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Review

Characterization and Treatment of Inflammation and Insulin Resistance in Obese Adipose Tissue

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Pages 3449-3460 | Published online: 01 Oct 2020

References

  • Sung H, Siegel RL, Torre LA, et al. Global patterns in excess body weight and the associated cancer burden. CA Cancer J Clin. 2019;69(2):88–112.
  • Andersen LB, Mota J, Di Pietro L. Update on the global pandemic of physical inactivity. Lancet. 2016;388(10051):1255–1256. doi:10.1016/S0140-6736(16)30960-6
  • Tomiyama AJ. Stress and obesity. Ann Rev Psychol. 2019;70(1):703–718. doi:10.1146/annurev-psych-010418-102936
  • Yang C, Kong APS, Cai Z, Chung ACK. Persistent organic pollutants as risk factors for obesity and diabetes. Curr Diab Rep. 2017;17(12).
  • WHO. Obesity and overweight fact sheet; 2018. Available from: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight.
  • Murtagh E. Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults. Lancet. 2017;390(10113):2627–2642.
  • Lauby-Secretan B, Scoccianti C, Loomis D, Grosse Y, Bianchini F, Straif K. Body fatness and cancer–viewpoint of the IARC working group. N Engl J Med. 2016;375(8):794–798. doi:10.1056/NEJMsr1606602
  • Gadde KM, Martin CK, Berthoud H-R, Heymsfield SB. Obesity pathophysiology and management. J Am Coll Cardiol. 2018;71(1):69–84. doi:10.1016/j.jacc.2017.11.011
  • Greco F, Mallio CA, Grippo R, et al. Increased visceral adipose tissue in male patients with non-clear cell renal cell carcinoma. Radiol Med. 2020;125(6):538–543. doi:10.1007/s11547-020-01146-6
  • Greco F, Quarta LG, Grasso RF, Beomonte Zobel B, Mallio CA. Increased visceral adipose tissue in clear cell renal cell carcinoma with and without peritumoral collateral vessels. Br J Radiol. 2020;93(1112):20200334. doi:10.1259/bjr.20200334
  • Matrone A, Ferrari F, Santini F, Elisei R. Obesity as a risk factor for thyroid cancer. Curr Opin Endocrinol Diabetes Obes. 2020;27(5):358–363. doi:10.1097/MED.0000000000000556
  • Silveira EA, Kliemann N, Noll M, Sarrafzadegan N, de Oliveira C. Visceral obesity and incident cancer and cardiovascular disease: an integrative review of the epidemiological evidence. Obes Rev. 2020. doi:10.1111/obr.13088
  • Hossain P, Kawar B, El Nahas M. Obesity and diabetes in the developing world–a growing challenge. N Engl J Med. 2007;356(3):213–215. doi:10.1056/NEJMp068177
  • Jiang G, Luk AO, Tam CHT, et al. Obesity, clinical, and genetic predictors for glycemic progression in Chinese patients with type 2 diabetes: a cohort study using the Hong Kong diabetes register and Hong Kong diabetes biobank. PLoS Med. 2020;17(7):e1003209. doi:10.1371/journal.pmed.1003209
  • Pellegrinelli V, Carobbio S, Vidal-Puig A. Adipose tissue plasticity: how fat depots respond differently to pathophysiological cues. Diabetologia. 2016;59(6):1075–1088. doi:10.1007/s00125-016-3933-4
  • Giralt M, Villarroya F. White, brown, beige/brite: different adipose cells for different functions? Endocrinology. 2013;154(9):2992–3000. doi:10.1210/en.2013-1403
  • Chait A, den Hartigh LJ. Adipose tissue distribution, inflammation and its metabolic consequences, including diabetes and cardiovascular disease. Front Cardiovasc Med. 2020;7:22.
  • Lee MJ, Wu Y, Fried SK. Adipose tissue heterogeneity: implication of depot differences in adipose tissue for obesity complications. Mol Aspects Med. 2013;34(1):1–11. doi:10.1016/j.mam.2012.10.001
  • Klein S, Fontana L, Young VL, et al. Absence of an effect of liposuction on insulin action and risk factors for coronary heart disease. N Engl J Med. 2004;350(25):2549–2557. doi:10.1056/NEJMoa033179
  • Hocking SL, Stewart RL, Brandon AE, et al. Subcutaneous fat transplantation alleviates diet-induced glucose intolerance and inflammation in mice. Diabetologia. 2015;58(7):1587–1600. doi:10.1007/s00125-015-3583-y
  • Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009;360(15):1509–1517. doi:10.1056/NEJMoa0810780
  • Ravussin E, Galgani JE. The implication of brown adipose tissue for humans. Annu Rev Nutr. 2011;31(1):33–47. doi:10.1146/annurev-nutr-072610-145209
  • Sidossis L, Kajimura S. Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis. J Clin Invest. 2015;125(2):478–486. doi:10.1172/JCI78362
  • Sepa-Kishi DM, Ceddia RB. White and beige adipocytes: are they metabolically distinct? Horm Mol Biol Clin Investig. 2018;33(2). doi:10.1515/hmbci-2018-0003
  • Lee BC, Lee J. Cellular and molecular players in adipose tissue inflammation in the development of obesity-induced insulin resistance. Biochim Biophys Acta. 2014;1842(3):446–462. doi:10.1016/j.bbadis.2013.05.017
  • Oishi Y, Manabe I. Macrophages in inflammation, repair and regeneration. Int Immunol. 2018;30(11):511–528.
  • Aron-Wisnewsky J, Tordjman J, Poitou C, et al. Human adipose tissue macrophages: m1 and m2 cell surface markers in subcutaneous and omental depots and after weight loss. J Clin Endocrinol Metab. 2009;94(11):4619–4623. doi:10.1210/jc.2009-0925
  • Russo L, Lumeng CN. Properties and functions of adipose tissue macrophages in obesity. Immunology. 2018;155(4):407–417. doi:10.1111/imm.13002
  • Qiu Y, Nguyen KD, Odegaard JI, et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell. 2014;157(6):1292–1308. doi:10.1016/j.cell.2014.03.066
  • 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(10):3466–3479. doi:10.1172/JCI42845
  • Ferrante AW Jr. The immune cells in adipose tissue. Diabetes Obes Metab. 2013;15(Suppl 3):34–38. doi:10.1111/dom.12154
  • Cinti S, Mitchell G, Barbatelli G, et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res. 2005;46(11):2347–2355. doi:10.1194/jlr.M500294-JLR200
  • Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 2007;117(1):175–184. doi:10.1172/JCI29881
  • 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(12):1821–1830.
  • Grygiel-Gorniak B. Peroxisome proliferator-activated receptors and their ligands: nutritional and clinical implications–a review. Nutr J. 2014;13(1):17. doi:10.1186/1475-2891-13-17
  • Oestreich KJ, Weinmann AS. Master regulators or lineage-specifying? Changing views on CD4+ T cell transcription factors. Nat Rev Immunol. 2012;12(11):799–804. doi:10.1038/nri3321
  • Winer S, Chan Y, Paltser G, et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med. 2009;15(8):921–929. doi:10.1038/nm.2001
  • Winer DA, Winer S, Shen L, et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med. 2011;17(5):610–617. doi:10.1038/nm.2353
  • Ahmed M, Gaffen SL. IL-17 in obesity and adipogenesis. Cytokine Growth Factor Rev. 2010;21(6):449–453. doi:10.1016/j.cytogfr.2010.10.005
  • DeFuria J, Belkina AC, Jagannathan-Bogdan M, et al. B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proc Natl Acad Sci U S A. 2013;110(13):5133–5138. doi:10.1073/pnas.1215840110
  • Blaszczak AM, Bernier M, Wright VP, et al. Obesogenic memory maintains adipose tissue inflammation and insulin resistance. Immunometabolism. 2020;2(3).
  • Toubal A, Kiaf B, Beaudoin L, et al. Mucosal-associated invariant T cells promote inflammation and intestinal dysbiosis leading to metabolic dysfunction during obesity. Nat Commun. 2020;11(1):3755. doi:10.1038/s41467-020-17307-0
  • Khan S, Tsai S, Winer DA. Adipose tissue B cells come of age: the AABs of fat inflammation. Cell Metab. 2019;30(6):997–999. doi:10.1016/j.cmet.2019.11.007
  • Guzik TJ, Skiba DS, Touyz RM, Harrison DG. The role of infiltrating immune cells in dysfunctional adipose tissue. Cardiovasc Res. 2017;113(9):1009–1023.
  • Frasca D, Diaz A, Romero M, Thaller S, Blomberg BB. Secretion of autoimmune antibodies in the human subcutaneous adipose tissue. PLoS One. 2018;13(5):e0197472. doi:10.1371/journal.pone.0197472
  • Bolus WR, Kennedy AJ, Hasty AH. Obesity‐induced reduction of adipose eosinophils is reversed with low‐calorie dietary intervention. Physiol Rep. 2018;6(22):22. doi:10.14814/phy2.13919
  • Wu D, Molofsky AB, Liang HE, et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science. 2011;332(6026):243–247. doi:10.1126/science.1201475
  • Knights AJ, Vohralik EJ, Houweling PJ, et al. Eosinophil function in adipose tissue is regulated by Krüppel-like factor 3 (KLF3). Nat Commun. 2020;11(1):1–12. doi:10.1038/s41467-020-16758-9
  • Watanabe Y, Nagai Y, Honda H, et al. Bidirectional crosstalk between neutrophils and adipocytes promotes adipose tissue inflammation. FASEB J. 2019;33(11):11821–11835.
  • Tam TH, Chan KL, Boroumand P, et al. Nucleotides released from palmitate-activated murine macrophages attract neutrophils. J Biol Chem. 2020;295(15):4902–4911. doi:10.1074/jbc.RA119.010868
  • Bertola A, Ciucci T, Rousseau D, et al. Identification of adipose tissue dendritic cells correlated with obesity-associated insulin-resistance and inducing Th17 responses in mice and patients. Diabetes. 2012;61(9):2238–2247. doi:10.2337/db11-1274
  • Stefanovic-Racic M, Yang X, Turner MS, et al. Dendritic cells promote macrophage infiltration and comprise a substantial proportion of obesity-associated increases in CD11c+ cells in adipose tissue and liver. Diabetes. 2012;61(9):2330–2339.
  • Zhou Y, Yu X, Chen H, et al. Leptin deficiency shifts mast cells toward anti-inflammatory actions and protects mice from obesity and diabetes by polarizing M2 macrophages. Cell Metab. 2015;22(6):1045–1058. doi:10.1016/j.cmet.2015.09.013
  • Liu J, Divoux A, Sun J, et al. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med. 2009;15(8):940–945. doi:10.1038/nm.1994
  • Lehr S, Hartwig S, Sell H. Adipokines: a treasure trove for the discovery of biomarkers for metabolic disorders. Proteomics Clin Appl. 2012;6(1‐2):91–101.
  • Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JMJN. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994;372(6505):425–432. doi:10.1038/372425a0
  • Hube F, Lietz U, Igel M, et al. Difference in leptin mRNA levels between omental and subcutaneous abdominal adipose tissue from obese humans. Horm Metab Res. 1996;28(12):690–693. doi:10.1055/s-2007-979879
  • Considine RV, Sinha MK, Heiman ML, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334(5):292–295.
  • Leshan RL, Bjornholm M, Munzberg H, Myers MG Jr. Leptin receptor signaling and action in the central nervous system. Obesity (Silver Spring). 2006;14(Suppl 5):208s–212s. doi:10.1038/oby.2006.310
  • Pan W, Allison MB, Sabatini P, et al. Transcriptional and physiological roles for STAT proteins in leptin action. Mol Metab. 2019;22:121–131. doi:10.1016/j.molmet.2019.01.007
  • Minokoshi Y, Kim Y-B, Peroni OD, et al. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature. 2002;415(6869):339–343. doi:10.1038/415339a
  • Myers MG, Cowley MA, Münzberg H. Mechanisms of leptin action and leptin resistance. Annu Rev Physiol. 2008;70(1):537–556. doi:10.1146/annurev.physiol.70.113006.100707
  • Mai S, Walker GE, Vietti R, et al. Acute vitamin D(3) supplementation in severe obesity: evaluation of multimeric adiponectin. Nutrients. 2017;9(5):459. doi:10.3390/nu9050459
  • Lihn AS, Bruun JM, He G, Pedersen SB, Jensen PF, Richelsen BJM. Lower expression of adiponectin mRNA in visceral adipose tissue in lean and obese subjects. Mol Cell Endocrinol. 2004;219(1–2):9–15. doi:10.1016/j.mce.2004.03.002
  • Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF. A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem. 1995;270(45):26746–26749. doi:10.1074/jbc.270.45.26746
  • Leal VdO MD. Adipokines in obesity. Clin Chim Acta. 2013;419:87–94.
  • Liu W, Zhou X, Li Y, et al. Serum leptin, resistin, and adiponectin levels in obese and non-obese patients with newly diagnosed type 2 diabetes mellitus: a population-based study. Medicine. 2020;99(6):e19052. doi:10.1097/MD.0000000000019052
  • Tsiotra PC, Tsigos C, Anastasiou E, et al. Peripheral mononuclear cell resistin mRNA expression is increased in type 2 diabetic women. Mediators Inflamm. 2008;2008:892864. doi:10.1155/2008/892864
  • Nagaev I, Bokarewa M, Tarkowski A, Smith U. Human resistin is a systemic immune-derived proinflammatory cytokine targeting both leukocytes and adipocytes. PLoS One. 2006;1(1):e31. doi:10.1371/journal.pone.0000031
  • Yang R-Z, Lee M-J, Hu H, et al. Identification of omentin as a novel depot-specific adipokine in human adipose tissue: possible role in modulating insulin action. Am J Physiol Endocrinol Metab. 2006;290(6):E1253–E1261. doi:10.1152/ajpendo.00572.2004
  • Elsaid NH, Sadik NA, Ahmed NR, Fayez SE, Mohammed NAE-G. Serum omentin-1 levels in type 2 diabetic obese women in relation to glycemic control, insulin resistance and metabolic parameters. J Clin Transl Endocrinol. 2018;13:14–19. doi:10.1016/j.jcte.2018.05.003
  • Zhong X, Li X, Liu F, Tan H, Shang DJB. Omentin inhibits TNF-α-induced expression of adhesion molecules in endothelial cells via ERK/NF-κB pathway. Biochem Biophys Res Commun. 2012;425(2):401–406.
  • Chen Y, Liu F, Han F, Lv L, Tang CE, Luo F. Omentin-1 ameliorated free fatty acid-induced impairment in proliferation, migration, and inflammatory states of HUVECs. Cardiol Res Pract. 2020;2020:3054379. doi:10.1155/2020/3054379
  • Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 1993;259(5091):87–91. doi:10.1126/science.7678183
  • Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J Clin Invest. 1995;95(5):2409–2415. doi:10.1172/JCI117936
  • Guilherme A, Virbasius JV, Puri V, Czech MP. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol. 2008;9(5):367–377.
  • Stanley TL, Zanni MV, Johnsen S, et al. TNF-alpha antagonism with etanercept decreases glucose and increases the proportion of high molecular weight adiponectin in obese subjects with features of the metabolic syndrome. J Clin Endocrinol Metab. 2011;96(1):E146–150. doi:10.1210/jc.2010-1170
  • 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(12):1796–1808. doi:10.1172/JCI200319246
  • Maachi M, Pieroni L, Bruckert E, et al. Systemic low-grade inflammation is related to both circulating and adipose tissue TNF α, leptin and IL-6 levels in obese women. Int J Obes. 2004;28(8):993–997. doi:10.1038/sj.ijo.0802718
  • Galic S, Oakhill JS, Steinberg GR. Adipose tissue as an endocrine organ. Mol Cell Endocrinol. 2010;316(2):129–139. doi:10.1016/j.mce.2009.08.018
  • Timper K, Denson JL, Steculorum SM, et al. IL-6 improves energy and glucose homeostasis in obesity via enhanced central IL-6 trans-signaling. Cell Rep. 2017;19(2):267–280. doi:10.1016/j.celrep.2017.03.043
  • Ray I, Mahata SK, De RK. Obesity: an immunometabolic perspective. Front Endocrinol (Lausanne). 2016;7:157. doi:10.3389/fendo.2016.00157
  • Nishimoto S, Fukuda D, Higashikuni Y, et al. Obesity-induced DNA released from adipocytes stimulates chronic adipose tissue inflammation and insulin resistance. Sci Adv. 2016;2(3):e1501332.
  • Weisberg SP, Hunter D, Huber R, et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest. 2006;116(1):115–124. doi:10.1172/JCI24335
  • Wang X, Jiang X, Deng B, Xiao J, Jin J, Huang Z. Lipopolysaccharide and palmitic acid synergistically induced MCP-1 production via MAPK-meditated TLR4 signaling pathway in RAW264.7 cells. Lipids Health Dis. 2019;18(1):71. doi:10.1186/s12944-019-1017-4
  • Christiansen T, Richelsen B, Bruun JM. Monocyte chemoattractant protein-1 is produced in isolated adipocytes, associated with adiposity and reduced after weight loss in morbid obese subjects. Int J Obes. 2005;29(1):146–150. doi:10.1038/sj.ijo.0802839
  • Stagakis I, Bertsias G, Karvounaris S, et al. Anti-tumor necrosis factor therapy improves insulin resistance, beta cell function and insulin signaling in active rheumatoid arthritis patients with high insulin resistance. Arthritis Res Ther. 2012;14(3):R141.
  • van den Oever IAM, Baniaamam M, Simsek S, et al. The effect of anti-TNF treatment on body composition and insulin resistance in patients with rheumatoid arthritis. Rheumatol Int. 2020. doi:10.1007/s00296-020-04666-6
  • Sun X, Han F, Yi J, Han L, Wang B. Effect of aspirin on the expression of hepatocyte NF-kappaB and serum TNF-alpha in streptozotocin-induced type 2 diabetic rats. J Korean Med Sci. 2011;26(6):765–770. doi:10.3346/jkms.2011.26.6.765
  • Ferraz-Amaro I, Arce-Franco M, Muniz J, et al. Systemic blockade of TNF-alpha does not improve insulin resistance in humans. Horm Metab Res. 2011;43(11):801–808. doi:10.1055/s-0031-1287783
  • Leporini C, Russo E. Insulin-sensiting effects of tumor necrosis factor alpha inhibitors in rheumatoid arthritis: a systematic review and meta-analysis. Rev Recent Clin Trials. 2018;13(3):184–191. doi:10.2174/1574887113666180314100340
  • Ruscitti P, Masedu F, Alvaro S, et al. Anti-interleukin-1 treatment in patients with rheumatoid arthritis and type 2 diabetes (TRACK): a multicentre, open-label, randomised controlled trial. PLoS Med. 2019;16(9):e1002901. doi:10.1371/journal.pmed.1002901
  • Castaneda S, Remuzgo-Martinez S, Lopez-Mejias R, et al. Rapid beneficial effect of the IL-6 receptor blockade on insulin resistance and insulin sensitivity in non-diabetic patients with rheumatoid arthritis. Clin Exp Rheumatol. 2019;37(3):465–473.
  • Bako HY, Ibrahim MA, Isah MS, Ibrahim S. Inhibition of JAK-STAT and NF-kappaB signalling systems could be a novel therapeutic target against insulin resistance and type 2 diabetes. Life Sci. 2019;239:117045. doi:10.1016/j.lfs.2019.117045
  • Ge Z, Zhang P, Hong T, et al. Erythropoietin alleviates hepatic insulin resistance via PPARgamma-dependent AKT activation. Sci Rep. 2015;5(1):17878. doi:10.1038/srep17878
  • Zhang H, Ge Z, Tang S, Meng R, Bi Y, Zhu D. Erythropoietin ameliorates PA-induced insulin resistance through the IRS/AKT/FOXO1 and GSK-3beta signaling pathway, and inhibits the inflammatory response in HepG2 cells. Mol Med Rep. 2017;16(2):2295–2301. doi:10.3892/mmr.2017.6810
  • Wolfe BM, Kvach E, Eckel RH. Treatment of obesity: weight loss and bariatric surgery. Circ Res. 2016;118(11):1844–1855. doi:10.1161/CIRCRESAHA.116.307591
  • Panel NIoHCD. Gastrointestinal surgery for severe obesity. Ann Intern Med. 1991;115:956–961.
  • Hanipah ZN, Schauer PR. Bariatric surgery as a long-term treatment for type 2 diabetes/metabolic syndrome. Annu Rev Med. 2020;71:1–15.
  • Bray GA, Heisel WE, Afshin A, et al. The science of obesity management: an endocrine society scientific statement. Endocr Rev. 2018;39(2):79–132.
  • English WJ, DeMaria EJ, Hutter MM, et al. American society for metabolic and bariatric surgery 2018 estimate of metabolic and bariatric procedures performed in the United States. Surg Obes Relat Dis. 2020;16(4):457–463. doi:10.1016/j.soard.2019.12.022
  • Sjostrom L. Bariatric surgery and reduction in morbidity and mortality: experiences from the SOS study. Int J Obes. 2008;32(Suppl 7):S93–97. doi:10.1038/ijo.2008.244
  • Jouan Y, Blasco H, Bongrani A, Couet C, Dupont J, Maillot F. Preoperative chemerin level is predictive of inflammatory status 1 year after bariatric surgery. Obes Surg. 2020;30(10):3852–3861. doi:10.1007/s11695-020-04584-3
  • Faramia J, Ostinelli G, Drolet-Labelle V, Picard F, Tchernof A. Metabolic adaptations after bariatric surgery: adipokines, myokines and hepatokines. Curr Opin Pharmacol. 2020;52:67–74. doi:10.1016/j.coph.2020.06.005
  • Sala P, Torrinhas R, Fonseca DC, et al. Intestinal expression of toll-like receptor gene changes early after gastric bypass surgery and association with type 2 diabetes remission. Nutrition. 2020;79–80:110885. doi:10.1016/j.nut.2020.110885
  • Salman MA, Salman AA, Nafea MA, et al. Study of changes of obesity-related inflammatory cytokines after laparoscopic sleeve gastrectomy. ANZ J Surg. 2019;89(10):1265–1269. doi:10.1111/ans.15427
  • Min T, Prior SL, Dunseath G, Churm R, Barry JD, Stephens JW. Temporal effects of bariatric surgery on adipokines, inflammation and oxidative stress in subjects with impaired glucose homeostasis at 4 years of follow-up. Obes Surg. 2020;30(5):1712–1718. doi:10.1007/s11695-019-04377-3
  • Kerr AG, Andersson DP, Rydén M, Arner P, Dahlman I. Long-term changes in adipose tissue gene expression following bariatric surgery. J Intern Med. 2020;288(2):219–233. doi:10.1111/joim.13066
  • Lee Y-H, Hsiao H-F, Yang H-T, Huang S-Y, Chan WP. Reproducibility and repeatability of computer tomography-based measurement of abdominal subcutaneous and visceral adipose tissues. Sci Rep. 2017;7(1):40389. doi:10.1038/srep40389
  • Bjorndal B, Burri L, Staalesen V, Skorve J, Berge RK. Different adipose depots: their role in the development of metabolic syndrome and mitochondrial response to hypolipidemic agents. J Obes. 2011;2011:490650. doi:10.1155/2011/490650
  • Shen W, Wang Z, Punyanita M, et al. Adipose tissue quantification by imaging methods: a proposed classification. Obes Res. 2003;11(1):5–16. doi:10.1038/oby.2003.3
  • Cuevas-Ramos D, Almeda-Valdes P, Aguilar-Salinas CA, Cuevas-Ramos G, Cuevas-Sosa AA, Gomez-Perez FJ. The role of fibroblast growth factor 21 (FGF21) on energy balance, glucose and lipid metabolism. Curr Diabetes Rev. 2009;5(4):216–220. doi:10.2174/157339909789804396
  • Geng L, Lam KSL, Xu A. The therapeutic potential of FGF21 in metabolic diseases: from bench to clinic. Nat Rev Endocrinol. 2020. doi:10.1038/s41574-020-0386-0
  • Alessi MC, Peiretti F, Morange P, Henry M, Nalbone G, Juhan-Vague I. Production of plasminogen activator inhibitor 1 by human adipose tissue: possible link between visceral fat accumulation and vascular disease. Diabetes. 1997;46(5):860–867. doi:10.2337/diab.46.5.860
  • Hosaka S, Yamada T, Takahashi K, et al. Inhibition of plasminogen activator inhibitor-1 activation suppresses high fat diet-induced weight gain via alleviation of hypothalamic leptin resistance. Front Pharmacol. 2020;11:943. doi:10.3389/fphar.2020.00943
  • Zheng Z, Nakamura K, Gershbaum S, et al. Interacting hepatic PAI-1/tPA gene regulatory pathways influence impaired fibrinolysis severity in obesity. J Clin Invest. 2020;10–1172.
  • Liu M, Zhu H, Dai Y, et al. Zinc-α2-glycoprotein is associated with obesity in chinese people and HFD-induced obese mice. Front Physiol. 2018;9:62. doi:10.3389/fphys.2018.00062
  • Severo JS, Morais JBS, Beserra JB, et al. Role of zinc in zinc-α2-glycoprotein metabolism in obesity: a review of literature. Biol Trace Elem Res. 2020;193(1):81–88. doi:10.1007/s12011-019-01702-w
  • Rychter AM, Skrzypczak-Zielińska M, Zielińska A, et al. Is the retinol-binding protein 4 a possible risk factor for cardiovascular diseases in obesity? Int J Mol Sci. 2020;21(15):5229. doi:10.3390/ijms21155229
  • Kilicarslan M, de Weijer BA, Simonyté Sjödin K, et al. RBP4 increases lipolysis in human adipocytes and is associated with increased lipolysis and hepatic insulin resistance in obese women. FASEB J. 2020;34(5):6099–6110. doi:10.1096/fj.201901979RR
  • Kelly KR, Kashyap SR, O’Leary VB, Major J, Schauer PR, Kirwan JP. Retinol-binding protein 4 (RBP4) protein expression is increased in omental adipose tissue of severely obese patients. Obesity (Silver Spring). 2010;18(4):663–666. doi:10.1038/oby.2009.328
  • Bozaoglu K, Bolton K, McMillan J, et al. Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology. 2007;148(10):4687–4694. doi:10.1210/en.2007-0175
  • Karczewska-Kupczewska M, Nikołajuk A, Stefanowicz M, Matulewicz N, Kowalska I, Strączkowski M. Serum and adipose tissue chemerin is differentially related to insulin sensitivity. Endocr Connect. 2020;9(5):360–369. doi:10.1530/EC-20-0084
  • Heo YJ, Choi SE, Jeon JY, et al. Visfatin induces inflammation and insulin resistance via the NF-κB and STAT3 signaling pathways in hepatocytes. J Diabetes Res. 2019;2019:4021623.
  • Nourbakhsh M, Nourbakhsh M, Gholinejad Z, Razzaghy-Azar M. Visfatin in obese children and adolescents and its association with insulin resistance and metabolic syndrome. Scand J Clin Lab Invest. 2015;75(2):183–188. doi:10.3109/00365513.2014.1003594