Macrophage deletion of SOCS1 increases sensitivity to LPS and palmitic acid and results in systemic inflammation and hepatic insulin resistance

Diabetes

Volumn 60, Issue 8, 2011, Pages 2023-2031

  Sachithanandan, Nirupa ^a   Graham, Kate L ^a   Galic, Sandra ^a   Honeyman, Jane E ^a   Fynch, Stacey L ^a   Hewitt, Kimberly A ^a   Steinberg, Gregory R ^a,b   Kay, Thomas W ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; GLYCOPROTEIN P 15095; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MONOCYTE CHEMOTACTIC PROTEIN; PALMITIC ACID; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; FLOW CYTOMETRY; GLUCOSE TOLERANCE TEST; HEPATITIS; HYPERINSULINEMIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; LYMPHOID CELL; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; INFLAMMATION; INSULIN; INSULIN RESISTANCE; LIPOPOLYSACCHARIDES; LIVER; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; PALMITIC ACID; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TOLL-LIKE RECEPTORS;

EID: 80052848442     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0259     Document Type: Article

References (46)

1. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 2006;116:1793-1801 (Pubitemid 44033299)
2. 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 (Pubitemid 23036092)
3. Steinberg GR, Michell BJ, van Denderen BJ, et al. Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab 2006;4:465-474 (Pubitemid 44834113)
4. Xu H, Barnes GT, Yang Q, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003;112:1821-1830 (Pubitemid 38063705)
5. 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 (Pubitemid 38063703)
6. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol 2001;1:135-145 (Pubitemid 33741967)
7. O'Neill LA, Bowie AG. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 2007;7:353-364 (Pubitemid 46674493)
8. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 2006;444:1022-1023 (Pubitemid 46018512)
9. Brun P, Castagliuolo I, Di Leo V, et al. Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steato-hepatitis. Am J Physiol Gastrointest Liver Physiol 2007;292:G518-G525
10. Membrez M, Blancher F, Jaquet M, et al. Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice. FASEB J 2008;22:2416-2426 (Pubitemid 351948659)
11. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 2006;116: 3015-3025 (Pubitemid 44684486)
12. Tsukumo DM, Carvalho-Filho MA, Carvalheira JB, et al. Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 2007;56:1986-1998 (Pubitemid 47195825)
13. Nguyen MT, Favelyukis S, Nguyen AK, et al. A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-dependent pathways. J Biol Chem 2007;282:35279-35292 (Pubitemid 350232441)
14. Ghanim H, Aljada A, Hofmeyer D, Syed T, Mohanty P, Dandona P. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation 2004;110:1564-1571 (Pubitemid 39297977)
15. Boden G, She P, Mozzoli M, et al. Free fatty acids produce insulin resistance and activate the proinflammatory nuclear factor-kB pathway in rat liver. Diabetes 2005;54:3458-3465 (Pubitemid 43334336)
16. Nguyen MT, Satoh H, Favelyukis S, et al. JNK and tumor necrosis factor-alpha mediate free fatty acid-induced insulin resistance in 3T3-L1 adipocytes. J Biol Chem 2005;280:35361-35371 (Pubitemid 41532725)
17. Yoshimura A, Naka T, Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol 2007;7:454-465 (Pubitemid 46834848)
18. Sakamoto H, Yasukawa H, Masuhara M, et al. A Janus kinase inhibitor, JAB, is an interferon-gamma-inducible gene and confers resistance to interferons. Blood 1998;92:1668-1676 (Pubitemid 28406871)
19. Sporri B, Kovanen PE, Sasaki A, Yoshimura A, Leonard WJ. JAB/SOCS1/SSI-1 is an interleukin-2-induced inhibitor of IL-2 signaling. Blood 2001;97:221-226 (Pubitemid 32061264)
20. Naka T, Narazaki M, Hirata M, et al. Structure and function of a new STAT-induced STAT inhibitor. Nature 1997;387:924-929 (Pubitemid 27289596)
21. Mansell A, Smith R, Doyle SL, et al. Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat Immunol 2006;7:148-155 (Pubitemid 43135880)
22. Starr R, Metcalf D, Elefanty AG, et al. Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc Natl Acad Sci USA 1998;95:14395-14399 (Pubitemid 28549378)
23. Chong MM, Metcalf D, Jamieson E, Alexander WS, Kay TW. Suppressor of cytokine signaling-1 in T cells and macrophages is critical for preventing lethal inflammation. Blood 2005;106:1668-1675 (Pubitemid 41208580)
24. Gylvin T, Ek J, Nolsøe R, et al. Functional SOCS1 polymorphisms are associated with variation in obesity in whites. Diabetes Obes Metab 2009;11: 196-203
25. Harada M, Nakashima K, Hirota T, et al. Functional polymorphism in the suppressor of cytokine signaling 1 gene associated with adult asthma. Am J Respir Cell Mol Biol 2007;36:491-496 (Pubitemid 46623008)
26. Ueki K, Kondo T, Kahn CR. Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol Cell Biol 2004;24:5434-5446 (Pubitemid 38738176)
27. Jamieson E, Chong MM, Steinberg GR, et al. Socs1 deficiency enhances hepatic insulin signaling. J Biol Chem 2005;280:31516-31521 (Pubitemid 41291894)
28. Sachithanandan N, Fam BC, Fynch S, et al. Liver-specific suppressor of cytokine signaling-3 deletion in mice enhances hepatic insulin sensitivity and lipogenesis resulting in fatty liver and obesity. Hepatology 2010;52: 1632-1642
29. Dzamko N, van Denderen BJ, Hevener AL, et al. AMPK beta1 deletion reduces appetite, preventing obesity and hepatic insulin resistance. J Biol Chem 2010;285:115-122
30. Steinberg GR, Watt MJ, Ernst M, Birnbaum MJ, Kemp BE, Jørgensen SB. Ciliary neurotrophic factor stimulates muscle glucose uptake by a PI3-kinase-dependent pathway that is impaired with obesity. Diabetes 2009; 58:829-839
31. Thomas HE, Parker JL, Schreiber RD, Kay TW. IFN-gamma action on pancreatic beta cells causes class I MHC upregulation but not diabetes. J Clin Invest 1998;102:1249-1257 (Pubitemid 28436285)
32. Kirchgessner TG, Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Tumor necrosis factor-alpha contributes to obesity-related hyperleptinemia by regulating leptin release from adipocytes. J Clin Invest 1997;100:2777-2782 (Pubitemid 28007546)
33. Lee JY, Sohn KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem 2001;276:16683-16689
34. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007;117: 175-184 (Pubitemid 46048464)
35. Ye J, Gao Z, Yin J, He Q. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am J Physiol Endocrinol Metab 2007;293:E1118-E1128 (Pubitemid 47535846)
36. Kosteli A, Sugaru E, Haemmerle G, et al. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Invest 2010; 120:3466-3479
37. Saberi M, Woods NB, de Luca C, et al. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab 2009;10:419-429
38. Kinjyo I, Hanada T, Inagaki-Ohara K, et al. SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity 2002;17:583-591 (Pubitemid 35351504)
39. Huang W, Metlakunta A, Dedousis N, et al. Depletion of liver Kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance. Diabetes 2010;59:347-357
40. Odegaard JI, Ricardo-Gonzalez RR, Red Eagle A, et al. Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab 2008;7:496-507 (Pubitemid 351729205)
41. Holmes AG, Mesa JL, Neill BA, et al. Prolonged interleukin-6 administration enhances glucose tolerance and increases skeletal muscle PPARalpha and UCP2 expression in rats. J Endocrinol 2008;198:367-374
42. Sadagurski M, Norquay L, Farhang J, D'Aquino K, Copps K, White MF. Human IL6 enhances leptin action in mice. Diabetologia 2010;53:525-535
43. Petersen EW, Carey AL, Sacchetti M, et al. Acute IL-6 treatment increases fatty acid turnover in elderly humans in vivo and in tissue culture in vitro. Am J Physiol Endocrinol Metab 2005;288:E155-E162 (Pubitemid 40023802)
44. Carey AL, Steinberg GR, Macaulay SL, et al. Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes 2006;55: 2688-2697 (Pubitemid 44923666)
45. Zhang Y, Pilon G, Marette A, Baracos VE. Cytokines and endotoxin induce cytokine receptors in skeletal muscle. Am J Physiol Endocrinol Metab 2000;279:E196-E205 (Pubitemid 30609962)
46. Weigert C, Hennige AM, Lehmann R, et al. Direct cross-talk of interleukin-6 and insulin signal transduction via insulin receptor substrate-1 in skeletal muscle cells. J Biol Chem 2006;281:7060-7067 (Pubitemid 43847469)