, (2005) Adipose tissue function in the insulin-resistance syndrome. Biochem Soc Trans 33: 1045-1048.
21. Coppack SW, Evans RD, Fisher RM, Frayn KN, Gibbons GF, et al. (1992) Adipose tissue metabolism in obesity: lipase action in vivo before and after a mixed meal. Metabolism 41: 264-272.
22. Wang Y, Kim KA, Kim JH, Sul HS, (2006) Pref-1, a preadipocyte secreted factor that inhibits adipogenesis. J Nutr 136: 2953-2956.
23. Villena JA, Choi CS, Wang Y, Kim S, Hwang YJ, et al. (2008) Resistance to high-fat diet-induced obesity but exacerbated insulin resistance in mice overexpressing preadipocyte factor-1 (Pref-1): a new model of partial lipodystrophy. Diabetes 57: 3258-3266.
24. Fu M, Rao M, Bouras T, Wang C, Wu K, et al. (2005) Cyclin D1 inhibits peroxisome proliferator-activated receptor gamma-mediated adipogenesis through histone deacetylase recruitment. J Biol Chem 280: 16934-16941.
25. Imai T, Takakuwa R, Marchand S, Dentz E, Bornert JM, et al. (2004) Peroxisome proliferator-activated receptor gamma is required in mature white and brown adipocytes for their survival in the mouse. Proc Natl Acad Sci U S A 101: 4543-4547.
26. Eguchi J, Yan QW, Schones DE, Kamal M, Hsu CH, et al. (2008) Interferon regulatory factors are transcriptional regulators of adipogenesis. Cell Metab 7: 86-94.
27. Ahmed MH, Byrne CD, (2007) Modulation of sterol regulatory element binding proteins (SREBPs) as potential treatments for non-alcoholic fatty liver disease (NAFLD). Drug Discov Today 12: 740-747.
28. Schadinger SE, Bucher NL, Schreiber BM, Farmer SR, (2005) PPARgamma2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes. Am J Physiol Endocrinol Metab 288: E1195-1205.
29. Savage DB, Choi CS, Samuel VT, Liu ZX, Zhang D, et al. (2006) Reversal of diet-induced hepatic steatosis and hepatic insulin resistance by antisense oligonucleotide inhibitors of acetyl-CoA carboxylases 1 and 2. J Clin Invest 116: 817-824.
30. Dentin R, Benhamed F, Hainault I, Fauveau V, Foufelle F, et al. (2006) Liver-specific inhibition of ChREBP improves hepatic steatosis and insulin resistance in ob/ob mice. Diabetes 55: 2159-2170.
31. Neschen S, Morino K, Hammond LE, Zhang D, Liu ZX, et al. (2005) Prevention of hepatic steatosis and hepatic insulin resistance in mitochondrial acyl-CoA:glycerol-sn-3-phosphate acyltransferase 1 knockout mice. Cell Metab 2: 55-65.
32. Fain JN, (2006) Release of interleukins and other inflammatory cytokines by human adipose tissue is enhanced in obesity and primarily due to the nonfat cells. Vitam Horm 74: 443-477.
33. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808.
34. Lumeng CN, Deyoung SM, Bodzin JL, Saltiel AR, (2007) Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes 56: 16-23.
35. Kirk EA, Sagawa ZK, McDonald TO, O'Brien KD, Heinecke JW, (2008) Monocyte chemoattractant protein deficiency fails to restrain macrophage infiltration into adipose tissue [corrected]. Diabetes 57: 1254-1261.
36. Hotamisligil GS, Shargill NS, Spiegelman BM, (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87-91.
37. Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G, (2001) Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 280: E745-751.
38. Hong EG, Ko HJ, Cho YR, Kim HJ, Ma Z, et al. (2009) Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 58: 2525-2535.
39. Steinberg GR, Michell BJ, van DBJ, Watt MJ, Carey AL, et al. (2006) Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab 4: 465-474.
40. Baffy G, (2009) Kupffer cells in non-alcoholic fatty liver disease: the emerging view. J Hepatol 51: 212-223.
41. Odegaard JI, Ricardo-Gonzalez RR, Red EA, Vats D, Morel CR, et al. (2008) Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab 7: 496-507.
42. Feingold KR, Grunfeld C, (1987) Tumor necrosis factor-alpha stimulates hepatic lipogenesis in the rat in vivo. J Clin Invest 80: 184-190.
43. De Taeye BM, Novitskaya T, McGuinness OP, Gleaves L, Medda M, et al. (2007) Macrophage TNF-alpha contributes to insulin resistance and hepatic steatosis in diet-induced obesity. Am J Physiol Endocrinol Metab 293: E713-725.
44. Donath MY, Shoelson SE, (2011) Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11: 98-107.
45. Rosen ED, Spiegelman BM, (2006) Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444: 847-853.
46. Guilherme A, Virbasius JV, Puri V, Czech MP, (2008) Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 9: 367-377.
47. Rabe K, Lehrke M, Parhofer KG, Broedl UC, (2008) Adipokines and insulin resistance. Mol Med 14: 741-751.
48. Kreuzer J, Nurnberg B, Krieger-Brauer HI, (2004) Ligand-dependent autophosphorylation of the insulin receptor is positively regulated by Gi-proteins. Biochem J 380: 831-836.
49. Kanoh Y, Ishizuka T, Morita H, Ishizawa M, Miura A, et al. (2000) Effect of pertussis toxin on insulin-induced signal transduction in rat adipocytes and soleus muscles. Cell Signal 12: 223-232.
50. Usui I, Imamura T, Satoh H, Huang J, Babendure JL, et al. (2004) GRK2 is an endogenous protein inhibitor of the insulin signaling pathway for glucose transport stimulation. EMBO J 23: 2821-2829.
51. Schioth HB, (2006) G protein-coupled receptors in regulation of body weight. CNS Neurol Disord Drug Targets 5: 241-249.
52. Larminie C, Murdock P, Walhin JP, Duckworth M, Blumer KJ, et al. (2004) Selective expression of regulators of G-protein signaling (RGS) in the human central nervous system. Brain Res Mol Brain Res 122: 24-34.
53. Cho H, Park C, Hwang IY, Han SB, Schimel D, et al. (2008) Rgs5 targeting leads to chronic low blood pressure and a lean body habitus. Mol Cell Biol 28: 2590-2597.