Increased Th17 rather than Th1 alloimmune response is associated with cardiac allograft vasculopathy after hypothermic preservation in the rat

Journal of Heart and Lung Transplantation

Volumn 29, Issue 9, 2010, Pages 1047-1057

  Syrjälä, Simo O ^a   Keränen, Mikko Ai ^a   Tuuminen, Raimo ^a   Nykänen, Antti I ^a   Tammi, Markku ^b   Krebs, Rainer ^a   Lemström, Karl B ^c  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Cardiac allograft; Innate immunity; Ischemia reperfusion injury; Preservation; rejection; Th17

Indexed keywords

B7 ANTIGEN; CD83 ANTIGEN; CHEMOKINE RECEPTOR CXCR7; CYCLOSPORIN A; GAMMA INTERFERON; HIGH MOBILITY GROUP B1 PROTEIN; HYALURONAN SYNTHASE 1; HYALURONAN SYNTHASE 2; INTERLEUKIN 23; INTERLEUKIN 6; MESSENGER RNA; SECONDARY LYMPHOID TISSUE CHEMOKINE; SYNTHETASE; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 3; CYCLOSPORIN; IMMUNOGLOBULIN; IMMUNOSUPPRESSIVE AGENT; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN;

ACUTE GRAFT REJECTION; ADAPTIVE IMMUNITY; ALLOIMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIOSCLEROSIS; ARTICLE; CARDIAC ALLOGRAFT VASCULOPATHY; CARDIAC GRAFT REJECTION; CD4+ T LYMPHOCYTE; CHRONIC GRAFT REJECTION; CRYOPRESERVATION; DENDRITIC CELL; HEART MUSCLE FIBROSIS; HEART MUSCLE ISCHEMIA; HEART TRANSPLANTATION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; LYMPHOCYTIC INFILTRATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH1 CELL; TH17 CELL; UPREGULATION; ACUTE DISEASE; ALLOTRANSPLANTATION; ANIMAL; CHRONIC DISEASE; GENETICS; GRAFT REJECTION; IMMUNOLOGY; METHODOLOGY; ORGAN PRESERVATION; PATHOLOGY; RAT STRAIN; REPERFUSION; TIME; WISTAR FURTH RAT;

ACUTE DISEASE; ANIMALS; ANTIGENS, CD; CHRONIC DISEASE; CYCLOSPORINE; DENDRITIC CELLS; GRAFT REJECTION; HEART TRANSPLANTATION; IMMUNOGLOBULINS; IMMUNOSUPPRESSIVE AGENTS; MEMBRANE GLYCOPROTEINS; ORGAN PRESERVATION; RATS; RATS, INBRED STRAINS; RATS, INBRED WF; REPERFUSION; RNA, MESSENGER; TH1 CELLS; TH17 CELLS; TIME FACTORS; TRANSPLANTATION, HOMOLOGOUS;

EID: 79551684235     PISSN: 10532498     EISSN: 15573117     Source Type: Journal    
DOI: 10.1016/j.healun.2010.04.012     Document Type: Article

References (42)

1. Lechler RI, Sykes M, Thomson AW, Turka LA. Organ transplantation - how much of the promise has been realized? Nat Med 2005;11: 605-13. (Pubitemid 40868300)
2. Taylor DO, Edwards LB, Aurora P, et al. Registry of the International Society for Heart and Lung Transplantation: twenty-fifth official adult heart transplant report - 2008. J Heart Lung Transplant 2008;27:943-56.
3. Wang CY, Aronson I, Takuma S, et al. cAMP pulse during preservation inhibits the late development of cardiac isograft and allograft vasculopathy. Circ Res 2000;86:982-8. (Pubitemid 30324311)
4. Banner NR, Thomas HL, Curnow E, Hussey JC, Rogers CA, Bonser RS. The importance of cold and warm cardiac ischemia for survival after heart transplantation. Transplantation 2008;86:542-7.
5. Dumitrescu C, Biondi R, Xia Y, et al. Myocardial ischemia results in tetrahydrobiopterin (BH4) oxidation with impaired endothelial function ameliorated by BH4. Proc Natl Acad Sci U S A 2007;104: 15081-6. (Pubitemid 47619596)
6. Boros P, Bromberg JS. New cellular and molecular immune pathways in ischemia/reperfusion injury. Am J Transplant 2006;6:652-8. (Pubitemid 43345001)
7. Walker WE, Nasr IW, Camirand G, Tesar BM, Booth CJ, Goldstein DR. Absence of innate MyD88 signaling promotes inducible allograft acceptance. J Immunol 2006;177:5307-16. (Pubitemid 44527603)
8. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature 2000;406:782-7.
9. Tsan MF, Gao B. Endogenous ligands of Toll-like receptors. J Leukoc Biol 2004;76:514-9. (Pubitemid 39129081)
10. Andrassy M, Volz HC, Igwe JC, et al. High-mobility group box-1 in ischemia-reperfusion injury of the heart. Circulation 2008;117:3216-26.
11. Barton GM, Medzhitov R. Toll-like receptor signaling pathways. Science 2003;300:1524-5. (Pubitemid 36682871)
12. Rossi M, Young JW. Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J Immunol 2005;175:1373-81. (Pubitemid 41023036)
13. Forster R, Davalos-Misslitz AC, Rot A. CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 2008;8:362-71. (Pubitemid 351595218)
14. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 cells. Annu Rev Immunol 2009;27:485-517.
15. Yuan X, Paez-Cortez J, Schmitt-Knosalla I, et al. A novel role of CD4 Th17 cells in mediating cardiac allograft rejection and vasculopathy. J Exp Med 2008;205:3133-44.
16. Tammi R, Agren UM, Tuhkanen AL, Tammi M. Hyaluronan metabolism in skin. Prog Histochem Cytochem 1994;29:1-81.
17. Lehmann M, Graser E, Risch K, et al. Anti-CD4 monoclonal antibodyinduced allograft tolerance in rats despite persistence of donor-reactive T cells. Transplantation 1997;64:1181-7. (Pubitemid 27467946)
18. Taylor AL, Watson CJ, Bradley JA. Immunosuppressive agents in solid organ transplantation: mechanisms of action and therapeutic efficacy. Crit Rev Oncol Hematol 2005;56:23-46. (Pubitemid 41278644)
19. Mas VR, Archer KJ, Yanek K, et al. Gene expression patterns in deceased donor kidneys developing delayed graft function after kidney transplantation. Transplantation 2008;85:626-35.
20. Tesar BM, Zhang J, Li Q, Goldstein DR. TH1 immune responses to fully MHC mismatched allografts are diminished in the absence of MyD88, a toll-like receptor signal adaptor protein. Am J Transplant 2004;4:1429-39. (Pubitemid 39159057)
21. Zhao P, Wang J, He L, et al. Deficiency in TLR4 signal transduction ameliorates cardiac injury and cardiomyocyte contractile dysfunction during ischemia. J Cell Mol Med 2009;13:1513-25.
22. Wu H, Chen G, Wyburn KR, et al. TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 2007;117:2847-59. (Pubitemid 47529615)
23. Shen XD, Ke B, Zhai Y, et al. Absence of toll-like receptor 4 (TLR4) signaling in the donor organ reduces ischemia and reperfusion injury in a murine liver transplantation model. Liver Transpl 2007;13:1435-43. (Pubitemid 47629578)
24. Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-inducible enhancers. FASEB J 1995;9:899-909.
25. Chen Q, Fisher DT, Clancy KA, et al. Fever-range thermal stress promotes lymphocyte trafficking across high endothelial venules via an interleukin 6 trans-signaling mechanism. Nat Immunol 2006;7: 1299-308. (Pubitemid 46111251)
26. Shen H, Goldstein DR. IL-6 and TNF-alpha synergistically inhibit allograft acceptance. J Am Soc Nephrol 2009;20:1032-40.
27. Bromley SK, Thomas SY, Luster AD. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat Immunol 2005;6:895-901. (Pubitemid 43090444)
28. Colvin BL, Wang Z, Nakano H, et al. CXCL9 antagonism further extends prolonged cardiac allograft survival in CCL19/CCL21-deficient mice. Am J Transplant 2005;5:2104-13. (Pubitemid 41648457)
29. Ensminger SM, Helm SN, Ohl L, et al. Increased transplant arteriosclerosis in the absence of CCR7 is associated with reduced expression of Foxp3. Transplantation 2008;86:590-600.
30. Nykänen AI, Sandelin H, Krebs R, et al. Targeting lymphatic vessel activation and CCL21 production by vascular endothelial growth factor receptor-3 inhibition has novel immunomodulatory and antiarteriosclerotic effects in cardiac allografts. Circulation 2010;121: 1413-22.
31. Chen L, Hamrah P, Cursiefen C, et al. Vascular endothelial growth factor receptor-3 mediates induction of corneal alloimmunity. Nat Med 2004;10:813-5. (Pubitemid 39070853)
32. Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 2003;3:199-210. (Pubitemid 37323205)
33. Xu L, Kitani A, Fuss I, Strober W. Cutting edge: regulatory T cells induce CD4-CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol 2007; 178:6725-9.
34. Muthukumar T, Dadhania D, Ding R, et al. Messenger RNA for FOXP3 in the urine of renal-allograft recipients. N Engl J Med 2005; 353:2342-51. (Pubitemid 41713746)
35. Dijke IE, Velthuis JH, Caliskan K, et al. Intragraft FOXP3 mRNA expression reflects antidonor immune reactivity in cardiac allograft patients. Transplantation 2007;83:1477-84. (Pubitemid 46934071)
36. Chen L, Ahmed E, Wang T, et al. TLR signals promote IL-6/IL-17- dependent transplant rejection. J Immunol 2009;182:6217-25.
37. Ayyoub M, Deknuydt F, Raimbaud I, et al. Human memory FOXP3- Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage-specific transcription factor RORgamma t. Proc Natl Acad Sci U S A 2009;106:8635-40.
38. Das J, Ren G, Zhang L, et al. Transforming growth factor beta is dispensable for the molecular orchestration of Th17 cell differentiation. J Exp Med 2009;206:2407-16.
39. Erratum in: J Exp Med 200921; 206:3157.
40. Park H, Li Z, Yang XO, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005;6:1133-41. (Pubitemid 41541791)
41. Zheng X, Lian D, Wong A, et al. Novel small interfering RNAcontaining solution protecting donor organs in heart transplantation. Circulation 2009;120:1099-107, 1 p following 107.
42. Basuroy S, Bhattacharya S, Leffler CW, Parfenova H. Nox4 NADPH oxidase mediates oxidative stress and apoptosis caused by TNF-alpha in cerebral vascular endothelial cells. Am J Physiol Cell Physiol 2009;296:C422-32.