Chronic kidney disease promotes chronic inflammation in visceral white adipose tissue

American Journal of Physiology - Renal Physiology

Volumn 312, Issue 4, 2017, Pages F689-F701

  Xiang, Dong Mei ^a   Song, Xiu Zhen ^a   Zhou, Zhan Mei ^a   Liu, Yang ^a   Dai, Xiao Yan ^a   Huang, Xiang Lan ^a   Hou, Fan Fan ^a   Zhou, Qiu Gen ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Chronic kidney disease; Inflammation; Macrophage; White adipose tissue

Indexed keywords

CD11B ANTIGEN; CHLORDANE; FATTY ACID; INTERLEUKIN 1; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PENTOBARBITAL; SILENT INFORMATION REGULATOR PROTEIN; TUMOR NECROSIS FACTOR; AUTACOID; CYTOKINE; SIRT1 PROTEIN, RAT; SIRTUIN 1;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CHRONIC INFLAMMATION; CHRONIC KIDNEY FAILURE; CONTROLLED STUDY; EX VIVO STUDY; INTRAPERITONEAL FAT; MALE; NONHUMAN; OXIDATIVE STRESS; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; RAT; RAT MODEL; RISK FACTOR; WHITE ADIPOSE TISSUE; ANIMAL; CELL COMMUNICATION; CELL CULTURE; COCULTURE; COMPLICATION; DISEASE MODEL; ENERGY METABOLISM; GENETICS; INTRAABDOMINAL FAT; MACROPHAGE; METABOLISM; PANNICULITIS; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TIME FACTOR;

ADIPOCYTES; ANIMALS; CELL COMMUNICATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; FATTY ACIDS, NONESTERIFIED; INFLAMMATION MEDIATORS; INTRA-ABDOMINAL FAT; MACROPHAGES; MALE; OXIDATIVE STRESS; PANNICULITIS; RATS, SPRAGUE-DAWLEY; RENAL INSUFFICIENCY, CHRONIC; SIGNAL TRANSDUCTION; SIRTUIN 1; TIME FACTORS;

EID: 85017011495     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00584.2016     Document Type: Article

References (39)

1. Akchurin OM, Kaskel F. Update on inflammation in chronic kidney disease. Blood Purif 39: 84-92, 2015. doi: 10.1159/000368940.
2. Axelsson J, Aström G, Sjölin E, Qureshi AR, Lorente-Cebrián S, Stenvinkel P, Rydén M. Uraemic sera stimulate lipolysis in human adipocytes: role of perilipin. Nephrol Dial Transplant 26: 2485-2491, 2011. doi: 10.1093/ndt/gfq755.
3. Boden G. Obesity and free fatty acids. Endocrinol Metab Clin North Am 37: 635-646, 2008. doi: 10.1016/j.ecl.2008.06.007.
4. Brookheart RT, Michel CI, Schaffer JE. As a matter of fat. Cell Metab 10: 9-12, 2009. doi: 10.1016/j.cmet.2009.03.011.
5. de Boer IH, Zelnick L, Afkarian M, Ayers E, Curtin L, Himmelfarb J, Ikizler TA, Kahn SE, Kestenbaum B, Utzschneider K. Impaired glucose and insulin homeostasis in moderate-severe CKD. J Am Soc Nephrol 27: 2861-2871, 2016.
6. 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. doi: 10.1172/JCI21625.
7. Grant RW, Dixit VD. Adipose tissue as an immunological organ. Obesity (Silver Spring) 23: 512-518, 2015. doi: 10.1002/oby.21003.
8. Hajri T, Hall AM, Jensen DR, Pietka TA, Drover VA, Tao H, Eckel R, Abumrad NA. CD36-facilitated fatty acid uptake inhibits leptin production and signaling in adipose tissue. Diabetes 56: 1872-1880, 2007. doi: 10.2337/db06-1699.
9. Hammond E, McKinnon E, Nolan D. Human immunodeficiency virus treatment-induced adipose tissue pathology and lipoatrophy: prevalence and metabolic consequences. Clin Infect Dis 51: 591-599, 2010. doi: 10.1086/655765.
10. Huang S, Rutkowsky JM, Snodgrass RG, Ono-Moore KD, Schneider DA, Newman JW, Adams SH, Hwang DH. Saturated fatty acids activate TLR-mediated proinflammatory signaling pathways. J Lipid Res 53: 2002-2013, 2012. doi: 10.1194/jlr.D029546.
11. Kao MP, Ang DS, Pall A, Struthers AD. Oxidative stress in renal dysfunction: mechanisms, clinical sequelae and therapeutic options. J Hum Hypertens 24: 1-8, 2010. doi: 10.1038/jhh.2009.70.
12. Kauppinen A, Suuronen T, Ojala J, Kaarniranta K, Salminen A. Antagonistic crosstalk between NF-κB and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Signal 25: 1939-1948, 2013. doi: 10.1016/j.cellsig.2013.06.007.
13. Keane WF, Tomassini JE, Neff DR. Lipid abnormalities in patients with chronic kidney disease. Contrib Nephrol 171: 135-142, 2011. doi: 10.1159/000327317.
14. Kusminski CM, Bickel PE, Scherer PE. Targeting adipose tissue in the treatment of obesity-associated diabetes. Nat Rev Drug Discov 15: 639-660, 2016. doi: 10.1038/nrd.2016.75.
15. Laine PS, Schwartz EA, Wang Y, Zhang WY, Karnik SK, Musi N, Reaven PD. Palmitic acid induces IP-10 expression in human macrophages via NF-kappaB activation. Biochem Biophys Res Commun 358: 150-155, 2007. doi: 10.1016/j.bbrc.2007.04.092.
16. Li C, Ding XY, Xiang DM, Xu J, Huang XL, Hou FF, Zhou QG. Enhanced M1 and impaired M2 macrophage polarization and reduced mitochondrial biogenesis via inhibition of AMP kinase in chronic kidney disease. Cell Physiol Biochem 36: 358-372, 2015. doi: 10.1159/000430106.
17. McLaughlin T, Liu LF, Lamendola C, Shen L, Morton J, Rivas H, Winer D, Tolentino L, Choi O, Zhang H, Hui Yen Chng M, Engleman E. T-cell profile in adipose tissue is associated with insulin resistance and systemic inflammation in humans. Arterioscler Thromb Vasc Biol 34: 2637-2643, 2014. doi: 10.1161/ATVBAHA.114.304636.
18. Minakuchi H, Wakino S, Hosoya K, Sueyasu K, Hasegawa K, Shinozuka K, Yoshifuji A, Futatsugi K, Komatsu M, Kanda T, Tokuyama H, Hayashi K, Itoh H. The role of adipose tissue asymmetric dimethylarginine/ dimethylarginine dimethylaminohydrolase pathway in adipose tissue phenotype and metabolic abnormalities in subtotally nephrectomized rats. Nephrol Dial Transplant 31: 413-423, 2016. doi: 10.1093/ndt/ gfv367.
19. Nguyen A, Tao H, Metrione M, Hajri T. Very low density lipoprotein receptor (VLDLR) expression is a determinant factor in adipose tissue inflammation and adipocyte-macrophage interaction. J Biol Chem 289: 1688-1703, 2014. doi: 10.1074/jbc.M113.515320.
20. Pearson KJ, Baur JA, Lewis KN, Peshkin L, Price NL, Labinskyy N, Swindell WR, Kamara D, Minor RK, Perez E, Jamieson HA, Zhang Y, Dunn SR, Sharma K, Pleshko N, Woollett LA, Csiszar A, Ikeno Y, Le Couteur D, Elliott PJ, Becker KG, Navas P, Ingram DK, Wolf NS, Ungvari Z, Sinclair DA, de Cabo R. Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell Metab 8: 157-168, 2008. doi: 10.1016/ j.cmet.2008.06.011.
21. Pelletier CC, Koppe L, Croze ML, Kalbacher E, Vella RE, Guebre-Egziabher F, Géloën A, Badet L, Fouque D, Soulage CO. White adipose tissue overproduces the lipid-mobilizing factor zinc α2-glycoprotein in chronic kidney disease. Kidney Int 83: 878-886, 2013. doi: 10.1038/ki.2013.9.
22. Preyat N, Leo O. Sirtuin deacylases: a molecular link between metabolism and immunity. J Leukoc Biol 93: 669-680, 2013. doi: 10.1189/jlb.1112557.
23. Ruan XZ, Moorhead JF, Varghese Z. Lipid redistribution in renal dysfunction. Kidney Int 74: 407-409, 2008. doi: 10.1038/ki.2008.226.
24. Schilling JD, Machkovech HM, He L, Sidhu R, Fujiwara H, Weber K, Ory DS, Schaffer JE. Palmitate and lipopolysaccharide trigger synergistic ceramide production in primary macrophages. J Biol Chem 288: 2923-2932, 2013. doi: 10.1074/jbc.M112.419978.
25. 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 116: 3015-3025, 2006. doi: 10.1172/JCI28898.
26. Snodgrass RG, Boß M, Zezina E, Weigert A, Dehne N, Fleming I, Brüne B, Namgaladze D. Hypoxia potentiates palmitate-induced proinflammatory activation of primary human macrophages. J Biol Chem 291: 413-424, 2016. doi: 10.1074/jbc.M115.686709.
27. Stockler-Pinto MB, Saldanha JF, Yi D, Mafra D, Fouque D, Soulage CO. The uremic toxin indoxyl sulfate exacerbates reactive oxygen species production and inflammation in 3T3-L1 adipose cells. Free Radic Res 50: 337-344, 2016. doi: 10.3109/10715762.2015.1125996.
28. Suganami T, Nishida J, Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler Thromb Vasc Biol 25: 2062-2068, 2005. doi: 10.1161/01.ATV.0000183883.72263.13.
29. Suganami T, Tanimoto-Koyama K, Nishida J, Itoh M, Yuan X, Mizuarai S, Kotani H, Yamaoka S, Miyake K, Aoe S, Kamei Y, Ogawa Y. Role of the Toll-like receptor 4/NF-kappaB pathway in saturated fatty acid-induced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler Thromb Vasc Biol 27: 84-91, 2007. doi: 10.1161/01.ATV.0000251608.09329.9a.
30. Weber K, Schilling JD. Lysosomes integrate metabolic-inflammatory cross-talk in primary macrophage inflammasome activation. J Biol Chem 289: 9158-9171, 2014. doi: 10.1074/jbc.M113.531202.
31. 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. doi: 10.1172/ JCI200319246.
32. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT, Brickey WJ, Ting JP. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 12: 408-415, 2011. doi: 10.1038/ni.2022.
33. Winer S, Winer DA. The adaptive immune system as a fundamental regulator of adipose tissue inflammation and insulin resistance. Immunol Cell Biol 90: 755-762, 2012. doi: 10.1038/icb.2011.110.
34. 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. doi: 10.1172/JCI200319451.
35. Xu H, Huang X, Arnlöv J, Cederholm T, Stenvinkel P, Lindholm B, Risérus U, Carrero JJ. Clinical correlates of insulin sensitivity and its association with mortality among men with CKD stages 3 and 4. Clin J Am Soc Nephrol 9: 690-697, 2014. doi: 10.2215/CJN.05230513.
36. Zhou QG, Fu XJ, Xu GY, Cao W, Liu HF, Nie J, Liang M, Hou FF. Vascular insulin resistance related to endoplasmic reticulum stress in aortas from a rat model of chronic kidney disease. Am J Physiol Heart Circ Physiol 303: H1154-H1165, 2012. doi: 10.1152/ajpheart.00407.2012.
37. Zhou QG, Hou FF, Guo ZJ, Liang M, Wang GB, Zhang X. 1,25-Dihydroxyvitamin D improved the free fatty-acid-induced insulin resistance in cultured C2C12 cells. Diabetes Metab Res Rev 24: 459-464, 2008. doi: 10.1002/dmrr.873.
38. Zhou QG, Zhou M, Hou FF, Peng X. Asymmetrical dimethylarginine triggers lipolysis and inflammatory response via induction of endoplasmic reticulum stress in cultured adipocytes. Am J Physiol Endocrinol Metab 296: E869-E878, 2009. doi: 10.1152/ajpendo.91011.2008.
39. Zhu Y, Chen YL, Li C, Ding XY, Xu GY, Hu LL, Hou FF, Zhou QG. The effect of inhibition of endoplasmic reticulum stress on lipolysis in white adipose tissue in a rat model of chronic kidney disease. Acta Pharmacol Sin 35: 356-362, 2014. doi: 10.1038/aps.2013.177.