Otopetrin 1 protects mice from obesity-associated metabolic dysfunction through attenuating adipose tissue inflammation

Diabetes

Volumn 63, Issue 4, 2014, Pages 1340-1352

  Wang, Guo Xiao ^a   Cho, Kae Won ^a   Uhm, Maeran ^a   Hu, Chun Rui ^b   Li, Siming ^a   Cozacov, Zoharit ^a   Xu, Acer E ^a   Cheng, Ji Xin ^b   Saltiel, Alan R ^a   Lumeng, Carey N ^a   Lin, Jiandie D ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INSULIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LEPTIN; OTOPETRIN 1; PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOSE TISSUE INFLAMMATION; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; HOMEOSTASIS; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE; ADIPOSE TISSUE, WHITE; ANIMALS; DIET, HIGH-FAT; HOMEOSTASIS; INFLAMMATION; INSULIN RESISTANCE; INTERFERON-GAMMA; MALE; MEMBRANE PROTEINS; MICE; OBESITY; STAT1 TRANSCRIPTION FACTOR;

EID: 84897862540     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1139     Document Type: Article

References (48)

1. Trujillo ME, Scherer PE. Adipose tissue-derived factors: impact on health and disease. Endocr Rev 2006;27:762-778
2. Tontonoz P, Spiegelman BM. Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 2008;77:289-312
3. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004;84:277-359
4. Lowell BB, Spiegelman BM. Towards a molecular understanding of adaptive thermogenesis. Nature 2000;404:652-660
5. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol 2011;29:415-445
6. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest 2011;121:2111-2117
7. Odegaard JI, Chawla A. Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis. Science 2013;339:172-177
8. Osborn O, Olefsky JM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 2012;18:363-374
9. Sun S, Ji Y, Kersten S, Qi L. Mechanisms of inflammatory responses in obese adipose tissue. Annu Rev Nutr 2012;32:261-286
10. Goldfine AB, Silver R, Aldhahi W, et al. Use of salsalate to target inflammation in the treatment of insulin resistance and type 2 diabetes. Clin Transl Sci 2008;1:36-43
11. Larsen CM, Faulenbach M, Vaag A, et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 2007;356:1517-1526
12. Hevener AL, Olefsky JM, Reichart D, et al. Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J Clin Invest 2007;117:1658-1669
13. Pascual G, Fong AL, Ogawa S, et al. A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature 2005;437:759-763
14. Aron-Wisnewsky J, Tordjman J, Poitou C, et al. Human adipose tissue macrophages: m1 and m2 cell surface markers in subcutaneous and omental depots and after weight loss. J Clin Endocrinol Metab 2009;94:4619-4623
15. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007;117:175-184
16. Lumeng CN, Deyoung SM, Bodzin JL, Saltiel AR. Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes 2007;56:16-23
17. Feuerer M, Herrero L, Cipolletta D, et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 2009;15:930-939
18. Nishimura S, Manabe I, Nagasaki M, et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 2009;15:914-920
19. Winer S, Chan Y, Paltser G, et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 2009;15:921-929
20. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993;259:87-91
21. Arkan MC, Hevener AL, Greten FR, et al. IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 2005;11:191-198
22. Cai D, Yuan M, Frantz DF, et al. Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat Med 2005;11:183-190
23. Chiang SH, Bazuine M, Lumeng CN, et al. The protein kinase IKKepsilon regulates energy balance in obese mice. Cell 2009;138:961-975
24. Hirosumi J, Tuncman G, Chang L, et al. A central role for JNK in obesity and insulin resistance. Nature 2002;420:333-336
25. Stienstra R, Joosten LA, Koenen T, et al. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab 2010;12:593-605
26. Vandanmagsar B, Youm YH, Ravussin A, et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 2011;17:179-188
27. Waki H, Tontonoz P. Endocrine functions of adipose tissue. Annu Rev Pathol 2007;2:31-56
28. Stark GR, Darnell JE Jr. The JAK-STAT pathway at twenty. Immunity 2012; 36:503-514
29. McGillicuddy FC, Chiquoine EH, Hinkle CC, et al. Interferon gamma attenuates insulin signaling, lipid storage, and differentiation in human adipocytes via activation of the JAK/STAT pathway. J Biol Chem 2009;284:31936-31944
30. Rocha VZ, Folco EJ, Sukhova G, et al. Interferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ Res 2008;103:467-476
31. Hughes I, Binkley J, Hurle B, Green ED, Sidow A, Ornitz DM; NISC Comparative Sequencing Program. Identification of the Otopetrin Domain, a conserved domain in vertebrate otopetrins and invertebrate otopetrin-like family members. BMC Evol Biol 2008;8:41
32. Hurle B, Marques-Bonet T, Antonacci F, et al.; NISC Comparative Sequencing Program. Lineage-specific evolution of the vertebrate Otopetrin gene family revealed by comparative genomic analyses. BMC Evol Biol 2011;11:23
33. Hughes I, Saito M, Schlesinger PH, Ornitz DM. Otopetrin 1 activation by purinergic nucleotides regulates intracellular calcium. Proc Natl Acad Sci USA 2007;104:12023-12028
34. Hurle B, Ignatova E, Massironi SM, et al. Non-syndromic vestibular disorder with otoconial agenesis in tilted/mergulhador mice caused by mutations in otopetrin 1. Hum Mol Genet 2003;12:777-789
35. Kim E, Hyrc KL, Speck J, et al. Missense mutations in Otopetrin 1 affect subcellular localization and inhibition of purinergic signaling in vestibular supporting cells. Mol Cell Neurosci 2011;46:655-661
36. Kim E, Hyrc KL, Speck J, et al. Regulation of cellular calcium in vestibular supporting cells by otopetrin 1. J Neurophysiol 2010;104:3439-3450
37. Klein J, Fasshauer M, Ito M, Lowell BB, Benito M, Kahn CR. beta(3)-adrenergic stimulation differentially inhibits insulin signaling and decreases insulin-induced glucose uptake in brown adipocytes. J Biol Chem 1999;274:34795-34802
38. Li S, Liu C, Li N, et al. Genome-wide coactivation analysis of PGC-1alpha identifies BAF60a as a regulator of hepatic lipid metabolism. Cell Metab 2008;8:105-117
39. Molusky MM, Li S, Ma D, Yu L, Lin JD. Ubiquitin-specific protease 2 regulates hepatic gluconeogenesis and diurnal glucose metabolism through 11b-hydroxysteroid dehydrogenase 1. Diabetes 2012;61:1025-1035
40. Rotter V, Nagaev I, Smith U. Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. J Biol Chem 2003;278:45777-45784
41. Folick A, Min W, Wang MC. Label-free imaging of lipid dynamics using Coherent Anti-stokes Raman Scattering (CARS) and Stimulated Raman Scattering (SRS) microscopy. Curr Opin Genet Dev 2011;21:585-590
42. Le TT, Yue S, Cheng JX. Shedding new light on lipid biology with coherent anti-Stokes Raman scattering microscopy. J Lipid Res 2010;51:3091-3102
43. Reilly SM, Chiang SH, Decker SJ, et al. An inhibitor of the protein kinases TBK1 and IKK-ε improves obesity-related metabolic dysfunctions in mice. Nat Med 2013;19:313-321
44. Saltiel AR. Insulin resistance in the defense against obesity. Cell Metab 2012;15:798-804
45. Oh DY, Talukdar S, Bae EJ, et al. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 2010;142:687-698
46. Hu X, Ivashkiv LB. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 2009;31:539-550
47. Wada T, Hoshino M, Kimura Y, et al. Both type I and II IFN induce insulin resistance by inducing different isoforms of SOCS expression in 3T3-L1 adipocytes. Am J Physiol Endocrinol Metab 2011;300:E1112-E1123
48. O'Rourke RW, White AE, Metcalf MD, et al. Systemic inflammation and insulin sensitivity in obese IFN-g knockout mice. Metabolism 2012;61:1152-1161