Gastroenterology
Volume 132, Issue 2 , Pages 601-614 , February 2007

Adiponectin Deficiency Protects Mice From Chemically Induced Colonic Inflammation

  • Raja Fayad

      Affiliations

    • Department of Human Nutrition, University of Illinois at Chicago, Chicago, Illinois
    • ,
  • Maria Pini

      Affiliations

    • Department of Human Nutrition, University of Illinois at Chicago, Chicago, Illinois
    • ,
  • Joseph A. Sennello

      Affiliations

    • Department of Human Nutrition, University of Illinois at Chicago, Chicago, Illinois
    • ,
  • Robert J. Cabay

      Affiliations

    • Department of Pathology, University of Illinois at Chicago, Chicago, Illinois
    • ,
  • Lawrence Chan

      Affiliations

    • Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas
    • ,
  • Aimin Xu

      Affiliations

    • Department of Medicine and Research Center for Heart, Brain, Hormone, and Healthy Aging, University of Hong Kong, Hong Kong, China
    • ,
  • Giamila Fantuzzi

      Affiliations

    • Department of Human Nutrition, University of Illinois at Chicago, Chicago, Illinois
    • Corresponding Author InformationAddress requests for reprints to: Giamila Fantuzzi, PhD, University of Illinois at Chicago, 1919 W. Taylor Street MC 517, Chicago, Illinois 60612. fax: (312) 413-0319.

Received 15 July 2006 ,Accepted 19 October 2006.

References 

  1. Kim JY, Scherer PE. Adiponectin, an adipocyte-derived hepatic insulin sensitizer regulation during development. Pediatr Endocrinol Rev. 2004;1(Suppl 3):428–431
  2. Waki H, Yamauchi T, Kamon J, Ito Y, Uchida S, Kita S, et al. Impaired multimerization of human adiponectin mutants associated with diabetes (Molecular structure and multimer formation of adiponectin). J Biol Chem. 2003;278:40352–40363
  3. Waki H, Yamauchi T, Kamon J, Kita S, Ito Y, Hada Y, et al. Generation of globular fragment of adiponectin by leukocyte elastase secreted by monocytic cell line THP-1. Endocrinology. 2005;146:790–796
  4. Kadowaki T, Yamauchi T. Adiponectin and adiponectin receptors. Endocr Rev. 2005;26:439–451
  5. Wang Y, Lam KS, Xu JY, Lu G, Xu LY, Cooper GJ, et al. Adiponectin inhibits cell proliferation by interacting with several growth factors in an oligomerization-dependent manner. J Biol Chem. 2005;280:18341–18347
  6. Hug C, Wang J, Ahmad NS, Bogan JS, Tsao TS, Lodish HF. T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc Natl Acad Sci U S A. 2004;101:10308–10313
  7. Shimada K, Miyazaki T, Daida H. Adiponectin and atherosclerotic disease. Clin Chim Acta. 2004;344:1–12
  8. Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol. 2005;115:911–920
  9. Ehling A, Schaffler A, Herfarth H, Tarner IH, Anders S, Distler O, et al. The potential of adiponectin in driving arthritis. J Immunol. 2006;176:4468–4478
  10. Ogunwobi OO, Beales IL. Adiponectin stimulates proliferation and cytokine secretion in colonic epithelial cells. Regul Pept. 2006;134:105–113
  11. Yamamoto K, Kiyohara T, Murayama Y, Kihara S, Okamoto Y, Funahashi T, et al. Production of adiponectin, an anti-inflammatory protein, in mesenteric adipose tissue in Crohn’s disease. Gut. 2005;54:789–796
  12. Karmiris K, Koutroubakis IE, Xidakis C, Polychronaki M, Voudouri T, Kouroumalis EA. Circulating levels of leptin, adiponectin, resistin, and ghrelin in inflammatory bowel disease. Inflamm Bowel Dis. 2006;12:100–105
  13. Nishihara T, Matsuda M, Araki H, Oshima K, Kihara S, Funahashi T, et al. Effect of adiponectin on murine colitis induced by dextran sulfate sodium. Gastroenterology. 2006;131:853–861
  14. Ma K, Cabrero A, Saha PK, Kojima H, Li L, Chang BH, et al. Increased β oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J Biol Chem. 2002;277:34658–34661
  15. 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
  16. Siegmund B, Rieder F, Albrich S, Wolf K, Bidlingmaier C, Firestein GS, et al. Adenosine kinase inhibitor GP515 improves experimental colitis in mice. J Pharmacol Exp Ther. 2001;296:99–105
  17. Atreya R, Mudter J, Finotto S, Mullberg J, Jostock T, Wirtz S, et al. Blockade of interleukin 6 transsignaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn’s disease and experimental colitis in vivo. Nat Med. 2000;6:583–588
  18. Siegmund B, Sennello JA, Jones-Carson J, Gamboni-Robertson F, Lehr HA, Batra A, et al. Leptin receptor expression on T lymphocytes modulates chronic intestinal inflammation in mice. Gut. 2004;53:965–972
  19. Chen B, Lam KS, Wang Y, Wu D, Lam MC, Shen J, et al. Hypoxia dysregulates the production of adiponectin and plasminogen activator inhibitor-1 independent of reactive oxygen species in adipocytes. Biochem Biophys Res Commun. 2006;341:549–556
  20. Johns TG, Luwor RB, Murone C, Walker F, Weinstock J, Vitali AA, et al. Antitumor efficacy of cytotoxic drugs and the monoclonal antibody 806 is enhanced by the EGF receptor inhibitor AG1478. Proc Natl Acad Sci U S A. 2003;100:15871–15876
  21. Morris AM, Sennello JA, Fayad R, Eckel RH, Dinarello CA, Fantuzzi G. T-cell-mediated hepatic inflammation modulates adiponectin levels in mice: role of tumor necrosis factor α. Metabolism. 2006;55:555–559
  22. Dignass AU, Tsunekawa S, Podolsky DK. Fibroblast growth factors modulate intestinal epithelial cell growth and migration. Gastroenterology. 1994;106:1254–1262
  23. Jeffers M, McDonald WF, Chillakuru RA, Yang M, Nakase H, Deegler LL, et al. A novel human fibroblast growth factor treats experimental intestinal inflammation. Gastroenterology. 2002;123:1151–1162
  24. Matsuda M, Shimomura I, Sata M, Arita Y, Nishida M, Maeda N, et al. Role of adiponectin in preventing vascular stenosis (The missing link of adipo-vascular axis). J Biol Chem. 2002;277:37487–37491
  25. El-Assal ON, Besner GE. HB-EGF enhances restitution after intestinal ischemia/reperfusion via PI3K/Akt and MEK/ERK1/2 activation. Gastroenterology. 2005;129:609–625
  26. Xia G, Rachfal AW, Martin AE, Besner GE. Up-regulation of endogenous heparin-binding EGF-like growth factor (HB-EGF) expression after intestinal ischemia/reperfusion injury. J Invest Surg. 2003;16:57–63
  27. Pillai SB, Hinman CE, Luquette MH, Nowicki PT, Besner GE. Heparin-binding epidermal growth factor-like growth factor protects rat intestine from ischemia/reperfusion injury. J Surg Res. 1999;87:225–231
  28. Xia G, Martin AE, Besner GE. Heparin-binding EGF-like growth factor down-regulates expression of adhesion molecules and infiltration of inflammatory cells after intestinal ischemia/reperfusion injury. J Pediatr Surg. 2003;38:434–439
  29. McCole DF, Rogler G, Varki N, Barrett KE. Epidermal growth factor partially restores colonic ion transport responses in mouse models of chronic colitis. Gastroenterology. 2005;129:591–608
  30. Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med. 2001;7:941–946
  31. 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
  32. Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE, et al. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab. 2001;86:1930–1935
  33. Okamoto Y, Kihara S, Ouchi N, Nishida M, Arita Y, Kumada M, et al. Adiponectin reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2002;106:2767–2770
  34. Yamauchi T, Kamon J, Waki H, Imai Y, Shimozawa N, Hioki K, et al. Globular adiponectin protected ob/ob mice from diabetes and ApoE-deficient mice from atherosclerosis. J Biol Chem. 2003;278:2461–2468
  35. Ouchi N, Kihara S, Arita Y, Nishida M, Matsuyama A, Okamoto Y, et al. Adipocyte-derived plasma protein, adiponectin, suppresses lipid accumulation and class A scavenger receptor expression in human monocyte-derived macrophages. Circulation. 2001;103:1057–1063
  36. Arita Y, Kihara S, Ouchi N, Maeda K, Kuriyama H, Okamoto Y, et al. Adipocyte-derived plasma protein adiponectin acts as a platelet-derived growth factor-BB-binding protein and regulates growth factor-induced common postreceptor signal in vascular smooth muscle cell. Circulation. 2002;105:2893–2898
  37. 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
  38. 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
  39. Peake PW, Shen Y, Campbell LV, Charlesworth JA. Human adiponectin binds to bacterial lipopolysaccharide. Biochem Biophys Res Commun. 2006;341:108–115
  40. Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006;131:117–129
  41. Kougias P, Chai H, Lin PH, Yao Q, Lumsden AB, Chen C. Effects of adipocyte-derived cytokines on endothelial functions: implication of vascular disease. J Surg Res. 2005;126:121–129
  42. 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
  43. Matsumoto H, Tamura S, Kamada Y, Kiso S, Fukushima J, Wada A, et al. Adiponectin deficiency exacerbates lipopolysaccharide/D-galactosamine-induced liver injury in mice. World J Gastroenterol. 2006;12:3352–3358
  44. Pini M, Sennello JA, Chan L, Fantuzzi G. Adiponectin deficiency does not affect the inflammatory response to endotoxin or Concanavalin A in mice. Endocrinology. 2006;147:5019–5022
  45. Vandenbroucke K, Hans W, Van Huysse J, Neirynck S, Demetter P, Remaut E, et al. Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice. Gastroenterology. 2004;127:502–513
  46. Xia G, Martin AE, Michalsky MP, Besner GE. Heparin-binding EGF-like growth factor preserves crypt cell proliferation and decreases bacterial translocation after intestinal ischemia/reperfusion injury. J Pediatr Surg. 2002;37:1081–1087
  47. Mehta VB, Besner GE. Inhibition of NF-κB activation and its target genes by heparin-binding epidermal growth factor-like growth factor. J Immunol. 2003;171:6014–6022
  48. Bohn E, Bechtold O, Zahir N, Frick JS, Reimann J, Jilge B, et al. Host gene expression in the colon of gnotobiotic interleukin-2 deficient mice colonized with commensal colitogenic or noncolitogenic bacterial strains: common patterns and bacteria strain specific signatures. Inflamm Bowel Dis. 2006;12:853–862
  49. Neumeier M, Hellerbrand C, Gabele E, Buettner R, Bollheimer C, Weigert J, et al. Adiponectin and its receptors in rodent models of fatty liver disease and liver cirrhosis. World J Gastroenterol. 2006;12:5490–5494
  50. Okamoto Y, Arita Y, Nishida M, Muraguchi M, Ouchi N, Takahashi M, et al. An adipocyte-derived plasma protein, adiponectin, adheres to injured vascular walls. Horm Metab Res. 2000;32:47–50
  51. Cooper HS, Murthy SN, Shah RS, Sedergran DJ. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest. 1993;69:238–249

 Supported by NIH grants DK061483 (to G.F.) and DK68037 and HL51586 (to L.C.), by a Hong Kong Research Council grant HKU 7486/04M (to A.X.), and by a CCFA career development award (to R.F.).

PII: S0016-5085(06)02481-4

doi: 10.1053/j.gastro.2006.11.026

Gastroenterology
Volume 132, Issue 2 , Pages 601-614 , February 2007

Article Tools

* Image Usage & Resolution