Journal of Hepatology
Volume 51, Issue 4 , Pages 765-777 , October 2009

Effects of weight loss induced by bariatric surgery on hepatic adipocytokine expression

  • Alexander R. Moschen

      Affiliations

    • Christian Doppler Research Laboratory for Gut Inflammation, Innsbruck Medical University, Anichstrasse 35, 6020 Innsbruck, Austria
    • Internal Medicine II (Gastroenterology and Hepatology), Innsbruck Medical University, Innsbruck, Austria
    • These authors contributed equally to this work.
  • ,
  • Clemens Molnar

      Affiliations

    • Internal Medicine I (Metabolic Diseases, Pulmology, Infectious Diseases, Endocrinology, Rheumatology and Angiology), Innsbruck Medical University, Innsbruck, Austria
    • These authors contributed equally to this work.
  • ,
  • Anna Maria Wolf

      Affiliations

    • Internal Medicine V (Hematology and Oncology), Innsbruck Medical University, Innsbruck, Austria
  • ,
  • Helmut Weiss

      Affiliations

    • Department of General and Transplant Surgery, Innsbruck Medical University, Innsbruck, Austria
  • ,
  • Ivo Graziadei

      Affiliations

    • Internal Medicine II (Gastroenterology and Hepatology), Innsbruck Medical University, Innsbruck, Austria
  • ,
  • Susanne Kaser

      Affiliations

    • Internal Medicine I (Metabolic Diseases, Pulmology, Infectious Diseases, Endocrinology, Rheumatology and Angiology), Innsbruck Medical University, Innsbruck, Austria
  • ,
  • Christoph F. Ebenbichler

      Affiliations

    • Internal Medicine I (Metabolic Diseases, Pulmology, Infectious Diseases, Endocrinology, Rheumatology and Angiology), Innsbruck Medical University, Innsbruck, Austria
  • ,
  • Sylvia Stadlmann

      Affiliations

    • Institute of Pathology, Kantonsspital Baden, Baden, Switzerland
  • ,
  • Patrizia L. Moser

      Affiliations

    • Institute of Pathology, Innsbruck Medical University, Innsbruck, Austria
  • ,
  • Herbert Tilg

      Affiliations

    • Christian Doppler Research Laboratory for Gut Inflammation, Innsbruck Medical University, Anichstrasse 35, 6020 Innsbruck, Austria
    • Internal Medicine II (Gastroenterology and Hepatology), Innsbruck Medical University, Innsbruck, Austria
    • Corresponding Author InformationCorresponding author. Tel.: +43 512 5040; fax: +43 512 5046723374.

Received 3 January 2009 ,Revised 20 May 2009 ,Accepted 2 June 2009.

References 

  1. Tilg H, Kaser A. Treatment strategies in nonalcoholic fatty liver disease. Nat Clin Pract Gastroenterol Hepatol. 2005;2:148–155
  2. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004;40:1387–1395
  3. Marchesini G, Forlani G. NASH: from liver diseases to metabolic disorders and back to clinical hepatology. Hepatology. 2002;35:497–499
  4. Tilg H, Hotamisligil GS. Nonalcoholic fatty liver disease: cytokine–adipokine interplay and regulation of insulin resistance. Gastroenterology. 2006;131:934–945
  5. Petersen KF, Dufour S, Befroy D, Lehrke M, Hendler RE, Shulman GI. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes. 2005;54:603–608
  6. Dixon JB, Bhathal PS, Hughes NR, O’Brien PE. Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss. Hepatology. 2004;39:1647–1654
  7. Kral JG, Thung SN, Biron S, Hould FS, Lebel S, Marceau S, et al. Effects of surgical treatment of the metabolic syndrome on liver fibrosis and cirrhosis. Surgery. 2004;135:48–58
  8. Silverman EM, Sapala JA, Appelman HD. Regression of hepatic steatosis in morbidly obese persons after gastric bypass. Am J Clin Pathol. 1995;104:23–31
  9. Luyckx FH, Desaive C, Thiry A, Dewe W, Scheen AJ, Gielen JE, et al. Liver abnormalities in severely obese subjects: effect of drastic weight loss after gastroplasty. Int J Obes Relat Metab Disord. 1998;22:222–226
  10. Chapman AE, Kiroff G, Game P, Foster B, O’Brien P, Ham J, et al. Laparoscopic adjustable gastric banding in the treatment of obesity: a systematic literature review. Surgery. 2004;135:326–351
  11. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol. 2006;6:772–783
  12. Xu A, Wang Y, Keshaw H, Xu LY, Lam KS, Cooper GJ. The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in mice. J Clin Invest. 2003;112:91–100
  13. Combs TP, Berg AH, Obici S, Scherer PE, Rossetti L. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J Clin Invest. 2001;108:1875–1881
  14. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature. 2003;423:762–769
  15. Maeda N, Shimomura I, Kishida K, Nishizawa H, Matsuda M, Nagaretani H, et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat Med. 2002;8:731–737
  16. Wolf AM, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun. 2004;323:630–635
  17. Heymsfield SB, Greenberg AS, Fujioka K, Dixon RM, Kushner R, Hunt T, et al. Recombinant leptin for weight loss in obese and lean adults: a randomized, controlled, dose-escalation trial. JAMA. 1999;282:1568–1575
  18. Matarese G, Moschos S, Mantzoros CS. Leptin in immunology. J Immunol. 2005;174:3137–3142
  19. Tilg H, Moschen AR. Role of adiponectin and PBEF/visfatin as regulators of inflammation: involvement in obesity-associated diseases. Clin Sci (Lond). 2008;114:275–288
  20. Kusminski CM, McTernan PG, Kumar S. Role of resistin in obesity, insulin resistance and type II diabetes. Clin Sci (Lond). 2005;109:243–256
  21. Fukuhara A, Matsuda M, Nishizawa M, Segawa K, Tanaka M, Kishimoto K, et al. Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science. 2005;307:426–430
  22. Moschen AR, Kaser A, Enrich B, Mosheimer B, Theurl M, Niederegger H, et al. Visfatin, an adipocytokine with pro-inflammatory and immunomodulating properties. J Immunol. 2007;178:1748–1758
  23. Jia SH, Li Y, Parodo J, Kapus A, Fan L, Rotstein OD, et al. Pre-B cell colony-enhancing factor inhibits neutrophil apoptosis in experimental inflammation and clinical sepsis. J Clin Invest. 2004;113:1318–1327
  24. Ye SQ, Simon BA, Maloney JP, Zambelli-Weiner A, Gao L, Grant A, et al. Pre-B-cell colony-enhancing factor as a potential novel biomarker in acute lung injury. Am J Respir Crit Care Med. 2005;171:361–370
  25. Otero M, Lago R, Gomez R, Lago F, Dieguez C, Gomez-Reino JJ, et al. Changes in plasma levels of fat-derived hormones adiponectin, leptin, resistin and visfatin in patients with rheumatoid arthritis. Ann Rheum Dis. 2006;65:1198–1201
  26. Weiss HG, Nehoda H, Labeck B, Peer-Kuehberger R, Oberwalder M, Aigner F, et al. Adjustable gastric and esophagogastric banding: a randomized clinical trial. Obes Surg. 2002;12:573–578
  27. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–419
  28. Ratziu V, Giral P, Jacqueminet S, Charlotte F, Hartemann-Heurtier A, Serfaty L, et al. Rosiglitazone for nonalcoholic steatohepatitis: one-year results of the randomized placebo-controlled fatty liver improvement with rosiglitazone therapy (FLIRT) trial. Gastroenterology. 2008;135:100–110
  29. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41:1313–1321
  30. Brunt EM, Janney CG, Di Bisceglie AM, Neuschwander-Tetri BA, Bacon BR. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol. 1999;94:2467–2474
  31. Kaser S, Moschen A, Cayon A, Kaser A, Crespo J, Pons-Romero F, et al. Adiponectin and its receptors in non-alcoholic steatohepatitis. Gut. 2005;54:117–121
  32. Bertolani C, Sancho-Bru P, Failli P, Bataller R, Aleffi S, DeFranco R, et al. Resistin as an intrahepatic cytokine: overexpression during chronic injury and induction of proinflammatory actions in hepatic stellate cells. Am J Pathol. 2006;169:2042–2053
  33. Supplement 1. American Diabetes Association: clinical practice recommendations 2000. Diabetes Care 2000;23(Suppl 1):S1–116.
  34. Jonsson JR, Moschen AR, Hickman IJ, Richardson MM, Kaser S, Clouston AD, et al. Adiponectin and its receptors in patients with chronic hepatitis C. J Hepatol. 2005;43:929–936
  35. Tilg H, Moschen AR. Insulin resistance, inflammation, and non-alcoholic fatty liver disease. Trends Endocrinol Metab. 2008;19:371–379
  36. Chitturi S, Farrell G, Frost L, Kriketos A, Lin R, Fung C, et al. Serum leptin in NASH correlates with hepatic steatosis but not fibrosis: a manifestation of lipotoxicity?. Hepatology. 2002;36:403–409
  37. Nakao K, Nakata K, Ohtsubo N, Maeda M, Moriuchi T, Ichikawa T, et al. Association between nonalcoholic fatty liver, markers of obesity, and serum leptin level in young adults. Am J Gastroenterol. 2002;97:1796–1801
  38. Zhou J, Lei W, Shen L, Luo HS, Shen ZX. Primary study of leptin and human hepatocellular carcinoma in vitro. World J Gastroenterol. 2008;14:2900–2904
  39. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun. 1999;257:79–83
  40. Hui JM, Hodge A, Farrell GC, Kench JG, Kriketos A, George J. Beyond insulin resistance in NASH: TNF-alpha or adiponectin?. Hepatology. 2004;40:46–54
  41. Kamada Y, Tamura S, Kiso S, Matsumoto H, Saji Y, Yoshida Y, et al. Enhanced carbon tetrachloride-induced liver fibrosis in mice lacking adiponectin. Gastroenterology. 2003;125:1796–1807
  42. Masaki T, Chiba S, Tatsukawa H, Yasuda T, Noguchi H, Seike M, et al. Adiponectin protects LPS-induced liver injury through modulation of TNF-alpha in KK-Ay obese mice. Hepatology. 2004;40:177–184
  43. Sennello JA, Fayad R, Morris AM, Eckel RH, Asilmaz E, Montez J, et al. Regulation of T cell-mediated hepatic inflammation by adiponectin and leptin. Endocrinology. 2005;146:2157–2164
  44. Ballantyne GH, Gumbs A, Modlin IM. Changes in insulin resistance following bariatric surgery and the adipoinsular axis: role of the adipocytokines, leptin, adiponectin and resistin. Obes Surg. 2005;15:692–699
  45. Baratta R, Amato S, Degano C, Farina MG, Patane G, Vigneri R, et al. Adiponectin relationship with lipid metabolism is independent of body fat mass: evidence from both cross-sectional and intervention studies. J Clin Endocrinol Metab. 2004;89:2665–2671
  46. Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, Boone T, et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science. 1995;269:540–543
  47. Oral EA, Simha V, Ruiz E, Andewelt A, Premkumar A, Snell P, et al. Leptin-replacement therapy for lipodystrophy. N Engl J Med. 2002;346:570–578
  48. Giannini E, Botta F, Cataldi A, Tenconi GL, Ceppa P, Barreca T, et al. Leptin levels in nonalcoholic steatohepatitis and chronic hepatitis C. Hepatogastroenterology. 1999;46:2422–2425
  49. Manco M, Marcellini M, Giannone G, Nobili V. Correlation of serum TNF-alpha levels and histologic liver injury scores in pediatric nonalcoholic fatty liver disease. Am J Clin Pathol. 2007;127:954–960
  50. Wong VW, Hui AY, Tsang SW, Chan JL, Tse AM, Chan KF, et al. Metabolic and adipokine profile of Chinese patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2006;4:1154–1161
  51. Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature. 1998;394:897–901
  52. Matarese G, Di Giacomo A, Sanna V, Lord GM, Howard JK, Di Tuoro A, et al. Requirement for leptin in the induction and progression of autoimmune encephalomyelitis. J Immunol. 2001;166:5909–5916
  53. Ikejima K, Takei Y, Honda H, Hirose M, Yoshikawa M, Zhang YJ, et al. Leptin receptor-mediated signaling regulates hepatic fibrogenesis and remodeling of extracellular matrix in the rat. Gastroenterology. 2002;122:1399–1410
  54. Leclercq IA, Farrell GC, Schriemer R, Robertson GR. Leptin is essential for the hepatic fibrogenic response to chronic liver injury. J Hepatol. 2002;37:206–213
  55. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, et al. The hormone resistin links obesity to diabetes. Nature. 2001;409:307–312
  56. Pagano C, Soardo G, Pilon C, Milocco C, Basan L, Milan G, et al. Increased serum resistin in nonalcoholic fatty liver disease is related to liver disease severity and not to insulin resistance. J Clin Endocrinol Metab. 2006;91:1081–1086
  57. Zou CC, Liang L, Hong F, Fu JF, Zhao ZY. Serum adiponectin, resistin levels and non-alcoholic fatty liver disease in obese children. Endocr J. 2005;52:519–524
  58. Younossi ZM, Jarrar M, Nugent C, Randhawa M, Afendy M, Stepanova M, et al. A novel diagnostic biomarker panel for obesity-related nonalcoholic steatohepatitis (NASH). Obes Surg. 2008;18:1430–1437
  59. Qatanani M, Szwergold NR, Greaves DR, Ahima RS, Lazar MA. Macrophage-derived human resistin exacerbates adipose tissue inflammation and insulin resistance in mice. J Clin Invest 2009; pii: 37273. doi:10.1172/JCI37273. [Epub ahead of print].
  60. Harrison SA, Fecht W, Brunt EM, Neuschwander-Tetri BA. Orlistat for overweight subjects with nonalcoholic steatohepatitis: a randomized, prospective trial. Hepatology. 2009;49:80–86
  61. Verma S, Li SH, Wang CH, Fedak PW, Li RK, Weisel RD, et al. Resistin promotes endothelial cell activation: further evidence of adipokine–endothelial interaction. Circulation. 2003;108:736–740
  62. Silswal N, Singh AK, Aruna B, Mukhopadhyay S, Ghosh S, Ehtesham NZ. Human resistin stimulates the pro-inflammatory cytokines TNF-alpha and IL-12 in macrophages by NF-kappaB-dependent pathway. Biochem Biophys Res Commun. 2005;334:1092–1101
  63. Samal B, Sun Y, Stearns G, Xie C, Suggs S, McNiece I. Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor. Mol Cell Biol. 1994;14:1431–1437
  64. Rongvaux A, Shea RJ, Mulks MH, Gigot D, Urbain J, Leo O, et al. Pre-B-cell colony-enhancing factor, whose expression is up-regulated in activated lymphocytes, is a nicotinamide phosphoribosyltransferase, a cytosolic enzyme involved in NAD biosynthesis. Eur J Immunol. 2002;32:3225–3234
  65. Wang T, Zhang X, Bheda P, Revollo JR, Imai S, Wolberger C. Structure of Nampt/PBEF/visfatin, a mammalian NAD+ biosynthetic enzyme. Nat Struct Mol Biol. 2006;13:661–662
  66. Kitani T, Okuno S, Fujisawa H. Growth phase-dependent changes in the subcellular localization of pre-B-cell colony-enhancing factor. FEBS Lett. 2003;544:74–78
  67. Koczan D, Guthke R, Thiesen HJ, Ibrahim SM, Kundt G, Krentz H, et al. Gene expression profiling of peripheral blood mononuclear leukocytes from psoriasis patients identifies new immune regulatory molecules. Eur J Dermatol. 2005;15:251–257
  68. Manco M, Fernandez-Real JM, Equitani F, Vendrell J, Valera Mora ME, Nanni G, et al. Effect of massive weight loss on inflammatory adipocytokines and the innate immune system in morbidly obese women. J Clin Endocrinol Metab. 2007;92:483–490

 The authors who have taken part in this study declared that they do not have anything to disclose regarding funding or conflict of interest with respect to this manuscript.

PII: S0168-8278(09)00443-7

doi: 10.1016/j.jhep.2009.06.016

Journal of Hepatology
Volume 51, Issue 4 , Pages 765-777 , October 2009