Adiponectin-stimulated CXCL8 release in primary human hepatocytes is regulated by ERK1/ERK2, p38 MAPK, NF-κB, and STAT3 signaling pathways

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 297, Issue 3, 2009, Pages

  Wanninger, Josef ^a   Neumeier, Markus ^a   Weigert, Johanna ^a   Bauer, Sabrina ^a   Weiss, Thomas S ^a   Schäffler, Andreas ^a   Krempl, Corinna ^a   Bleyl, Cornelia ^a   Aslanidis, Charalampos ^a   Schölmerich, Jürgen ^a   Buechler, Christa ^a  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

Adiponectin; Adiponectin receptor 1; Extracellular signal regulated kinase; Hepatocyte; Mitogen activated protein kinase; Nuclear factor B; STAT3

Indexed keywords

ADIPONECTIN; ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; LEPTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; SMALL INTERFERING RNA; STAT3 PROTEIN;

ARTICLE; CANCER CELL CULTURE; CARCINOMA CELL; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL; LIVER CELL CARCINOMA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

ADIPONECTIN; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; HEPATOCYTES; HUMANS; INTERLEUKIN-8; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; RECEPTORS, ADIPONECTIN; RECOMBINANT PROTEINS; RNA INTERFERENCE; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TIME FACTORS; UP-REGULATION;

EID: 69749095451     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90644.2008     Document Type: Article

References (48)

1. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 257: 79-83, 1999. (Pubitemid 29299050)
2. Bullen JW Jr, Bluher S, Kelesidis T, Mantzoros CS. Regulation of adiponectin and its receptors in response to development of diet-induced obesity in mice. Am J Physiol Endocrinol Metab 292: E1079-E1086, 2007. (Pubitemid 46536507)
3. de la Iglesia N, Konopka G, Lim KL, Nutt CL, Bromberg JF, Frank DA, Mischel PS, Louis DN, Bonni A. Deregulation of a STAT3- interleukin 8 signaling pathway promotes human glioblastoma cell proliferation and invasiveness. J Neurosci 28: 5870-5878, 2008.
4. Fantuzzi G. Adiponectin and inflammation: consensus and controversy. J Allergy Clin Immunol 121: 326-330, 2008.
5. Fielding CA, McLoughlin RM, McLeod L, Colmont CS, Najdovska M, Grail D, Ernst M, Jones SA, Topley N, Jenkins BJ. IL-6 regulates neutrophil trafficking during acute inflammation via STAT3. J Immunol 181: 2189-2195, 2008.
6. Gharavi NM, Alva JA, Mouillesseaux KP, Lai C, Yeh M, Yeung W, Johnson J, Szeto WL, Hong L, Fishbein M, Wei L, Pfeffer LM, Berliner JA. Role of the Jak/STAT pathway in the regulation of interleukin- 8 transcription by oxidized phospholipids in vitro and in atherosclerosis in vivo. J Biol Chem 282: 31460-31468, 2007. (Pubitemid 350044874)
7. Gregory SH, Wing EJ, Danowski KL, van Rooijen N, Dyer KF, Tweardy DJ. IL-6 produced by Kupffer cells induces STAT protein activation in hepatocytes early during the course of systemic listerial infections. J Immunol 160: 6056-6061, 1998.
8. Hanson JC, Bostick MK, Campe CB, Kodali P, Lee G, Yan J, Maher JJ. Transgenic overexpression of interleukin-8 in mouse liver protects against galactosamine/endotoxin toxicity. J Hepatol 44: 359-367, 2006. (Pubitemid 43069218)
9. Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M. Multiple control of interleukin-8 gene expression. J Leukoc Biol 72: 847-855, 2002. (Pubitemid 35365158)
10. Jarrar MH, Baranova A, Collantes R, Ranard B, Stepanova M, Bennett C, Fang Y, Elariny H, Goodman Z, Chandhoke V, Younossi ZM. Adipokines and cytokines in non-alcoholic fatty liver disease. Aliment Pharmacol Ther 27: 412-421, 2008.
11. Jeschke MG, Klein D, Thasler WE, Bolder U, Schlitt HJ, Jauch KW, Weiss TS. Insulin decreases inflammatory signal transcription factor expression in primary human liver cells after LPS challenge. Mol Med 14: 11-19, 2008. (Pubitemid 351356881)
12. Joshi-Barve S, Barve SS, Amancherla K, Gobejishvili L, Hill D, Cave M, Hote P, McClain CJ. Palmitic acid induces production of proinflammatory cytokine interleukin-8 from hepatocytes. Hepatology 46: 823-830, 2007. (Pubitemid 47436129)
13. Kitahara K, Kusunoki N, Kakiuchi T, Suguro T, Kawai S. Adiponectin stimulates IL-8 production by rheumatoid synovial fibroblasts. Biochem Biophys Res Commun 378: 218-223, 2009.
14. Klein C, Wustefeld T, Assmus U, Roskams T, Rose-John S, Muller M, Manns MP, Ernst M, Trautwein C. The IL-6-gp130-STAT3 pathway in hepatocytes triggers liver protection in T cell-mediated liver injury. J Clin Invest 115: 860-869, 2005. (Pubitemid 40489390)
15. Kobashi C, Urakaze M, Kishida M, Kibayashi E, Kobayashi H, Kihara S, Funahashi T, Takata M, Temaru R, Sato A, Yamazaki K, Nakamura N, Kobayashi M. Adiponectin inhibits endothelial synthesis of interleukin-8. Circ Res 97: 1245-1252, 2005. (Pubitemid 43755181)
16. Lee MH, Klein RL, El-Shewy HM, Luttrell DK, Luttrell LM. The adiponectin receptors AdipoR1 and AdipoR2 activate ERK1/2 through a Src/Ras-dependent pathway and stimulate cell growth. Biochemistry 47: 11682-11692, 2008.
17. Liao W, Yu C, Wen J, Jia W, Li G, Ke Y, Zhao S, Campell W. Adiponectin Induces Interleukin-6 Production and Activates STAT3 in Adult Mouse Cardiac Fibroblasts. Biol Cell 101: 263-272, 2008.
18. Luedde T, Beraza N, Kotsikoris V, van Loo G, Nenci A, De Vos R, Roskams T, Trautwein C, Pasparakis M. Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 11: 119-132, 2007. (Pubitemid 46209851)
19. Man K, Zhao Y, Xu A, Lo CM, Lam KS, Ng KT, Ho JW, Sun CK, Lee TK, Li XL, Fan ST. Fat-derived hormone adiponectin combined with FTY720 significantly improves small-for-size fatty liver graft survival. Am J Transplant 6: 467-476, 2006. (Pubitemid 43382132)
20. Matsukawa A, Kudo S, Maeda T, Numata K, Watanabe H, Takeda K, Akira S, Ito T. Stat3 in resident macrophages as a repressor protein of inflammatory response. J Immunol 175: 3354-3359, 2005. (Pubitemid 41170557)
21. Matsuura F, Oku H, Koseki M, Sandoval JC, Yuasa-Kawase M, Tsubakio-Yamamoto K, Masuda D, Maeda N, Tsujii K, Ishigami M, Nishida M, Hirano K, Kihara S, Hori M, Shimomura I, Yamashita S. Adiponectin accelerates reverse cholesterol transport by increasing high density lipoprotein assembly in the liver. Biochem Biophys Res Commun 358: 1091-1095, 2007. (Pubitemid 46829000)
22. Miyazaki T, Bub JD, Uzuki M, Iwamoto Y. Adiponectin activates c-Jun NH2-terminal kinase and inhibits signal transducer and activator of transcription 3. Biochem Biophys Res Commun 333: 79-87, 2005. (Pubitemid 40813449)
23. Neumeier M, Hellerbrand C, Gabele E, Buettner R, Bollheimer C, Weigert J, Schaffler A, Weiss TS, Lichtenauer M, Scholmerich J, Buechler C. Adiponectin and its receptors in rodent models of fatty liver disease and liver cirrhosis. World J Gastroenterol 12: 5490-5494, 2006. (Pubitemid 44501807)
24. Neumeier M, Weigert J, Schaffler A, Weiss T, Kirchner S, Laberer S, Scholmerich J, Buechler C. Regulation of adiponectin receptor 1 in human hepatocytes by agonists of nuclear receptors. Biochem Biophys Res Commun 334: 924-929, 2005. (Pubitemid 41033208)
25. Neumeier M, Weigert J, Schaffler A, Weiss TS, Schmidl C, Buttner R, Bollheimer C, Aslanidis C, Scholmerich J, Buechler C. Aldehyde oxidase 1 is highly abundant in hepatic steatosis and is downregulated by adiponectin and fenofibric acid in hepatocytes in vitro. Biochem Biophys Res Commun 350: 731-735, 2006. (Pubitemid 44547907)
26. Osawa Y, Nagaki M, Banno Y, Brenner DA, Asano T, Nozawa Y, Moriwaki H, Nakashima S. Tumor necrosis factor alpha-induced interleukin- 8 production via NF-kappaB and phosphatidylinositol 3-kinase/Akt pathways inhibits cell apoptosis in human hepatocytes. Infect Immun 70: 6294-6301, 2002. (Pubitemid 35192721)
27. Parganas E, Wang D, Stravopodis D, Topham DJ, Marine JC, Teglund S, Vanin EF, Bodner S, Colamonici OR, van Deursen JM, Grosveld G, Ihle JN. Jak2 is essential for signaling through a variety of cytokine receptors. Cell 93: 385-395, 1998. (Pubitemid 28232083)
28. Remick DG. Interleukin-8. Crit Care Med 33: S466-S467, 2005.
29. Rovin BH, Song H. Chemokine induction by the adipocyte-derived cytokine adiponectin. Clin Immunol 120: 99-105, 2006. (Pubitemid 43903386)
30. Saijo S, Nagata K, Nakano Y, Tobe T, Kobayashi Y. Inhibition by adiponectin of IL-8 production by human macrophages upon coculturing with late apoptotic cells. Biochem Biophys Res Commun 334: 1180-1183, 2005. (Pubitemid 41074698)
31. Schaffler A, Ehling A, Neumann E, Herfarth H, Paul G, Tarner I, Gay S, Buechler C, Scholmerich J, Muller-Ladner U. Role of specificity protein-1, PPARgamma, and pituitary protein transcription factor-1 in transcriptional regulation of the murine CORS-26 promoter. Biochim Biophys Acta 1678: 150-156, 2004. (Pubitemid 38626176)
32. Schaffler A, Scholmerich J, Buchler C. Mechanisms of disease: adipocytokines and visceral adipose tissue- emerging role in nonalcoholic fatty liver disease. Nat Clin Pract Gastroenterol Hepatol 2: 273-280, 2005. (Pubitemid 40895403)
33. Straczkowski M, Dzienis-Straczkowska S, Stepien A, Kowalska I, Szelachowska M, Kinalska I. Plasma interleukin-8 concentrations are increased in obese subjects and related to fat mass and tumor necrosis factor-alpha system. J Clin Endocrinol Metab 87: 4602-4606, 2002. (Pubitemid 35247047)
34. Tang CH, Chiu YC, Tan TW, Yang RS, Fu WM. Adiponectin enhances IL-6 production in human synovial fibroblast via an AdipoR1 receptor, AMPK, p38, and NF-kappa B pathway. J Immunol 179: 5483-5492, 2007.
35. Thasler WE, Weiss TS, Schillhorn K, Stoll PT, Irrgang B, Jauch KW. Charitable State-Controlled Foundation Human Tissue and Cell Research: Ethic and Legal Aspects in the Supply of Surgically Removed Human Tissue For Research in the Academic and Commercial Sector in Germany. Cell Tissue Bank 4: 49-56, 2003.
36. Tomizawa A, Hattori Y, Kasai K, Nakano Y. Adiponectin induces NF-kappaB activation that leads to suppression of cytokine-induced NF-kappaB activation in vascular endothelial cells: globular adiponectin vs. high molecular weight adiponectin. Diab Vasc Dis Res 5: 123-127, 2008. (Pubitemid 351839284)
37. Torres DM, Harrison SA. Diagnosis and therapy of nonalcoholic steatohepatitis. Gastroenterology 134: 1682-1698, 2008.
38. Tsao TS, Murrey HE, Hug C, Lee DH, Lodish HF. Oligomerization state-dependent activation of NF-kappa B signaling pathway by adipocyte complement-related protein of 30 kDa (Acrp30). J Biol Chem 277: 29359-29362, 2002. (Pubitemid 41079218)
39. Uribe M, Zamora-Valdes D, Moreno-Portillo M, Bermejo-Martinez L, Pichardo-Bahena R, Baptista-Gonzalez HA, Ponciano-Rodriguez G, Uribe MH, Medina-Santillan R, Mendez-Sanchez N. Hepatic expression of ghrelin and adiponectin and their receptors in patients with nonalcoholic fatty liver disease. Ann Hepatol 7: 67-71, 2008.
40. Weigert J, Neumeier M, Wanninger J, Wurm S, Kopp A, Schober F, Filarsky M, Schaffler A, Zeitoun M, Aslanidis C, Buechler C. Reduced response to adiponectin and lower abundance of adiponectin receptor proteins in type 2 diabetic monocytes. FEBS Lett 582: 1777-1782, 2008.
41. Weiss TS, Pahernik S, Scheruebl I, Jauch KW, Thasler WE. Cellular damage to human hepatocytes through repeated application of 5-aminolevulinic acid. J Hepatol 38: 476-482, 2003. (Pubitemid 36399251)
42. Welte T, Zhang SS, Wang T, Zhang Z, Hesslein DG, Yin Z, Kano A, Iwamoto Y, Li E, Craft JE, Bothwell AL, Fikrig E, Koni PA, Flavell RA, Fu XY. STAT3 deletion during hematopoiesis causes Crohn's disease- like pathogenesis and lethality: a critical role of STAT3 in innate immunity. Proc Natl Acad Sci USA 100: 1879-1884, 2003.
43. 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 112: 91-100, 2003. (Pubitemid 38056380)
44. Yamauchi T, Nio Y, Maki T, Kobayashi M, Takazawa T, Iwabu M, Okada-Iwabu M, Kawamoto S, Kubota N, Kubota T, Ito Y, Kamon J, Tsuchida A, Kumagai K, Kozono H, Hada Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Awazawa M, Takamoto I, Froguel P, Hara K, Tobe K, Nagai R, Ueki K, Kadowaki T. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med 13: 332-339, 2007. (Pubitemid 46376688)
45. Yan E, Durazo F, Tong M, Hong K. Nonalcoholic fatty liver disease: pathogenesis, identification, progression, and management. Nutr Rev 65: 376-384, 2007. (Pubitemid 351804353)
46. Yoshida N, Katada K, Handa O, Takagi T, Kokura S, Naito Y, Mukaida N, Soma T, Shimada Y, Yoshikawa T, Okanoue T. Interleukin- 8 production via protease-activated receptor 2 in human esophageal epithelial cells. Int J Mol Med 19: 335-340, 2007.
47. Yu Z, Kone BC. The STAT3 DNA-binding domain mediates interaction with NF-kappaB p65 and iuducible nitric oxide synthase transrepression in mesangial cells. J Am Soc Nephrol 15: 585-591, 2004. (Pubitemid 38294788)
48. Zografos TA, Liaskos C, Rigopoulou EI, Togousidis E, Makaritsis K, Germenis A, Dalekos GN. Adiponectin: a new independent predictor of liver steatosis and response to IFN-alpha treatment in chronic hepatitis C. Am J Gastroenterol 103: 605-614, 2008.