Nitric oxide produced by macrophages inhibits adipocyte differentiation and promotes profibrogenic responses in preadipocytes to induce adipose tissue fibrosis

Diabetes

Volumn 65, Issue 9, 2016, Pages 2516-2528

  Jang, Jung Eun ^a,b   Ko, Myoung Seok ^b   Yun, Ji Young ^b   Kim, Mi Ok ^b   Kim, Jin Hee ^b   Park, Hye Sun ^b   Kim, Ah Ram ^b   Kim, Hyuk Joong ^b   Kim, Bum Joong ^b   Ahn, Young Eun ^a,b   Oh, Jin Sun ^a,b   Lee, Woo Je ^a,b   Harris, Robert A ^c   Koh, Eun Hee ^a,b   Lee, Ki Up ^a,b  

^a University of Ulsan College of Medicine   (South Korea)

^b Asan Institute for Life Sciences   (South Korea)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; ALPHA SMOOTH MUSCLE ACTIN; ARGINASE 1; CD209 ANTIGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 1ALPHA; COLLAGEN TYPE 3ALPHA; CYCLOOXYGENASE 1; CYCLOOXYGENASE IV; CYCLOOXYGENASE V; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; HYPOXIA INDUCIBLE FACTOR 3ALPHA; INTERLEUKIN 10; INTERLEUKIN 6; MACROPHAGE GALACTOSE TYPE C TYPE LECTIN 2; MANNOSE RECEPTOR; MANNOSE RECEPTOR 1; MESSENGER RNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN P21; PROTEIN P53; ROSIGLITAZONE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; ENZYME INHIBITOR; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRITE; S-METHYLISOTHIOPSEUDOURONIUM; THIOUREA DERIVATIVE;

ADIPOCYTE; ADIPOSE TISSUE FIBROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA DAMAGE; FIBROGENESIS; FIBROSIS; GENETIC TRANSCRIPTION; INFLAMMATORY INFILTRATE; INSULIN RESISTANCE; LIPID STORAGE; MACROPHAGE; MALE; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE TOLERANCE TEST; KNOCKOUT MOUSE; METABOLISM; RAW 264.7 CELL LINE;

ADIPOCYTES; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; ENZYME INHIBITORS; FIBROSIS; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE TOLERANCE TEST; ISOTHIURONIUM; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; RAW 264.7 CELLS;

EID: 84987638172     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-1624     Document Type: Article

References (50)

1. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 2011;11:98-107
2. Sun K, Tordjman J, Clément K, Scherer PE. Fibrosis and adipose tissue dysfunction. Cell Metab 2013;18:470-477
3. Buechler C, Krautbauer S, Eisinger K. Adipose tissue fibrosis. World J Diabetes 2015;6:548-553
4. Charbonneau A, Marette A. Inducible nitric oxide synthase induction underlies lipid-induced hepatic insulin resistance in mice: potential role of tyrosine nitration of insulin signaling proteins. Diabetes 2010;59:861-871
5. Perreault M, Marette A. Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat Med 2001; 7:1138-1143
6. Aram G, Potter JJ, Liu X, Torbenson MS, Mezey E. Lack of inducible nitric oxide synthase leads to increased hepatic apoptosis and decreased fibrosis in mice after chronic carbon tetrachloride administration. Hepatology 2008;47:2051-2058
7. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007;117:175-184
8. Shaul ME, Bennett G, Strissel KJ, Greenberg AS, Obin MS. Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during highfat diet-induced obesity in mice. Diabetes 2010;59:1171-1181
9. Tsuchiya K, Sakai H, Suzuki N, et al. Chronic blockade of nitric oxide synthesis reduces adiposity and improves insulin resistance in high fat-induced obese mice. Endocrinology 2007;148:4548-4556
10. Halberg N, Khan T, Trujillo ME, et al. Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol 2009;29:4467-4483
11. Jiang C, Qu A, Matsubara T, et al. Disruption of hypoxia-inducible factor 1 in adipocytes improves insulin sensitivity and decreases adiposity in high-fat dietfed mice. Diabetes 2011;60:2484-2495
12. Sun K, Halberg N, Khan M, Magalang UJ, Scherer PE. Selective inhibition of hypoxia-inducible factor 1α ameliorates adipose tissue dysfunction. Mol Cell Biol 2013;33:904-917
13. Brüne B, Zhou J. Nitric oxide and superoxide: interference with hypoxic signaling. Cardiovasc Res 2007;75:275-282
14. Kleinert H, Pautz A, Linker K, Schwarz PM. Regulation of the expression of inducible nitric oxide synthase. Eur J Pharmacol 2004;500:255-266
15. Hagen T, Taylor CT, Lam F, Moncada S. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 2003;302:1975-1978
16. Sandau KB, Fandrey J, Brüne B. Accumulation of HIF-1alpha under the influence of nitric oxide. Blood 2001;97:1009-1015
17. Brown GC, Borutaite V. Nitric oxide and mitochondrial respiration in the heart. Cardiovasc Res 2007;75:283-290
18. Nisoli E, Clementi E, Paolucci C, et al. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003;299:896-899
19. Dromparis P, Paulin R, Sutendra G, Qi AC, Bonnet S, Michelakis ED. Uncoupling protein 2 deficiency mimics the effects of hypoxia and endoplasmic reticulum stress on mitochondria and triggers pseudohypoxic pulmonary vascular remodeling and pulmonary hypertension. Circ Res 2013;113:126-136
20. Shimizu I, Yoshida Y, Moriya J, et al. Semaphorin3E-induced inflammation contributes to insulin resistance in dietary obesity. Cell Metab 2013;18:491-504
21. Shimizu I, Yoshida Y, Suda M, Minamino T. DNA damage response and metabolic disease. Cell Metab 2014;20:967-977
22. Stewart SA, Weinberg RA. Telomeres: cancer to human aging. Annu Rev Cell Dev Biol 2006;22:531-557
23. Sahin E, Colla S, Liesa M, et al. Telomere dysfunction induces metabolic and mitochondrial compromise. Nature 2011;470:359-365
24. Mao K, Chen S, Chen M, et al. Nitric oxide suppresses NLRP3 inflammasome activation and protects against LPS-induced septic shock. Cell Res 2013;23:201-212
25. Chalkiadaki A, Guarente L. High-fat diet triggers inflammation-induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metab 2012;16:180-188
26. Szabó C, Southan GJ, Thiemermann C. Beneficial effects and improved survival in rodent models of septic shock with S-methylisothiourea sulfate, a potent and selective inhibitor of inducible nitric oxide synthase. Proc Natl Acad Sci U S A 1994;91:12472-12476
27. Koh EH, Park JY, Park HS, et al. Essential role of mitochondrial function in adiponectin synthesis in adipocytes. Diabetes 2007;56:2973-2981
28. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA doublestranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998;273:5858-5868
29. Pennathur S, Vivekanandan-Giri A, Locy ML, et al. Oxidative modifications of protein tyrosyl residues are increased in plasma of human subjects with interstitial lung disease. Am J Respir Crit Care Med 2016;193:861-868
30. Koh EH, Kim AR, Kim H, et al. 11β-HSD1 reduces metabolic efficacy and adiponectin synthesis in hypertrophic adipocytes. J Endocrinol 2015;225:147-158
31. Lee J. Adipose tissue macrophages in the development of obesity-induced inflammation, insulin resistance and type 2 diabetes. Arch Pharm Res 2013;36:208-222
32. Yang S, Wang B, Humphries F, Hogan AE, O'Shea D, Moynagh PN. The E3 ubiquitin ligase Pellino3 protects against obesity-induced inflammation and insulin resistance. Immunity 2014;41:973-987
33. Keith B, Johnson RS, Simon MC. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 2011;12:9-22
34. Dai DF, Rabinovitch PS, Ungvari Z. Mitochondria and cardiovascular aging. Circ Res 2012;110:1109-1124
35. Cani PD, Bibiloni R, Knauf C, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008;57:1470-1481
36. Sorisky A, Molgat AS, Gagnon A. Macrophage-induced adipose tissue dysfunction and the preadipocyte: should I stay (and differentiate) or should I go? Adv Nutr 2013;4:67-75
37. Keophiphath M, Achard V, Henegar C, Rouault C, Clément K, Lacasa D. Macrophage-secreted factors promote a profibrotic phenotype in human preadipocytes. Mol Endocrinol 2009;23:11-24
38. Lacasa D, Taleb S, Keophiphath M, Miranville A, Clement K. Macrophagesecreted factors impair human adipogenesis: involvement of proinflammatory state in preadipocytes. Endocrinology 2007;148:868-877
39. Gagnon A, Yarmo MN, Landry A, Sorisky A. Macrophages alter the differentiation-dependent decreases in fibronectin and collagen I/III protein levels in human preadipocytes. Lipids 2012;47:873-880
40. Brüne B, Schneiderhan N. Nitric oxide evoked p53-accumulation and apoptosis. Toxicol Lett 2003;139:119-123
41. Banin S, Moyal L, Shieh S, et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 1998;281:1674-1677
42. Sperka T, Wang J, Rudolph KL. DNA damage checkpoints in stem cells, ageing and cancer. Nat Rev Mol Cell Biol 2012;13:579-590
43. Hahn WS, Kuzmicic J, Burrill JS, et al. Proinflammatory cytokines differentially regulate adipocyte mitochondrial metabolism, oxidative stress, and dynamics. Am J Physiol Endocrinol Metab 2014;306:E1033-E1045
44. Hartupee J, Mann DL. Role of inflammatory cells in fibroblast activation. J Mol Cell Cardiol 2016;93:143-148
45. Braga TT, Agudelo JS, Camara NO. Macrophages during the fibrotic process: M2 as friend and foe. Front Immunol 2015;6:602
46. Becerril S, Rodríguez A, Catalán V, et al. Deletion of inducible nitric-oxide synthase in leptin-deficient mice improves brown adipose tissue function. PLoS One 2010;5:e10962
47. Lu M, Li P, Pferdekamper J, et al. Inducible nitric oxide synthase deficiency in myeloid cells does not prevent diet-induced insulin resistance. Mol Endocrinol 2010;24:1413-1422
48. Chen Y, Hozawa S, Sawamura S, et al. Deficiency of inducible nitric oxide synthase exacerbates hepatic fibrosis in mice fed high-fat diet. Biochem Biophys Res Commun 2005;326:45-51
49. Nozaki Y, Fujita K, Wada K, et al. Deficiency of iNOS-derived NO accelerates lipid accumulation-independent liver fibrosis in non-alcoholic steatohepatitis mouse model. BMC Gastroenterol 2015;15:42
50. Anavi S, Eisenberg-Bord M, Hahn-Obercyger M, Genin O, Pines M, Tirosh O. The role of iNOS in cholesterol-induced liver fibrosis. Lab Invest 2015;95:914-924