Myeloid-cell protein tyrosine phosphatase-1B deficiency in mice protects against high-fat diet and lipopolysaccharide-induced inflammation, hyperinsulinemia, and endotoxemia through an IL-10 STAT3-dependent mechanism

Diabetes

Volumn 63, Issue 2, 2014, Pages 456-470

  Grant, Louise ^a   Shearer, Kirsty D ^a   Czopek, Alicja ^a   Lees, Emma K ^a   Owen, Carl ^a   Agouni, Abdelali ^a   Workman, James ^a   Martin Granados, Cristina ^a   Forrester, John V ^a   Wilson, Heather M ^a   Mody, Nimesh ^a   Delibegovic, Mirela ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; GLUCOSE; INSULIN; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MESSENGER RNA; PROTEIN TYROSINE PHOSPHATASE 1B; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ADIPOSE TISSUE; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; BONE MARROW CELL; CONTROLLED STUDY; ENDOTOXEMIA; ENZYME PHOSPHORYLATION; GLUCOSE TOLERANCE; HYPERINSULINEMIA; IN VITRO STUDY; INFLAMMATION; INSULIN TOLERANCE TEST; LIPID DIET; LIVER INJURY; MACROPHAGE; MALE; METABOLISM; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL;

ADIPOSE TISSUE, WHITE; ANIMALS; CELL LINE; DIETARY FATS; DRUG-INDUCED LIVER INJURY; ENDOTOXEMIA; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; HOMEOSTASIS; HYPERINSULINISM; INFLAMMATION; INTERLEUKIN-10; JANUS KINASES; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, KNOCKOUT; MYELOID CELLS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; SIGNAL TRANSDUCTION; SPLEEN; STAT3 TRANSCRIPTION FACTOR;

EID: 84893128687     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-0885     Document Type: Article

References (47)

1. Elchebly M, Payette P, Michaliszyn E, et al. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 1999;283:1544-1548
2. Klaman LD, Boss O, Peroni OD, et al. Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in proteintyrosine phosphatase 1B-deficient mice. Mol Cell Biol 2000;20:5479-5489
3. Bence KK, Delibegovic M, Xue B, et al. Neuronal PTP1B regulates body weight, adiposity and leptin action. Nat Med 2006;12:917-924
4. Delibegovic M, Bence KK, Mody N, et al. Improved glucose homeostasis in mice with muscle-specific deletion of protein-tyrosine phosphatase 1B. Mol Cell Biol 2007;27:7727-7734
5. Delibegovic M, Zimmer D, Kauffman C, et al. Liver-specific deletion of protein-tyrosine phosphatase 1B (PTP1B) improves metabolic syndrome and attenuates diet-induced endoplasmic reticulum stress. Diabetes 2009; 58:590-599
6. Owen C, Czopek A, Agouni A, et al. Adipocyte-specific protein tyrosine phosphatase 1B deletion increases lipogenesis, adipocyte cell size and is a minor regulator of glucose homeostasis. PLoS ONE 2012;7:e32700
7. 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
8. 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
9. 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
10. Jager J, Grémeaux T, Cormont M, Le Marchand-Brustel Y, Tanti JF. Interleukin-1beta-induced insulin resistance in adipocytes through downregulation of insulin receptor substrate-1 expression. Endocrinology 2007; 148:241-251
11. Senn JJ, Klover PJ, Nowak IA, Mooney RA. Interleukin-6 induces cellular insulin resistance in hepatocytes. Diabetes 2002;51:3391-3399
12. Chen A, Mumick S, Zhang C, et al. Diet induction of monocyte chemoattractant protein-1 and its impact on obesity. Obes Res 2005;13:1311-1320
13. 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
14. 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
15. Xu H, An H, Hou J, et al. Phosphatase PTP1B negatively regulates MyD88-and TRIF-dependent proinflammatory cytokine and type I interferon production in TLR-triggered macrophages. Mol Immunol 2008; 45:3545-3552
16. Nasimian A, Taheripak G, Gorgani-Firuzjaee S, Sadeghi A, Meshkani R. Protein tyrosine phosphatase 1B (PTP1B) modulates palmitate-induced cytokine production in macrophage cells. Inflamm Res 2013;62:239-246
17. Heinonen KM, Dubé N, Bourdeau A, Lapp WS, Tremblay ML. Protein tyrosine phosphatase 1B negatively regulates macrophage development through CSF-1 signaling. Proc Natl Acad Sci USA 2006;103:2776-2781
18. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Förster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 1999;8:265-277
19. Ren Y, Xie Y, Jiang G, et al. Apoptotic cells protect mice against lipopolysaccharide-induced shock. J Immunol 2008;180:4978-4985
20. Agouni A, Mody N, Owen C, et al. Liver-specific deletion of protein tyrosine phosphatase (PTP) 1B improves obesity-and pharmacologically induced endoplasmic reticulum stress. Biochem J 2011;438:369-378
21. Agouni A, Owen C, Czopek A, Mody N, Delibegovic M. In vivo differential effects of fasting, re-feeding, insulin and insulin stimulation time course on insulin signaling pathway components in peripheral tissues. Biochem Biophys Res Commun 2010;401:104-111
22. Erwig LP, Kluth DC, Walsh GM, Rees AJ. Initial cytokine exposure determines function of macrophages and renders them unresponsive to other cytokines. J Immunol 1998;161:1983-1988
23. Cani PD, Amar J, Iglesias MA, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007;56:1761-1772
24. Niemand C, Nimmesgern A, Haan S, et al. Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling. J Immunol 2003;170:3263-3272
25. Heinonen KM, Bourdeau A, Doody KM, Tremblay ML. Protein tyrosine phosphatases PTP-1B and TC-PTP play nonredundant roles in macrophage development and IFN-gamma signaling. Proc Natl Acad Sci USA 2009;106: 9368-9372
26. Murray PJ. STAT3-mediated anti-inflammatory signalling. Biochem Soc Trans 2006;34:1028-1031
27. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001;19:683-765
28. Schindler C, Levy DE, Decker T. JAK-STAT signaling: from interferons to cytokines. J Biol Chem 2007;282:20059-20063
29. Myers MP, Andersen JN, Cheng A, et al. TYK2 and JAK2 are substrates of protein-tyrosine phosphatase 1B. J Biol Chem 2001;276:47771-47774
30. Benkhart EM, Siedlar M, Wedel A, Werner T, Ziegler-Heitbrock HW. Role of Stat3 in lipopolysaccharide-induced IL-10 gene expression. J Immunol 2000;165:1612-1617
31. Bourdeau A, Dubé N, Tremblay ML. Cytoplasmic protein tyrosine phosphatases, regulation and function: the roles of PTP1B and TC-PTP. Curr Opin Cell Biol 2005;17:203-209
32. Lu X, Malumbres R, Shields B, et al. PTP1B is a negative regulator of interleukin 4-induced STAT6 signaling. Blood 2008;112:4098-4108
33. Feldhammer M, Uetani N, Miranda-Saavedra D, Tremblay ML. PTP1B: a simple enzyme for a complex world. Crit Rev Biochem Mol Biol 2013;48: 430-445
34. Zhang J, Wang B, Zhang W, et al. Protein tyrosine phosphatase 1B deficiency ameliorates murine experimental colitis via the expansion of myeloid-derived suppressor cells. PLoS ONE 2013;8:e70828
35. van Exel E, Gussekloo J, de Craen AJ, Frölich M, Bootsma-Van Der Wiel A, Westendorp RG; Leiden 85 Plus Study. Low production capacity of interleukin-10 associates with the metabolic syndrome and type 2 diabetes: the Leiden 85-Plus Study. Diabetes 2002;51:1088-1092
36. Esposito K, Pontillo A, Giugliano F, et al. Association of low interleukin-10 levels with the metabolic syndrome in obese women. J Clin Endocrinol Metab 2003;88:1055-1058
37. Scarpelli D, Cardellini M, Andreozzi F, et al. Variants of the interleukin-10 promoter gene are associated with obesity and insulin resistance but not type 2 diabetes in caucasian italian subjects. Diabetes 2006;55:1529-1533
38. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007;117:175-184
39. Hong EG, Ko HJ, Cho YR, et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 2009;58:2525-2535
40. Kim HJ, Higashimori T, Park SY, et al. Differential effects of interleukin-6 and-10 on skeletal muscle and liver insulin action in vivo. Diabetes 2004; 53:1060-1067
41. Ogilvy S, Metcalf D, Print CG, Bath ML, Harris AW, Adams JM. Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc Natl Acad Sci USA 1999;96:14943-14948
42. Yoo JY, Huso DL, Nathans D, Desiderio S. Specific ablation of Stat3beta distorts the pattern of Stat3-responsive gene expression and impairs recovery from endotoxic shock. Cell 2002;108:331-344
43. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-174
44. Serafini P, De Santo C, Marigo I, et al. Derangement of immune responses by myeloid suppressor cells. Cancer Immunol Immunother 2004;53:64-72
45. Nagaraj S, Gupta K, Pisarev V, et al. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat Med 2007;13:828-835
46. Liu C, Yu S, Kappes J, et al. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood 2007;109: 4336-4342
47. Sinha P, Clements VK, Bunt SK, Albelda SM, Ostrand-Rosenberg S. Crosstalk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol 2007;179:977-983