Toll-like receptor 4 mediates the early inflammatory response after cold ischemia/reperfusion

Transplantation

Volumn 84, Issue 10, 2007, Pages 1279-1287

  Kaczorowski, David J ^a   Nakao, Atsunori ^a   Mollen, Kevin P ^a   Vallabhaneni, Raghuveer ^a   Sugimoto, Ryujiro ^a   Kohmoto, Junichi ^a   Tobita, Kimimasa ^b   Zuckerbraun, Brian S ^a   McCurry, Kenneth R ^a   Murase, Noriko ^a   Billiar, Timothy R ^a,c  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b MCGOWAN INSTITUTE FOR REGENERATIVE MEDICINE   (United States)

^c PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

Author keywords

Cold storage; Inflammation; Ischemia reperfusion; Toll like receptors; Transplant

Indexed keywords

CYTOKINE; EARLY GROWTH RESPONSE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TOLL LIKE RECEPTOR 8; TROPONIN I; TUMOR NECROSIS FACTOR; TLR4 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; COLD ISCHEMIA; CONTROLLED STUDY; CYTOKINE PRODUCTION; GRAFT DYSFUNCTION; HEART GRAFT; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART TRANSPLANTATION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; ISOGRAFT; MALE; MEDIATOR; MOUSE; MOUSE MUTANT; NEUTROPHIL CHEMOTAXIS; NONHUMAN; ORGAN DONOR; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEFICIENCY; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; C3H MOUSE; COLD; GENETICS; PATHOPHYSIOLOGY; PHYSIOLOGY; POSTOPERATIVE COMPLICATION; REPERFUSION INJURY;

ANIMALS; COLD; HEART TRANSPLANTATION; INFLAMMATION; MALE; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; POSTOPERATIVE COMPLICATIONS; REPERFUSION INJURY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 38449109334     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.tp.0000287597.87571.17     Document Type: Article

References (61)

1. Laskowski I, Pratschke J, Wilhelm MJ, et al. Molecular and cellular events associated with ischemia/reperfusion injury. Ann Transplant 2000; 5: 29.
2. Morita K, Miura M, Paolone DR, et al. Early chemokine cascades in murine cardiac grafts regulate T cell recruitment and progression of acute allograft rejection. J Immunol 2001; 167: 2979.
3. Jassem W, Heaton ND. The role of mitochondria in ischemia/reperfusion injury in organ transplantation. Kidney Int 2004; 66: 514.
4. Boros P, Bromberg JS. New cellular and molecular immune pathways in ischemia/reperfusion injury. Am J Transplant 2006; 6: 652.
5. He H, Stone JR, Perkins DL. Analysis of robust innate immune response after transplantation in the absence of adaptive immunity. Transplantation 2002; 73: 853.
6. Miyake K. Innate immune sensing of pathogens and danger signals by cell surface Toll-like receptors. Semin Immunol 2007.
7. Mollen KP, Anand RJ, Tsung A, et al. Emerging paradigm: Toll-like receptor 4-sentinel for the detection of tissue damage. Shock 2006; 26: 430.
8. Akira S, Takeda K, Kaisho T. Toll-like receptors: Critical proteins linking innate and acquired immunity. Nat Immunol 2001; 2: 675.
9. Shen XD, Ke B, Zhai Y, et al. Toll-like receptor and heme oxygenase-1 signaling in hepatic ischemia/reperfusion injury. Am J Transplant 2005; 5: 1793.
10. Wu HS, Zhang JX, Wang L, et al. Toll-like receptor 4 involvement in hepatic ischemia/reperfusion injury in mice. Hepatobiliary Pancreat Dis Int 2004; 3: 250.
11. Zhai Y, Shen XD, O'Connell R, et al. Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3-dependent MyD88-independent pathway. J Immunol 2004; 173: 7115.
12. Tsung A, Hoffman RA, Izuishi K, et al. Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells. J Immunol 2005; 175: 7661.
13. Tsung A, Sahai R, Tanaka H, et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005; 201: 1135.
14. Shimamoto A, Pohlman TH, Shomura S, et al. Toll-like receptor 4 mediates lung ischemia-reperfusion injury. Ann Thorac Surg 2006; 82: 2017.
15. Chong AJ, Shimamoto A, Hampton CR, et al. Toll-like receptor 4 mediates ischemia/reperfusion injury of the heart. J Thorac Cardiovasc Surg 2004; 128: 170.
16. Oyama J, Blais C, Jr., Liu X, et al. Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation 2004; 109: 784.
17. Shimamoto A, Chong AJ, Yada M, et al. Inhibition of Toll-like receptor 4 with eritoran attenuates myocardial ischemia-reperfusion injury. Circulation 2006; 114: I270.
18. Poltorak A, He X, Smirnova I, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 1998; 282: 2085.
19. Ono K, Lindsey ES. Improved technique of heart transplantation in rats. J Thorac Cardiovasc Surg 1969; 57: 225.
20. Schmittgen TD, Zakrajsek BA, Mills AG, et al. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: Comparison of endpoint and real-time methods. Anal Biochem 2000; 285: 194.
21. Wang CY, Naka Y, Liao H, et al. Cardiac graft intercellular adhesion molecule-1 (ICAM-1) and interleukin-1 expression mediate primary isograft failure and induction of ICAM-1 in organs remote from the site of transplantation. Circ Res 1998; 82: 762.
22. Pinsky D, Oz M, Liao H, et al. Restoration of the camp 2nd messenger pathway enhances cardiac preservation for transplantation in a heterotopic rat model. J Clin Invest 1993; 92: 2994.
23. Nakao A, Neto JS, Kanno S, et al. Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant 2005; 5: 282.
24. Daemen MA, van't Veer C, Wolfs TG, Buurman WA. Ischemia/reperfusion- induced IFN-gamma up-regulation: involvement of IL-12 and IL-18. J Immunol 1999; 162: 5506.
25. Li L, Huang L, Sung SS, et al. NKT cell activation mediates neutrophil IFN-gamma production and renal ischemia-reperfusion injury. J Immunol 2007; 178: 5899.
26. Lappas CM, Day YJ, Marshall MA, et al. Adenosine A2A receptor activation reduces hepatic ischemia reperfusion injury by inhibiting CD1d-dependent NKT cell activation. J Exp Med 2006; 203: 2639.
27. Eppinger MJ, Ward PA, Bolling SF, Deeb GM. Regulatory effects of interleukin-10 on lung ischemia-reperfusion injury. J Thorac Cardiovasc Surg 1996; 112: 1301.
28. Donckier V, Loi P, Closset J et al. Preconditioning of donors with interleukin-10 reduces hepatic ischemia-reperfusion injury after liver transplantation in pigs. Transplantation 2003; 75: 902.
29. Hayward R, Nossuli TO, Scalia R, Lefer AM. Cardioprotective effect of interleukin-10 in murine myocardial ischemia-reperfusion. Eur J Pharmacol 1997; 334: 157.
30. Yamazaki T, Seko Y, Tamatani T, et al. Expression of intercellular adhesion molecule-1 in rat heart with ischemia/reperfusion and limitation of infarct size by treatment with antibodies against cell adhesion molecules. Am J Pathol 1993; 143: 410.
31. Jaakkola K, Jalkanen S, Kaunismaki K, et al. Vascular adhesion protein-1, intercellular adhesion molecule-1 and P-selectin mediate leukocyte binding to ischemic heart in humans. J Am Coll Cardiol 2000; 36: 122.
32. Ma XL, Lefer DJ, Lefer AM, Rothlein R. Coronary endothelial and cardiac protective effects of a monoclonal antibody to intercellular adhesion molecule-1 in myocardial ischemia and reperfusion. Circulation 1992; 86: 937.
33. Tamiya Y, Yamamoto N, Uede T. Protective effect of monoclonal antibodies against LFA-1 and ICAM-1 on myocardial reperfusion injury following global ischemia in rat hearts. Immunopharmacology 1995; 29: 53.
34. Yan SF, Fujita T, Lu J, et al. Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat Med 2000; 6: 1355.
35. Bhindi R, Khachigian LM, Lowe HC. DNAzymes targeting the transcription factor Egr-1 reduce myocardial infarct size following ischemia-reperfusion in rats. J Thromb Haemost 2006; 4: 1479.
36. Okada M, Wang CY, Hwang DW, et al. Transcriptional control of cardiac allograft vasculopathy by early growth response gene-1 (Egr-1). Circ Res 2002; 91: 135.
37. Zuckerbraun BS, Billiar TR. Heme oxygenase-1: A cellular hercules. Hepatology 2003; 37: 742.
38. Amersi F, Buelow R, Kato H, et al. Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J Clin Invest 1999; 104: 1631.
39. Chauveau C, Bouchet D, Roussel JC, et al. Gene transfer of heme oxygenase-1 and carbon monoxide delivery inhibit chronic rejection. Am J Transplant 2002; 2: 581.
40. Soares MP, Lin Y, Anrather J, et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 1998; 4: 1073.
41. Shears LL, Kawaharada N, Tzeng E, et al. Inducible nitric oxide synthase suppresses the development of allograft arteriosclerosis. J Clin Invest 1997; 100: 2035.
42. Koglin J, Glysing-Jensen T, Mudgett JS, Russell ME. Exacerbated transplant arteriosclerosis in inducible nitric oxide-deficient mice. Circulation 1998; 97: 2059.
43. Baumgarten G, Knuefermann P, Schuhmacher G, et al. Toll-like receptor 4, nitric oxide, and myocardial depression in endotoxemia. Shock 2006; 25: 43.
44. Boyd JH, Mathur S, Wang Y, et al. Toll-like receptor stimulation in cardiomyoctes decreases contractility and initiates an NF-kappaB dependent inflammatory response. Cardiovasc Res 2006; 72: 384.
45. Jordan JE, Zhao ZQ, Vinten-Johansen J. The role of neutrophils in myocardial ischemia-reperfusion injury. Cardiovasc Res 1999; 43: 860.
46. Adams JE, III, Sicard GA, Allen BT, et al. Diagnosis of perioperative myocardial infarction with measurement of cardiac troponin I. N Engl J Med 1994; 330: 670.
47. Labarrere CA, Nelson DR, Cox CJ, et al. Cardiac-specific troponin I levels and risk of coronary artery disease and graft failure following heart transplantation. JAMA 2000; 284: 457.
48. Akashi S, Shimazu R, Ogata H, et al. Cutting edge: Cell surface expression and lipopolysaccharide signaling via the toll-like receptor 4-MD-2 complex on mouse peritoneal macrophages. J Immunol 2000; 164: 3471.
49. Sabroe I, Dower SK, Whyte MK. The role of Toll-like receptors in the regulation of neutrophil migration, activation, and apoptosis. Clin Infect Dis 2005:41 Suppl 7: S421.
50. Zeuke S, Ulmer AJ, Kusumoto S, et al. TLR4-mediated inflammatory activation of human coronary artery endothelial cells by LPS. Cardiovasc Res 2002; 56: 126.
51. Kim SC, Ghanem A, Stapel H, et al. Toll-like receptor 4 deficiency: Smaller infarcts, but no gain in function. BMC Physiol 2007; 7: 5.
52. Samstein B, Johnson GB, Platt JL. Toll-like receptor-4 and allograft responses. Transplantation 2004; 77: 475.
53. Chen L, Wang T, Zhou P, et al. TLR engagement prevents transplantation tolerance. Am J Transplant 2006; 6: 2282.
54. Thornley TB, Brehm MA, Markees TG, et al. TLR agonists abrogate costimulation blockade-induced prolongation of skin allografts. J Immunol 2006; 176: 1561.
55. Goldstein DR, Tesar BM, Akira S, Lakkis FG. Critical role of the Toll-like receptor signal adaptor protein MyD88 in acute allograft rejection. J Clin Invest 2003; 111: 1571.
56. McKay D, Shigeoka A, Rubinstein M, Surh C, Sprent J. Simultaneous deletion of MyD88 and Trif delays major histocompatibility and minor antigen mismatch allograft rejection. Eur J Immunol 2006; 36: 1994.
57. Palmer SM, Burch LH, Trindade AJ, et al. Innate immunity influences long-term outcomes after human lung transplant. Am J Respir Crit Care Med 2005; 171: 780.
58. Palmer SM, Burch LH, Mir S, et al. Donor polymorphisms in Toll-like receptor-4 influence the development of rejection after renal transplantation. Clin Transplant 2006; 20: 30.
59. Tanaka M, Mokhtari GK, Terry RD, et al. Prolonged cold ischemia in rat cardiac allografts promotes ischemia-reperfusion injury and the development of graft coronary artery disease in a linear fashion. J Heart Lung Transplant 2005; 24: 1906.
60. Methe H, Zimmer E, Grimm C, et al. Evidence for a role of toll-like receptor 4 in development of chronic allograft rejection after cardiac transplantation. Transplantation 2004; 78: 1324.
61. O'Neill LAJ, Bowie AG. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nature Rev Immunol 2007; 7: 353.