P65 inactivation in adipocytes and macrophages attenuates adipose inflammatory response in lean but not in obese mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 308, Issue 6, 2015, Pages E496-E505

  Gao, Zhanguo ^a,b   Zhang, Jin ^b   Henagan, Tara M ^b,c   Lee, Jong Han ^b   Ye, Xin ^b   Wang, Hui ^a   Ye, Jianping ^b  

^a XINXIANG MEDICAL UNIVERSITY   (China)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Apoptosis; Crown like structure; Inflammation; Macrophage polarization; Nuclear factor B

Indexed keywords

GLUCOSE; SYNAPTOTAGMIN I; AUTACOID; RELA PROTEIN, MOUSE; TRANSCRIPTION FACTOR RELA;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BODY FAT; BODY WEIGHT; CHRONIC INFLAMMATION; CONTROLLED STUDY; ENERGY EXPENDITURE; FOOD INTAKE; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; INFLAMMATION; INSULIN TOLERANCE TEST; LIGHT DARK CYCLE; LOXP SITE; MACROPHAGE; MACROPHAGE ACTIVATION; MEDICAL RESEARCH; MOUSE; NONHUMAN; OBESITY; OXYGEN CONSUMPTION; PHYSICAL ACTIVITY; POLARIZATION; PRIORITY JOURNAL; ROOM TEMPERATURE; WEIGHT REDUCTION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; COMPLICATION; GENE SILENCING; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE MUTANT; PANNICULITIS; PATHOLOGY;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; GENE SILENCING; INFLAMMATION MEDIATORS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, OBESE; OBESITY; PANNICULITIS; THINNESS; TRANSCRIPTION FACTOR RELA;

EID: 84937458513     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00532.2014     Document Type: Article

References (60)

1. Alkhouri N, Gornicka A, Berk MP, Thapaliya S, Dixon LJ, Kashyap S, Schauer PR, Feldstein AE. Adipocyte apoptosis, a link between obesity, insulin resistance, and hepatic steatosis. J Biol Chem 285: 3428-3438, 2010.
2. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, Wynshaw-Boris A, Poli G, Olefsky J, Karin M. IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 11: 191-198, 2005.
3. Arner E, Westermark PO, Spalding KL, Britton T, Ryden M, Frisen J, Bernard S, Arner P. Adipocyte turnover: relevance to human adipose tissue morphology. Diabetes 59: 105-109, 2010.
4. Baker RG, Hayden MS, Ghosh S. NF-κB, inflammation, and metabolic Disease. Cell Metab 13: 11-22, 2011.
5. Bluher M, Klöting N, Wueest S, Schoenle EJ, Schön MR, Dietrich A, Fasshauer M, Stumvoll M, Konrad D. Fas and FasL expression in human adipose tissue is related to obesity, insulin resistance, and type 2 diabetes. J Clin Endocrinol Metab 99: E36-E44, 2014.
6. Boord JB, Maeda K, Makowski L, Babaev VR, Fazio S, Linton MF, Hotamisligil GS. Combined adipocyte-macrophage fatty acid-binding protein deficiency improves metabolism, atherosclerosis, and survival in apolipoprotein E-deficient mice. Circulation 110: 1492-1498, 2004.
7. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, Wang S, Fortier M, Greenberg AS, Obin MS. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 46: 2347-2355, 2005.
8. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11: 98-107, 2011.
9. Eguchi J, Wang X, Yu S, Kershaw EE, Chiu PC, Dushay J, Estall JL, Klein U, Maratos-Flier E, Rosen ED. Transcriptional control of adipose lipid handling by IRF4. Cell Metab 13: 249-259, 2011.
10. Fleischman A, Shoelson SE, Bernier R, Goldfine AB. Salsalate improves glycemia and inflammatory parameters in obese young adults. Diabetes Care 31: 289-294, 2008.
11. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114: 1752-1761, 2004.
12. Goldfine AB, Conlin PR, Halperin F, Koska J, Permana P, Schwenke D, Shoelson SE, Reaven PD. A randomised trial of salsalate for insulin resistance and cardiovascular risk factors in persons with abnormal glucose tolerance. Diabetologia 56: 714-723, 2013.
13. Goldfine AB, Fonseca V, Jablonski KA, Chen YD, Tipton L, Staten MA, Shoelson SE; Targeting Inflammation Using Salsalate in Type 2 Diabetes Study Team. Salicylate (salsalate) in patients with type 2 diabetes: a randomized trial. Ann Intern Med 159: 1-12, 2013.
14. Goldfine AB, Silver R, Aldhahi W, Cai D, Tatro E, Lee J, Shoelson SE. Use of salsalate to target inflammation in the treatment of insulin resistance and type 2 diabetes. Clin Transl Sci 1: 36-43, 2008.
15. Han MS, Jung DY, Morel C, Lakhani SA, Kim JK, Flavell RA, Davis RJ. JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation. Science 339: 218-222, 2013.
16. He W, Barak Y, Hevener A, Olson P, Liao D, Le J, Nelson M, Ong E, Olefsky JM, Evans RM. Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci USA 100: 15712-15717, 2003.
17. Herrero L, Shapiro H, Nayer A, Lee J, Shoelson SE. Inflammation and adipose tissue macrophages in lipodystrophic mice. Proc Natl Acad Sci USA 107: 240-245, 2010.
18. Hirosumi J, Tuncman G, Chang L, Gorgun C, Uysal K, Maeda K, Karin M, Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature 420: 333-336, 2002.
19. Hofmann SM, Zhou L, Perez-Tilve D, Greer T, Grant E, Wancata L, Thomas A, Pfluger PT, Basford JE, Gilham D, Herz J, Tschop MH, Hui DY. Adipocyte LDL receptor-related protein-1 expression modulates postprandial lipid transport and glucose homeostasis in mice. J Clin Invest 117: 3271-3282, 2007.
20. Hosogai N, Fukuhara A, Oshima K, Miyata Y, Tanaka S, Segawa K, Furukawa S, Tochino Y, Komuro R, Matsuda M, Shimomura I. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 56: 901-911, 2007.
21. Jiao P, Feng B, Ma J, Nie Y, Paul E, Li Y, Xu H. Constitutive activation of IKKβ in adipose tissue prevents diet-induced obesity in mice. Endocrinology 153: 154-165, 2012.
22. Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol 3: 221-227, 2002.
23. Keuper M, Wernstedt Asterholm I, Scherer PE, Westhoff MA, Möller P, Debatin KM, Strauss G, Wabitsch M, Fischer-Posovszky P. TRAIL (TNF-related apoptosis-inducing ligand) regulates adipocyte metabolism by caspase-mediated cleavage of PPARgamma. Cell Death Dis 4: e474, 2013.
24. Kumar A, Lawrence JC Jr, Jung DY, Ko HJ, Keller SR, Kim JK, Magnuson MA, Harris TE. Fat cell-specific ablation of rictor in mice impairs insulin-regulated fat cell and whole-body glucose and lipid metabolism. Diabetes 59: 1397-1406, 2010.
25. Lee JY, Ye J, Gao Z, Youn HS, Lee WH, Zhao L, Sizemore N, Hwang DH. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J Biol Chem 278: 37041-37051, 2003.
26. Lee KY, Russell SJ, Ussar S, Boucher J, Vernochet C, Mori MA, Smyth G, Rourk M, Cederquist C, Rosen E, Kahn B, Kahn CR. Lessons on conditional gene targeting in mouse adipose tissue. Diabetes 62: 864-874, 2013.
27. Lee YH, Petkova AP, Granneman JG. Identification of an adipogenic niche for adipose tissue remodeling and restoration. Cell Metab 18: 355-367, 2013.
28. 2 consumption triggers HIF-1α, causing inflammation and insulin resistance in obesity. Cell 157: 1339-1352, 2014.
29. Li P, Fan W, Xu J, Lu M, Yamamoto H, Auwerx J, Sears DD, Talukdar S, Oh D, Chen A, Bandyopadhyay G, Scadeng M, Ofrecio JM, Nalbandian S, Olefsky JM. Adipocyte NCoR knockout decreases PPARgamma phosphorylation and enhances PPARgamma activity and insulin sensitivity. Cell 147: 815-826, 2011.
30. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117: 175-184, 2007.
31. Makowski L, Boord JB, Maeda K, Babaev VR, Uysal KT, Morgan MA, Parker RA, Suttles J, Fazio S, Hotamisligil GS, Linton MF. Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat Med 7: 699-705, 2001.
32. Mullican SE, Tomaru T, Gaddis CA, Peed LC, Sundaram A, Lazar MA. A novel adipose-specific gene deletion model demonstrates potential pitfalls of existing methods. Mol Endocrinol 27: 127-134, 2013.
33. Nagel SA, Keuper M, Zagotta I, Enlund E, Ruperez AI, Debatin KM, Wabitsch M, Fischer-Posovszky P. Up-regulation of Bcl-2 during adipogenesis mediates apoptosis resistance in human adipocytes. Mol Cell Endocrinol 382: 368-376, 2014.
34. Ogihara T, Asano T, Katagiri H, Sakoda H, Anai M, Shojima N, Ono H, Fujishiro M, Kushiyama A, Fukushima Y, Kikuchi M, Noguchi N, Aburatani H, Gotoh Y, Komuro I, Fujita T. Oxidative stress induces insulin resistance by activating the nuclear factor-kappaB pathway and disrupting normal subcellular distribution of phosphatidylinositol 3-kinase. Diabetologia 47: 794-805, 2004.
35. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH, Hotamisligil GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461, 2004.
36. Pajvani UB, Trujillo ME, Combs TP, Iyengar P, Jelicks L, Roth KA, Kitsis RN, Scherer PE. Fat apoptosis through targeted activation of caspase 8: a new mouse model of inducible and reversible lipoatrophy. Nat Med 11: 797-803, 2005.
37. Papa S, Zazzeroni F, Bubici C, Jayawardena S, Alvarez K, Matsuda S, Nguyen DU, Pham CG, Nelsbach AH, Melis T, Smaele ED, Tang WJ, D'Adamio L, Franzoso G. Gadd45beta mediates the NF-kappaB suppression of JNK signalling by targeting MKK7/JNKK2. Nat Cell Biol 6: 146-153, 2004.
38. Prins JB, Niesler CU, Winterford CM, Bright NA, Siddle K, O'Rahilly S, Walker NI, Cameron DP. Tumor necrosis factor-alpha induces apoptosis of human adipose cells. Diabetes 46: 1939-1944, 1997.
39. Qiu Y, Nguyen KD, Odegaard JI, Cui X, Tian X, Locksley RM, Palmiter RD, Chawla A. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 157: 1292-1308, 2014.
40. Sabio G, Das M, Mora A, Zhang Z, Jun JY, Ko HJ, Barrett T, Kim JK, Davis RJ. A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 322: 1539-1543, 2008.
41. Samuel VT, Shulman GI. Mechanisms for insulin resistance: common threads and missing links. Cell 148: 852-871, 2012.
42. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 116: 1793-1801, 2006.
43. Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, Blomqvist L, Hoffstedt J, Naslund E, Britton T, Concha H, Hassan M, Ryden M, Frisen J, Arner P. Dynamics of fat cell turnover in humans. Nature 453: 783-787, 2008.
44. Strissel KJ, Stancheva Z, Miyoshi H, Perfield JW 2nd, DeFuria J, Jick Z, Greenberg AS, Obin MS. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 56: 2910-2918, 2007.
45. Talukdar S, Oh DY, Bandyopadhyay G, Li D, Xu J, McNelis J, Lu M, Li P, Yan Q, Zhu Y, Ofrecio J, Lin M, Brenner MB, Olefsky JM. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 18: 1407-1412, 2012.
46. Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M, Lin A. Inhibition of JNK activation through NF-kappaB target genes. Nature 414: 313-317, 2001.
47. Tang T, Zhang J, Yin J, Staszkiewicz J, Gawronska-Kozak B, Jung DY, Ko HJ, Ong H, Kim JK, Mynatt R, Martin RJ, Keenan M, Gao Z, Ye J. Uncoupling of inflammation and insulin resistance by NF-kappaB in transgenic mice through elevated energy expenditure. J Biol Chem 285: 4637-4644, 2010.
48. Wang QA, Tao C, Gupta RK, Scherer PE. Tracking adipogenesis during white adipose tissue development, expansion and regeneration. Nat Med 19: 1338-1344, 2013.
49. 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 112: 1796-1808, 2003.
50. Wernstedt Asterholm I, Tao C, Morley TS, Wang QA, Delgado-Lopez F, Wang ZV, Scherer PE. Adipocyte inflammation is essential for healthy adipose tissue expansion and remodeling. Cell Metab 20: 103-118, 2014.
51. Wu D, Molofsky AB, Liang HE, Ricardo-Gonzalez RR, Jouihan HA, Bando JK, Chawla A, Locksley RM. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332: 243-247, 2011.
52. Wueest S, Rapold RA, Schumann DM, Rytka JM, Schildknecht A, Nov O, Chervonsky AV, Rudich A, Schoenle EJ, Donath MY, Konrad D. Deletion of Fas in adipocytes relieves adipose tissue inflammation and hepatic manifestations of obesity in mice. J Clin Invest 120: 191-202, 2010.
53. Xu F, Burk D, Gao Z, Yin J, Zhang X, Weng J, Ye J. Angiogenic deficiency and adipose tissue dysfunction are associated with macrophage malfunction in SIRT1-/-mice. Endocrinology 153 1706-1716, 2012.
54. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830, 2003.
55. Ye J. Mechanisms of insulin resistance in obesity. Front Med 7: 14-24, 2013.
56. 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 293: E1118-E1128, 2007.
57. Ye J, McGuinness OP. Inflammation during obesity is not all bad: evidence from animal and human studies. Am J Physiol Endocrinol Metab 304: E466-E477, 2013.
58. Yin J, Gao Z, He Q, Ye J. Role of hypoxia in obesity-induced disorders of glucose and lipid metabolism in adipose tissue. Am J Physiol Endocrinol Metab 296: E333-E342, 2009.
59. Zhang J, Wang Y, Gao Z, Yun Z, Ye J. Hypoxia-inducible factor 1 activation from adipose protein 2-cre mediated knockout of von hippellindau gene leads to embryonic lethality. Clin Exp Pharmacol Physiol 39: 145-150, 2012.
60. Zhang N, Ahsan MH, Zhu L, Sambucetti LC, Purchio AF, West DB. NF-kappaB and not the MAPK signaling pathway regulates GADD45beta expression during acute inflammation. J Biol Chem 280: 21400-21408, 2005.