Erythropoietin signaling: A novel regulator of white adipose tissue inflammation during diet-induced obesity

Diabetes

Volumn 63, Issue 7, 2014, Pages 2415-2431

  Alnaeeli, Mawadda ^a,b,c   Raaka, Bruce M ^a   Gavrilova, Oksana ^a   Teng, Ruifeng ^a   Chanturiya, Tatyana ^a   Noguchi, Constance Tom ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b OHIO UNIVERSITY   (United States)

^c OHIO UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCL1 CHEMOKINE; CXCL11 CHEMOKINE; ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 4 RECEPTOR; LEPTIN; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 5; STAT3 PROTEIN; STAT5 PROTEIN; STAT6 PROTEIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIET; ERYTHROID CELL; FAT MASS; FLOW CYTOMETRY; GLUCOSE BLOOD LEVEL; GLUCOSE INFUSION; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; HEMATOCRIT; IN VITRO STUDY; INFLAMMATION; INSULIN BLOOD LEVEL; INSULIN INFUSION; INSULIN RESISTANCE; INSULIN SENSITIVITY; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WEIGHT GAIN; WESTERN BLOTTING; WHITE ADIPOSE TISSUE; WHITE ADIPOSE TISSUE INFLAMMATION;

ADIPOSE TISSUE, WHITE; ANIMALS; CELLS, CULTURED; DIET, HIGH-FAT; ERYTHROPOIETIN; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OBESITY; PANNICULITIS; RECEPTORS, ERYTHROPOIETIN; SIGNAL TRANSDUCTION;

EID: 84902267066     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-0883     Document Type: Article

References (50)

1. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 2010;72:219-246
2. Zeyda M, Stulnig TM. Obesity, inflammation, and insulin resistance - a mini-review. Gerontology 2009;55:379-386
3. de Luca C, Olefsky JM. Inflammation and insulin resistance. FEBS Lett 2008;582:97-105 (Pubitemid 50010731)
4. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest 2011;121:2111-2117
5. 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)
6. 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
7. Wentworth JM, Naselli G, Brown WA, et al. Pro-inflammatory CD11c+CD206+ adipose tissue macrophages are associated with insulin resistance in human obesity. Diabetes 2010;59:1648-1656
8. Lumeng CN, DelProposto JB, Westcott DJ, Saltiel AR. Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 2008;57:3239-3246
9. Kanda H, Tateya S, Tamori Y, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 2006;116:1494-1505
10. Kamei N, Tobe K, Suzuki R, et al. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 2006;281:26602- 26614
11. Arkan MC, Hevener AL, Greten FR, et al. IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 2005;11:191-198 (Pubitemid 40321355)
12. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, et al. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 2007;447:1116-1120 (Pubitemid 47014427)
13. 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 (Pubitemid 46871350)
14. Mauer J, Chaurasia B, Plum L, et al. Myeloid cell-restricted insulin receptor deficiency protects against obesity-induced inflammation and systemic insulin resistance. PLoS Genet 2010;6:e1000938
15. Kiefer FW, Zeyda M, Gollinger K, et al. Neutralization of osteopontin inhibits obesity-induced inflammation and insulin resistance. Diabetes 2010;59:935-946
16. Féral CC, Neels JG, Kummer C, Slepak M, Olefsky JM, Ginsberg MH. Blockade of alpha4 integrin signaling ameliorates the metabolic consequences of high-fat diet-induced obesity. Diabetes 2008;57:1842-1851
17. Westcott DJ, Delproposto JB, Geletka LM, et al. MGL1 promotes adipose tissue inflammation and insulin resistance by regulating 7/4hi monocytes in obesity. J Exp Med 2009;206:3143-3156
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. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-α in human obesity and insulin resistance. J Clin Invest 1995;95:2409-2415
20. Heilbronn LK, Campbell LV. Adipose tissue macrophages, low grade inflammation and insulin resistance in human obesity. Curr Pharm Des 2008;14:1225-1230 (Pubitemid 351997835)
21. 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)
22. Ebert BL, Bunn HF. Regulation of the erythropoietin gene. Blood 1999;94:1864-1877 (Pubitemid 29430402)
23. Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 1992;12:5447-5454
24. Semenza GL. Involvement of oxygen-sensing pathways in physiologic and pathologic erythropoiesis. Blood 2009;114:2015-2019
25. Sohmiya M, Kakiba T, Kato Y. Therapeutic use of continuous subcutaneous infusion of recombinant human erythropoietin in malnourished predialysis anemic patients with diabetic nephropathy. Eur J Endocrinol 1998;139:367-370 (Pubitemid 28494079)
26. Noguchi CT, Wang L, Rogers HM, Teng R, Jia Y. Survival and proliferative roles of erythropoietin beyond the erythroid lineage. Expert Rev Mol Med 2008;10:e36
27. Kertesz N, Wu J, Chen TH, Sucov HM, Wu H. The role of erythropoietin in regulating angiogenesis. Dev Biol 2004;276:101-110 (Pubitemid 39452849)
28. Wu H, Lee SH, Gao J, Liu X, Iruela-Arispe ML. Inactivation of erythropoietin leads to defects in cardiac morphogenesis. Development 1999;126:3597-3605 (Pubitemid 29419516)
29. Yu X, Shacka JJ, Eells JB, et al. Erythropoietin receptor signalling is required for normal brain development. Development 2002;129:505-516 (Pubitemid 34863815)
30. Ueda K, Takano H, Niitsuma Y, et al. Sonic hedgehog is a critical mediator of erythropoietin-induced cardiac protection in mice. J Clin Invest 2010;120:2016-2029
31. Bernaudin M, Marti HH, Roussel S, et al. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 1999;19:643-651 (Pubitemid 30161216)
32. Villa P, Bigini P, Mennini T, et al. Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J Exp Med 2003;198:971-975 (Pubitemid 37152934)
33. Nairz M, Schroll A, Moschen AR, et al. Erythropoietin contrastingly affects bacterial infection and experimental colitis by inhibiting nuclear factor-κB-inducible immune pathways. Immunity 2011;34:61-74
34. Yuan R, Maeda Y, Li W, Lu W, Cook S, Dowling P. Erythropoietin: a potent inducer of peripheral immuno/inflammatory modulation in autoimmune EAE. PLoS One 2008;3:e1924
35. Foskett A, Alnaeeli M, Wang L, Teng R, Noguchi CT. The effects of erythropoietin dose titration during high-fat diet-induced obesity. J Biomed Biotechnol 2011;2011:373781
36. Teng R, Gavrilova O, Suzuki N, et al. Disrupted erythropoietin signalling promotes obesity and alters hypothalamus proopiomelanocortin production. Nat Commun 2011;2:520
37. Katz O, Stuible M, Golishevski N, et al. Erythropoietin treatment leads to reduced blood glucose levels and body mass: insights from murine models. J Endocrinol 2010;205:87-95
38. Hojman P, Brolin C, Gissel H, et al. Erythropoietin over-expression protects against diet-induced obesity in mice through increased fat oxidation in muscles. PLoS ONE 2009;4:e5894
39. Suzuki N, Ohneda O, Takahashi S, et al. Erythroid-specific expression of the erythropoietin receptor rescued its null mutant mice from lethality. Blood 2002;100:2279-2288
40. Choi D, Schroer SA, Lu SY, et al. Erythropoietin protects against diabetes through direct effects on pancreatic beta cells. J Exp Med 2010;207:2831-2842
41. Wang R-H, Kim H-S, Xiao C, Xu X, Gavrilova O, Deng CX. Hepatic Sirt1 deficiency in mice impairs mTorc2/Akt signaling and results in hyperglycemia, oxidative damage, and insulin resistance. J Clin Invest 2011;121:4477-4490
42. King IL, Dickendesher TL, Segal BM. Circulating Ly-6C+ myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood 2009;113:3190-3197
43. Krutzik PO, Nolan GP. Intracellular phospho-protein staining techniques for flow cytometry: monitoring single cell signaling events. Cytometry A 2003;55:61-70 (Pubitemid 37522508)
44. 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
45. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 2006;116:1793-1801 (Pubitemid 44033299)
46. Jenkins SJ, Ruckerl D, Cook PC, et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 2011;332:1284-1288
47. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity 2010;32:593-604
48. Brombacher F, Arendse B, Peterson R, Hölscher A, Hölscher C. Analyzing classical and alternative macrophage activation in macrophage/neutrophilspecific IL-4 receptor-α-deficient mice. Methods Mol Biol 2009;531:225-252
49. Herbert DR, Hölscher C, Mohrs M, et al. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 2004;20:623-635 (Pubitemid 38659504)
50. Takeda K, Tanaka T, Shi W, et al. Essential role of Stat6 in IL-4 signalling. Nature 1996;380:627-630 (Pubitemid 26119015)