Deficiency of TNFR1 protects myocardium through SOCS3 and IL-6 but not p38 MAPK or IL-1β

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 292, Issue 4, 2007, Pages

  Wang, Meijing ^a   Markel, Troy ^a   Crisostomo, Paul ^a   Herring, Christine ^a   Meldrum, Kirstan K ^a   Lillemoe, Keith D ^a   Meldrum, Daniel R ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Emerson Hall 215 ^*  (United States)

Author keywords

Cytokines; Inflammation; Ischemia; Reperfusion; Signaling; Suppressors of cytokine signaling; Tumor necrosis factor receptor type 1

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE P38; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR ALPHA RECEPTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; HEART FAILURE; HEART PROTECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; HEART; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; MICE; MICE, KNOCKOUT; MYOCARDITIS; MYOCARDIUM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34147185577     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01063.2006     Document Type: Article

References (45)

1. Alexander WS, Hilton DJ. The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu Rev Immunol 22: 503-529, 2004.
2. Berlato C, Cassatella MA, Kinjyo I, Gatto L, Yoshimura A, Bazzoni F. Involvement of suppressor of cytokine signaling-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation. J Immunol 168: 6404-6411, 2002.
3. Beyaert R, Cuenda A, Vanden Berghe W, Plaisance S, Lee JC, Haegeman G, Cohen P, Fiers W. The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J 15: 1914-1923, 1996.
4. Bode JG, Nimmesgern A, Schmitz J, Schaper F, Schmitt M, Frisch W, Haussinger D, Heinrich PC, Graeve L. LPS and TNFalpha induce SOCS3 mRNA and inhibit IL-6-induced activation of STAT3 in macrophages. FEBS Lett 463: 365-370, 1999.
5. Croker BA, Krebs DL, Zhang JG, Wormald S, Willson TA, Stanley EG, Robb L, Greenhalgh CJ, Forster I, Clausen BE, Nicola NA, Metcalf D, Hilton DJ, Roberts AW, Alexander WS. SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immun 4: 540-545, 2003.
6. Finkel MS, Oddis CV, Jacob TD, Watkins SC, Hattler BG, Simmons RL. Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science 257: 387-389, 1992.
7. Fisher CJ Jr, Agosti JM, Opal SM, Lowry SF, Balk RA, Sadoff JC, Abraham E, Schein RM, Benjamin E. Treatment of septic shock with the tumor necrosis factor receptor: Fc fusion protein. The Soluble TNF Receptor Sepsis Study Group. N Engl J Med 334: 1697-1702, 1996.
8. Frangogiannis NG, Lindsey ML, Michael LH, Youker KA, Bressler RB, Mendoza LH, Spengler RN, Smith CW, Entman ML. Resident cardiac mast cells degranulate and release preformed TNF-alpha, initiating the cytokine cascade in experimental canine myocardial ischemia/reperfusion. Circulation 98: 699-710, 1998.
9. Hong F, Nguyen VA, Gao B. Tumor necrosis factor alpha attenuates interferon alpha signaling in the liver: involvement of SOCS3 and SHP2 and implication in resistance to interferon therapy. FASEB J 15: 1595-1597, 2001.
10. Hsu H, Shu HB, Pan MG, Goeddel DV. TRADD-TRAF2 and TRADDFADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84: 299-308, 1996.
11. Irwin MW, Mak S, Mann DL, Qu R, Penninger JM, Yan A, Dawood F, Wen WH, Shou Z, Liu P. Tissue expression and immunolocalization of tumor necrosis factor-alpha in postinfarction dysfunctional myocardium. Circulation 99: 1492-1498, 1999.
12. Jo D, Liu D, Yao S, Collins RD, Hawiger J. Intracellular protein therapy with SOCS3 inhibits inflammation and apoptosis. Nat Med 11: 892-898, 2005.
13. Kadokami T, McTiernan CF, Kubota T, Frye CS, Bounoutas GS, Robbins PD, Watkins SC, Feldman AM. Effects of soluble TNF receptor treatment on lipopolysaccharide-induced myocardial cytokine expression. Am J Physiol Heart Circ Physiol 280: H2281-H2291, 2001.
14. Krown KA, Page MT, Nguyen C, Zechner D, Gutierrez V, Comstock KL, Glembotski CC, Quintana PJ, Sabbadini RA. Tumor necrosis factor alpha-induced apoptosis in cardiac myocytes. Involvement of the sphingolipid signaling cascade in cardiac cell death. J Clin Invest 98: 2854-2865, 1996.
15. Kubota T, Bounoutas GS, Miyagishima M, Kadokami T, Sanders VJ, Bruton C, Robbins PD, McTiernan CF, Feldman AM. Soluble tumor necrosis factor receptor abrogates myocardial inflammation but not hypertrophy in cytokine-induced cardiomyopathy. Circulation 101: 2518-2525, 2000.
16. Kubota T, Miyagishima M, Frye CS, Alber SM, Bounoutas GS, Kadokami T, Watkins SC, McTiernan CF, Feldman AM. Overexpression of tumor necrosis factor-alpha activates both anti- and pro-apoptotic pathways in the myocardium. J Mol Cell Cardiol 33: 1331-1344, 2001.
17. Kupatt C, Habazettl H, Goedecke A, Wolf DA, Zahler S, Boekstegers P, Kelly RA, Becker BF. Tumor necrosis factor-alpha contributes to ischemia- and reperfusion-induced endothelial activation in isolated hearts. Circ Res 84: 392-400, 1999.
18. Kurrelmeyer KM, Michael LH, Baumgarten G, Taffet GE, Peschon JJ, Sivasubramanian N, Entman ML, Mann DL. Endogenous tumor necrosis factor protects the adult cardiac myocyte against ischemicinduced apoptosis in a murine model of acute myocardial infarction. Proc Natl Acad Sci USA 97: 5456-5461, 2000.
19. Maass DL, White J, Horton JW. IL-1beta and IL-6 act synergistically with TNF-alpha to alter cardiac contractile function after burn trauma. Shock 18: 360-366, 2002.
20. MacEwan DJ. TNF receptor subtype signalling: differences and cellular consequences. Cell Signal 14: 477-492, 2002.
21. Maekawa N, Wada H, Kanda T, Niwa T, Yamada Y, Saito K, Fujiwara H, Sekikawa K, Seishima M. Improved myocardial ischemia/ reperfusion injury in mice lacking tumor necrosis factor-alpha. J Am Coll Cardiol 39: 1229-1235, 2002.
22. Meldrum DR. Tumor necrosis factor in the heart. Am J Physiol Regul Integr Comp Physiol 274: R577-R595, 1998.
23. Meldrum DR, Cleveland JC Jr, Cain BS, Meng X, Harken AH. Increased myocardial tumor necrosis factor-alpha in a crystalloid-perfused model of cardiac ischemia-reperfusion injury. Ann Thorac Surg 65: 439-443, 1998.
24. Mizushima Y, Wang P, Jarrar D, Cioffi WG, Bland KI, Chaudry IH. Preinduction of heat shock proteins protects cardiac and hepatic functions following trauma and hemorrhage. Am J Physiol Regul Integr Comp Physiol 278: R352-R359, 2000.
25. Oral H, Dorn GW 2nd, Mann DL. Sphingosine mediates the immediate negative inotropic effects of tumor necrosis factor-alpha in the adult mammalian cardiac myocyte. J Biol Chem 272: 4836-4842, 1997.
26. Ramani R, Mathier M, Wang P, Gibson G, Togel S, Dawson J, Bauer A, Alber S, Watkins SC, McTiernan CF, Feldman AM. Inhibition of tumor necrosis factor receptor-1-mediated pathways has beneficial effects in a murine model of postischemic remodeling. Am J Physiol Heart Circ Physiol 287: H1369-H1377, 2004.
27. Sack M. Tumor necrosis factor-alpha in cardiovascular biology and the potential role for anti-tumor necrosis factor-alpha therapy in heart disease. Pharmacol Ther 94: 123-135, 2002.
28. Song GY, Chung CS, Chaudry IH, Ayala A. MAPK p38 antagonism as a novel method of inhibiting lymphoid immune suppression in polymicrobial sepsis. Am J Physiol Cell Physiol 281: C662-C669, 2001.
29. Song GY, Chung CS, Jarrar D, Chaudry IH, Ayala A. Evolution of an immune suppressive macrophage phenotype as a product of P38 MAPK activation in polymicrobial sepsis. Shock 15: 42-48, 2001.
30. Szalay L, Shimizu T, Suzuki T, Yu HP, Choudhry MA, Schwacha MG, Rue LW 3rd, Bland KI, Chaudry IH. Estradiol improves cardiac and hepatic function after trauma-hemorrhage: role of enhanced heat shock protein expression. Am J Physiol Regul Integr Comp Physiol 290: R812-R818, 2006.
31. Tavener SA, Kubes P. Cellular and molecular mechanisms underlying LPS-associated myocyte impairment. Am J Physiol Heart Circ Physiol 290: H800-H806, 2006.
32. Thobe BM, Frink M, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH. Src family kinases regulate p38 MAPK-mediated IL-6 production in Kupffer cells following hypoxia. Am J Physiol Cell Physiol 291: C476-C482, 2006.
33. Torre-Amione G, Kapadia S, Lee J, Bies RD, Lebovitz R, Mann DL. Expression and functional significance of tumor necrosis factor receptors in human myocardium. Circulation 92: 1487-1493, 1995.
34. Vanden Berghe W, Plaisance S, Boone E, De Bosscher K, Schmitz ML, Fiers W, Haegeman G. p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways are required for nuclear factor-kappaB p65 transactivation mediated by tumor necrosis factor. J Biol Chem 273: 3285-3290, 1998.
35. Vandenabeele P, Declercq W, Beyaert R, Fiers W. Two tumour necrosis factor receptors: structure and function. Trends Cell Biol 5: 392-399, 1995.
36. Wang M, Baker L, Tsai BM, Meldrum KK, Meldrum DR. Sex differences in the myocardial inflammatory response to ischemia-reperfusion injury. Am J Physiol Endocrinol Metab 288: E321-E326, 2005.
37. Wang M, Sankula R, Tsai BM, Meldrum KK, Turrentine M, March KL, Brown JW, Dinarello CA, Meldrum DR. P38 MAPK mediates myocardial proinflammatory cytokine production and endotoxin-induced contractile suppression. Shock 21: 170-174, 2004.
38. Wang M, Tsai BM, Crisostomo PR, Meldrum DR. Tumor necrosis factor receptor 1 signaling resistance in the female myocardium during ischemia. Circulation 114: I282-I289, 2006.
39. Wang M, Tsai BM, Kher A, Baker LB, Wairiuko GM, Meldrum DR. Role of endogenous testosterone in myocardial proinflammatory and proapoptotic signaling after acute ischemia-reperfusion. Am J Physiol Heart Circ Physiol 288: H221-H226, 2005.
40. Wang M, Tsai BM, Turrentine MW, Mahomed Y, Brown JW, Meldrum DR. p38 Mitogen activated protein kinase mediates both death signaling and functional depression in the heart. Ann Thorac Surg 80: 2235-2241, 2005.
41. Wang Y, Ahmad N, Kudo M, Ashraf M. Contribution of Akt and endothelial nitric oxide synthase to diazoxide-induced late preconditioning. Am J Physiol Heart Circ Physiol 287: H1125-H1131, 2004.
42. ATP channel as an end effector of cardioprotection during late preconditioning: triggering role of nitric oxide. J Mol Cell Cardiol 33: 2037-2046, 2001.
43. Wysk M, Yang DD, Lu HT, Flavell RA, Davis RJ. Requirement of mitogen-activated protein kinase kinase 3 (MKK3) for tumor necrosis factor-induced cytokine expression. Proc Natl Acad Sci USA 96: 3763-3768, 1999.
44. Xu M, Wang Y, Hirai K, Ayub A, Ashraf M. Calcium preconditioning inhibits mitochondrial permeability transition and apoptosis. Am J Physiol Heart Circ Physiol 280: H899-H908, 2001.
45. 2+-overload. Biochem Biophys Res Commun 327: 57-63, 2005.