Journal of Molecular and Cellular Cardiology
Volume 48, Issue 6 , Pages 1236-1244 , June 2010

Cardiomyocyte Toll-like receptor 4 is involved in heart dysfunction following septic shock or myocardial ischemia

  • Reut Fallach

      Affiliations

    • Gonda (Goldschmied) Medical Diagnostic Research Center, The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel
    • The Cardiac Research Laboratory of the Department of Cardiothoracic Surgery, Felsenstein Medical Research Center, Rabin Medical Center, Tel Aviv University, Petah Tikva, Israel
    • ,
  • Asher Shainberg

      Affiliations

    • Gonda (Goldschmied) Medical Diagnostic Research Center, The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel
    • ,
  • Orna Avlas

      Affiliations

    • Gonda (Goldschmied) Medical Diagnostic Research Center, The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel
    • The Cardiac Research Laboratory of the Department of Cardiothoracic Surgery, Felsenstein Medical Research Center, Rabin Medical Center, Tel Aviv University, Petah Tikva, Israel
    • ,
  • Michael Fainblut

      Affiliations

    • The Cardiac Research Laboratory of the Department of Cardiothoracic Surgery, Felsenstein Medical Research Center, Rabin Medical Center, Tel Aviv University, Petah Tikva, Israel
    • ,
  • Yelena Chepurko

      Affiliations

    • The Cardiac Research Laboratory of the Department of Cardiothoracic Surgery, Felsenstein Medical Research Center, Rabin Medical Center, Tel Aviv University, Petah Tikva, Israel
    • ,
  • Eyal Porat

      Affiliations

    • The Cardiac Research Laboratory of the Department of Cardiothoracic Surgery, Felsenstein Medical Research Center, Rabin Medical Center, Tel Aviv University, Petah Tikva, Israel
    • ,
  • Edith Hochhauser

      Affiliations

    • The Cardiac Research Laboratory of the Department of Cardiothoracic Surgery, Felsenstein Medical Research Center, Rabin Medical Center, Tel Aviv University, Petah Tikva, Israel
    • Corresponding Author InformationCorresponding author. Cardiac Research Laboratory, Felsenstein Medical Research Center, Rabin Medical Center, Petah Tikva 49100, Israel. Tel.: +972 3 9376284; fax: +972 3 9211478.

Received 16 September 2009 ,Revised 23 February 2010 ,Accepted 23 February 2010.

References 

  1. Timmers L, Sluijter PGJ, Van Keulen JK, Hoefer IE, Nederhoff MGJ, Goumans MJ, et al. Toll-like receptor 4 mediated mal adaptive left ventricular remodeling and impairs cardiac function after myocardial infarction. Circ Res. 2008;102:257–264
  2. Binck BW, Tsen MF, Islas M, White DJ, Schultz RA, Willis MS, et al. Bone marrow-derived cells contribute to contractile dysfunction in endotoxic shock. Am J Physiol Heart Circ Physiol. 2005;288:577–583
  3. John HB, Sumeet M, Yingjin W, Ryon MB, Keith RW. Toll-like receptor stimulation in cardiomyoctes decreases contractility and initiates an NF-κB dependent inflammatory response. Cardiovasc Res. 2006;72:384–393
  4. Baumgarten G, Knuefermann P, Nozaki N, Sivasurbramanian N, Mann DL, Vallejo JG. In vivo expression of proinflammatory mediators in the adult heart after endotoxin administration: the role of Toll-like receptor 4. J Infect Dis. 2001;183:1617–1624
  5. Oyama J, Blais C, Liu X, Pu M, Kobzik L, Kelly RA, et al. Reduced myocardial ischemia reperfusion injury in Toll-like receptor 4-deficient mice. Circulation. 2004;109:784–789
  6. Frantz S, Ertl G, Bauersachs J. Mechanisms of disease. Toll-like receptors in cardiovascular disease. Nature. 2007;4:444–454
  7. Thompson M, Kliewer A, Maass D. Increased cardiomyocyte intracellular calcium during endotoxin induced cardiac dysfunction in guinea pigs. Pediatr Res. 2000;47:669–676
  8. Hollestelle SC, De Vries MR, Van Keulen JK, Schoneveld AH, Vink A, Strijder CF, et al. Toll-like receptor 4 is involved in outward arterial remodeling. Circulation. 2004;109:393–398
  9. Ohashi K, Burkart V, Flohe S, Kolb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor 4 complex. J Immunol. 2000;164:558–561
  10. Frantz S, Kobzik L, Kim YD, Fukazawa R, Medzhitov R, Lee RT, et al. Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J Clin Invest. 1999;104:271–280
  11. Baumgarten G, Knuefermann P, Schuhmacher G, Vervoglvi V, Von Rappard J, Dreiner U, et al. Toll-like receptor 4, nitric oxide and myocardial depression in endotoxemia. Shock. 2006;25:43–49
  12. Boyd JH, Mathur S, Wang Y, Bateman RM, Walley KR. Toll-like receptor stimulation in cardiomyoctes decreases contractility and initiates an NF-kappaB dependent. Cardiovasc Res. 2006;72:384–393
  13. Tavener SA, Long EM, Robbins SM, McRae KM, Van Remmen H, Kubes P. Immune cell Toll-like receptor 4 is required for cardiac myocyte impairment during endotoxemia. Circ Res. 2004;95:700–707
  14. Zhao P, Wang J, He L, Ma H, Zhang X, Zhu X, et al. Deficiency in TLR4 signal transduction ameliorates cardiac injury and cardiomyocyte contractile dysfunction during ischemia. J Cell Mol Med. 2009;13:1513–1525
  15. Kim SC, Ghanem A, Stapel H, Tiemann K, Knuefermann P, Hoeft A, et al. Toll-like receptor 4 deficiency: smaller infarcts, but no gain in function. BMC Physiol. 2007;7:5–15
  16. Poon BY, Raharjo E, Patel KD, Tavener S, Kubes P. Complexity of inducible nitric oxide synthase: cellular source determines benefit versus toxicity. Circulation. 2003;108:1107–1112
  17. Hochhauser E, Cheporko Y, Yasovich N, Pinchas L, Offen D, Barhum Y, et al. Bax deficiency reduces infarct size and improves long-term function after myocardial infarction. Cell Biochem Biophys. 2007;47:11–20
  18. Kurrelmeyer KM, Michael LH, Baumgarten G, Taffet GE, Peschon JJ, Sivasubramanian N, et al. Endogenous tumor necrosis factor protects the adult cardiac myocyte against ischemic-induced apoptosis in a murine model of acute myocardial infarction. Proc Natl Acad Sci USA. 2000;97:5456–5461
  19. Ofir M, Arad M, Porat E, Freimark D, Chepurko Y, Vidne BA, et al. Increased glycogen stores due to gamma-AMPK overexpression protects against ischemia and reperfusion damage. Biochem Pharmacol. 2008;75:1482–1491
  20. Pearl-Yafe M, Yolcu ES, Stein J, Kaplan O, Shirwan H, Yaniv I, et al. Expression of Fas and Fas-ligand in donor hematopoietic stem and progenitor cells is dissociated from the sensitivity to apoptosis. Exp Hematol. 2007;35:1601–1612
  21. Nemoto S, Vallejo JG, Knuefermann P, Misra A, Defreitas G, Carabello BA, et al. Escherichia coli LPS-induced LV dysfunction: role of Toll-like receptor-4 in the adult heart. Am J Physiol Heart Circ Physiol. 2002;282:2316–2323
  22. Freeman BJ, Roberts MS, Vogler CA, Nicholes A, Hofling AA, Sands MS. Behavior and therapeutic efficacy of beta-glucuronidase-positive mononuclear phagocytes in a murine model of mucopolysaccharidosis type VII. Blood. 1999;94:2142–2150
  23. Feng Y, Zhao H, Xu X, Buys ES, Raher MJ, Bopassa JC, et al. Innate immune adaptor MyD88 mediates neutrophil recruitment and myocardial injury after ischemia–reperfusion in mice. Am J Physiol Heart Circ Physiol. 2008;295:1311–1318
  24. Riad A, Jäger S, Sobirey M, Escher F, Yaulema-Riss A, Westermann D, et al. Toll-like receptor-4 modulates survival by induction of left ventricular remodeling after myocardial infarction in mice. J Immunol. 2008;180:6954–6961
  25. Raeburn CD, Calkins CM, Zimmerman MA, Song Y, Ao L, Banerjee A, et al. Vascular cell adhesion molecule-1 expression is obligatory for endotoxin-induced myocardial neutrophil accumulation and contractile dysfunction. Surgery. 2001;130:319–325
  26. Tanaka M, Brooks SE, Richard VJ, FitzHarris GP, Stoler RC, Jennings RB, et al. Effect of anti-CD18 antibody on myocardial neutrophil accumulation and infarct size after ischemia and reperfusion in dogs. Circulation. 1993;87:526–535
  27. Romson JL, Hook BG, Kunkel SL, Abrams GD, Schork MA, Lucchesi BR. Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation. 1983;67:1016–1023
  28. Ao L, Zou N, Cleveland JC, Fullerton DA, Meng X. Myocardial TLR4 is a determinant of neutrophil infiltration after global myocardial ischemia: mediating KC and MCP-1 expression induced by extracellular HSC70. Am J Physiol Heart Circ Physiol. 2009;297:H21–H28
  29. Nian M, Lee P, Khaper N, Liu P. Inflammatory cytokines and post-myocardial infarction remodeling. Circ Res. 2004;94:1543–1553
  30. Piper HM, Meuter K, Schafer C. Cellular mechanisms of ischemia–reperfusion injury. Ann Thorac Surg. 2003;75:644–648
  31. Poon BY, Raharjo E, Patel KD, Tavener S, Kubes P. Complexity of inducible nitric oxide synthase: cellular source determines benefit versus toxicity. Circulation. 2003;108:1107–1112
  32. Feldman AM, Combes A, Wagner D, Kadakomi T, Kubota T, Li YY, et al. The role of tumor necrosis factor in the pathophysiology of heart failure. J Am Coll Cardiol. 2000;35:537–544
  33. Muller-Werdan U, Engelmann H, Werdan K. Cardiodepression by tumor necrosis factor-α. Eur Cytokine Netw. 1998;9:689–691
  34. Palsson McDermott EM, O'Neill LA. Signal transduction by the lipopolysaccharide receptor, Toll-like receptor 4. Immunology. 2004;113:153–162
  35. Kagan JC, Su T, Horng T, Chow A, Akira S, Medzhitov R. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferone-beta. Nat Immunol. 2008;9:343–345
  36. Chong AJ, Shimamoto A, Hampton CR, Takayama H, Spring DJ, Rothnie CL, et al. Toll-like receptor 4 mediates ischemia/reperfusion injury of the heart. J Thorac Cardiovasc Surg. 2004;128:170–179
  37. Cain BS, Meldrum DR, Dinarello CA, Meng X, Joo KS, Banerjee A, et al. Tumor necrosis factor-alpha and interleukin-1beta synergistically depress human myocardial function. Crit Care Med. 1999;27:1309–1318
  38. Thielmann M, Dörge H, Martin C, Belosjorow S, Schwanke U, van De Sand A, et al. Myocardial dysfunction with coronary microembolization: signal transduction through a sequence of nitric oxide, tumor necrosis factor-alpha, and sphingosine. Circ Res. 2002;19(90):807–813
  39. Cha J, Wang Z, Ao L, Zou N, Dinarello CA, Banerjee A, et al. Cytokines link Toll-like receptor 4 signaling to cardiac dysfunction after global myocardial ischemia. Ann Thorac Surg. 2008;85:1678–1685
  40. Valeur HS, Valen G. Innate immunity and myocardial adaptation to ischemia. Basic Res Cardiol. 2009;104:22–32
  41. Belosjorow S, Schulz R, Dörge H, Schade FU, Heusch G. Endotoxin and ischemic preconditioning: TNF-alpha concentration and myocardial infarct development in rabbits. Am J Physiol. 1999;277(6 Pt 2):H2470–H2475
  42. Skyschally A, Gres P, Hoffmann S, Haude M, Erbel R, Schulz R, et al. Bidirectional role of tumor necrosis factor-alpha in coronary microembolization: progressive contractile dysfunction versus delayed protection against infarction. Circ Res. 2007;100:140–146
  43. Baumgarten G, Kim SC, Stapel H, Vervölgyi V, Bittig A, Hoeft A, et al. Myocardial injury modulates the innate immune system and changes myocardial sensitivity. Basic Res Cardiol. 2006;101:427–435
  44. Roger T, Froidevaux C, Le Roy D, Reymond MK, Chanson AL, Mauri D, et al. Protection from lethal gram-negative bacterial sepsis by targeting Toll-like receptor 4. Proc Nati Acad Sci USA. 2009;106:2348–2352

PII: S0022-2828(10)00081-7

doi: 10.1016/j.yjmcc.2010.02.020

Journal of Molecular and Cellular Cardiology
Volume 48, Issue 6 , Pages 1236-1244 , June 2010

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