Inflammatory triggers of acute rejection of organ allografts

Immunological Reviews

Volumn 258, Issue 1, 2014, Pages 132-144

  Mori, Daniel N ^a   Kreisel, Daniel ^b   Fullerton, James N ^c   Gilroy, Derek W ^c   Goldstein, Daniel R ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Inflammation; Organ transplantation; Resolution

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIGEN; CYTOKINE; DNA; F PEPTIDE; HAPTOGLOBIN; HEAT SHOCK PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; HYALURONIC ACID; PEPTIDE; UNCLASSIFIED DRUG; URIC ACID; AUTACOID;

ACUTE GRAFT REJECTION; HUMAN; INFECTION; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; ORGAN INJURY; ORGAN TRANSPLANTATION; PERIOPERATIVE PERIOD; PRIORITY JOURNAL; REVIEW; ADVERSE EFFECTS; ALLOGRAFT; ANIMAL; GRAFT REJECTION; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

ALLOGRAFTS; ANIMALS; GRAFT REJECTION; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INFLAMMATION MEDIATORS; ORGAN TRANSPLANTATION; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

EID: 84893557923     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12146     Document Type: Review

References (115)

1. Floerchinger B, Oberhuber R, Tullius SG. Effects of brain death on organ quality and transplant outcome. Transplant Rev 2012;26:54-59.
2. Terasaki PI, Cecka JM, Gjertson DW, Takemoto S. High survival rates of kidney transplants from spousal and living unrelated donors. N Engl J Med 1995;333:333-336.
3. Zweers N, et al. Donor brain death aggravates chronic rejection after lung transplantation in rats. Transplantation 2004;78:1251-1258.
4. Zhang SJ, Wang T. The influence of brain death on donor liver and the potential mechanisms of protective intervention. Front Med 2011;5:8-14.
5. Danobeitia JS, et al. Early activation of the inflammatory response in the liver of brain-dead non-human primates. J Surg Res 2012;176:639-648.
6. Koudstaal LG, et al. Brain death induces inflammation in the donor intestine. Transplantation 2008;86:148-154.
7. Floerchinger B, et al. Inflammatory immune responses in a reproducible mouse brain death model. Transpl Immunol 2012;27:25-29.
8. de Vries DK, Lindeman JHN, Ringers J, Reinders MEJ, Rabelink TJ, Schaapherder AFM. Donor brain death predisposes human kidney grafts to a proinflammatory reaction after transplantation. Am J Transplant 2011;11:1064-1070.
9. Atkinson C, Varela JC, Tomlinson S. Complement-dependent inflammation and injury in a murine model of brain dead donor hearts. Circ Res 2009;105:1094-1101.
10. Atkinson C, et al. Donor brain death exacerbates complement-dependent ischemia/reperfusion injury in transplanted hearts. Circulation 2013;127:1290-1299.
11. Damman J, et al. Targeting complement activation in brain-dead donors improves renal function after transplantation. Transpl Immunol 2011;24:233-237.
12. van der Vliet JA, Warlé MC. The need to reduce cold ischemia time in kidney transplantation. Curr Opin Organ Transplant 2013;18:174-178.
13. Goto R, Issa F, Heidt S, Taggart D, Wood KJ. Ischemia-reperfusion injury accelerates human antibody-mediated transplant vasculopathy. Transplantation 2013;96:139-145.
14. Yi T, et al. Reperfusion injury intensifies the adaptive human T cell alloresponse in a human-mouse chimeric artery model. Arterioscler Thromb Vasc Biol 2012;32:353-360.
15. Sanchez PG, D'Ovidio F. Ex-vivo lung perfusion. Curr Opin Organ Transplant 2012;17:490-495.
16. Eltzschig HK, Eckle T. Ischemia and reperfusion-from mechanism to translation. Nat Med 2011;17:1391-1401.
17. Rock KL, Hearn A, Chen CJ, Shi Y. Natural endogenous adjuvants. Springer Semin Immunopathol 2005;26:231-246.
18. Rock KL, Latz E, Ontiveros F, Kono H. The sterile inflammatory response. Annu Rev Immunol 2010;28:321-342.
19. Shen H, Kreisel D, Goldstein DR. Processes of sterile inflammation. J Immunol 2013;191:2857-2863.
20. Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science 2010;327:291-295.
21. Rabadi MM, Ghaly T, Goligorksy MS, Ratliff BB. HMGB1 in renal ischemic injury. Am J Physiol Renal Pyhysiol 2012;303:F873-F885.
22. Zhu H, Li J, Wang S, Liu K, Wang L, Huang L. Hmgb1-TLR4-IL-23-IL-17A axis promote ischemia-reperfusion injury in a cardiac transplantation model. Transplantation 2013;5:1448-1454.
23. Kamo N, et al. ASC/caspase-1/IL-1β signaling triggers inflammatory responses by promoting HMGB1 induction in liver ischemia/reperfusion injury. Hepatology 2013;58:351-362.
24. Itoh T, et al. Elevation of high-mobility group box 1 after clinical autologous islet transplantation and its inverse correlation with outcomes. Cell Transplant 2012 [Epub ahead of print]
25. Matsuoka N, et al. High-mobility group box 1 is involved in the initial events of early loss of transplanted islets in mice. J Clin Invest 2010;120:735-743.
26. Wu H, et al. HMGB1 contributes to kidney ischemia reperfusion injury. J Am Soc Nephro 2010;21:1878-1890.
27. Li J, et al. Neutralization of the extracellular HMGB1 released by ischaemic damaged renal cells protects against renal ischaemia-reperfusion injury. Nephrol Dial Transplant 2011;26:469-478.
28. Tsung A, et al. HMGB1 release induced by liver ischemia involves Toll-like receptor 4-dependent reactive oxygen species production and calcium-mediated signaling. J Exp Med 2007;204:2913-2923.
29. Zhai Y, et al. Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3-dependent MyD88-independent pathway. J Immunol 2004;173:7115-7119.
30. Sharma AK, Lapar DJ, Stone ML, Zhao Y, Kron IL, Laubach VE. Receptor for advanced glycation end products (RAGE) on iNKT cells mediates lung ischemia-reperfusion injury. Am J Transplant 2013;13:2255-2267.
31. Zeng S, et al. Receptor for advanced glycation end product (RAGE)-dependent modulation of early growth response-1 in hepatic ischemia/reperfusion injury. J Hepatol 2009;50:929-936.
32. Moser B, et al. Blockade of RAGE suppresses alloimmune reactions in vitro and delays allograft rejection in murine heart transplantation. Am J Transplant 2007;7:293-302.
33. Huang Y, et al. Extracellular Hmgb1 functions as an innate immune-mediator implicated in murine cardiac allograft acute rejection. Am J Transplant 2007;7:799-808.
34. Krüger B, et al. Donor Toll-like receptor 4 contributes to ischemia and reperfusion injury following human kidney transplantation. Proc Natl Acad Sci USA 2009;106:3390-3395.
35. Palmer SM, et al. The role of innate immunity in acute allograft rejection after lung transplantation. Am J Respir Crit Care Med 2003;168:628-632.
36. Palmer SM, et al. Role of TLR4 in acute pulmonary allograft rejection. Am J Respir Crit Care Med 2004;169:A269.
37. 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.
38. Lubbers NL, et al. Oral bimoclomol elevates heat shock protein 70 and reduces myocardial infarct size in rats. Eur J Pharmacol 2002;435:79-83.
39. Trieb K, et al. Heat shock protein expression in the transplanted human kidney. Transpl Int 2001;14:281-286.
40. Oh K-H, et al. Targeted gene disruption of the heat shock protein 72 gene (hsp70.1) in the donor tissue is associated with a prolonged rejection-free survival in the murine skin allograft model. Transpl Immunol 2004;13:273-281.
41. Tesar B, Goldstein DR. Acute allograft rejections occurs independently of inducible HSP-70. Transplantation 2007;11:1513-1517.
42. 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;111:1571-1578.
43. Kovalchin JT, Mendonca C, Wagh MS, Wang R, Chandawarkar RY. In vivo treatment of mice with heat shock protein, gp96, improves survival of skin grafts with minor and major antigenic disparity. Transpl Immunol 2006;15:179-185.
44. O' Neill S, Ross JA, WIgmore SJ, Harrison EM. The role of heat shock protein 90 in modulating ischemia-reperfusion injury in the kidney. Expert Opin Investig Drugs 2012;21:1535-1548.
45. Wells A, Larsson E, Hanas E, Laurent T, Hallgren R, Tufveson G. Increased hyaluronan in acutely rejecting human kidney grafts. Transplantation 1993;55:1346-1349.
46. Tesar BM, Jiang D, Liang J, Palmer SM, Noble PW, Goldstein DR. The role of hyaluronan degradation products as innate alloimmune agonists. Am J Transplant 2006;6:2622-2635.
47. Termeer CC, et al. Oligosaccharides of hyaluronan are potent activators of dendritic cells. J Immunol 2000;165:1863-1870.
48. Termeer C, et al. Oligosaccharides of hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med 2002;195:99-111.
49. Jiang D, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 2005;11:1173-1179.
50. Bollyky PL, et al. Cutting edge: high molecular weight hyaluronan promotes the suppressive effects of CD4 + CD25 + regulatory T cells. J Immunol 2007;179:744-747.
51. Knoflach A, et al. Immunomodulatory functions of low-molecular weight hyaluronate in an acute rat renal allograft rejection model. J Am Soc Nephrol 1999;10:1059-1066.
52. Knoflach A, et al. Immunomodulatory functions of hyaluronate in the LEW-to-F344 model of chronic cardiac allograft rejection. Transplantation 1999;67:909-914.
53. Zhang Q, et al. Circulating mitochondrial DAMPs cause inflammatory responses to injur. Nature 2010;464:104-107.
54. Zucchini N, et al. Cutting edge: overlapping functions of TLR7 and TLR9 for innate defense against a herpesvirus infection. J Immunol 2008;180:5799-5803.
55. Iyer SS, et al. Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci USA 2009;106:20388-20393.
56. Shi Y, Evans J, Rock K. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003;425:516-521.
57. Chen C-J, Kono H, Golenbock D, Reed G, Akira S, Rock KL. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med 2007;13:851-856.
58. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006;440:237-241.
59. Haririan A, et al. Association of serum uric acid with graft survival after kidney transplantation: a time-varying analysis. Am J Transplant 2011;11:1943-1950.
60. Seto T, et al. Upregulation of the apoptosis-related inflammasome in cardiac allograft rejection. J Heart Lung Transplant 2010;29:352-359.
61. Cantu E, et al. Gene set enrichment analysis identifies key innate immune pathways in primary graft dysfunction after lung transplantation. Am J Transplant 2013;13:1898-1904.
62. Shen H, et al. Haptoglobin activates innate immunity to enhance acute transplant rejection in mice. J Clin Invest 2012;122:383-387.
63. Wang Y, Kinzie E, Berger FG, Lim SK, Baumann H. Haptoglobin, an inflammation-inducible plasma protein. Redox Rep 2001;6:379-385.
64. Quaye IK. Haptoglobin, inflammation and disease. Trans R Soc Trop Med Hyg 2008;102:735-742.
65. Li P, et al. Localization of haptoglobin in normal human skin and some skin diseases. Int J Dermatol 2005;44:280-284.
66. Zager RA, Vijayan A, Johnson ACM. Proximal tubule haptoglobin gene activation is an integral component of the acute kidney injury "stress response". Am J Physiol Renal Pyhysiol 2012;303:F139-F148.
67. Arredouani MS, Kasran A, Vanoirbeek JA, Berger FG, Baumann H, Ceuppens JL. Haptoglobin dampens endotoxin-induced inflammatory effects both in vitro and in vivo. Immunology 2005;114:263-271.
68. Rossbacher L, Wagner L, Pasternack MS. Inhibitory effect of haptoglobin on granulocyte chemotaxis, phagocytosis and bactericidal activity. Scand J Immunol 1999;50:399-404.
69. Galicia G, et al. Haptoglobin deficiency facilitates the development of autoimmune inflammation. Eur J Immunol 2009;39:3404-3412.
70. Maffei M, et al. The obesity and inflammatory marker haptoglobin attracts monocytes via interaction with chemokine (C-C motif) receptor 2 (CCR2). BMC Biol 2009;7:87.
71. Huntoon KM, et al. The acute phase protein haptoglobin regulates host immunity. J Leukoc Biol 2008;84:170-181.
72. Chapelle J-P, Albert A, Smeets J-P, Heusghem C, Kulbertus HE. Effect of the haptoglobin phenotype on the size of a myocardial infarct. N Engl J Med 1982;307:457-463.
73. Suleiman M, et al. Haptoglobin type and 30-day mortality in diabetic individuals presenting with acute myocardial infarction. Diabetes Care 2003;26:2699-2700.
74. Cole JE, Mitra AT, Monaco C. Treating atherosclerosis: the potential of toll-like receptors as therapeutic targets. Expert Rev Cardiovasc Ther 2010;8:1619-1635.
75. Levy A, et al. Haptoglobin phenotype and vascular complications in patients with diabetes. N Engl J Med 2000;343:969-970.
76. Avalos AM, Busconi L, Marshak-Rothstein A. Regulation of autoreactive B cell responses to endogenous TLR ligands. Autoimmunity 2010;43:76-83.
77. McGuirk J, et al. Serum proteomic profiling and haptoglobin polymorphisms in patients with GVHD after allogeneic hematopoietic cell transplantation. J Hematol Oncol 2009;2:17.
78. Asleh R, Levy A. In vivo and in vitro studies establishing haptoglobin as a major susceptibility gene for diabetic vascular disease. Vasc Health Risk Manag 2005;1:19-28.
79. Wu H, et al. TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 2007;117:2847-2859.
80. Speeckaert R, et al. Donor haptoglobin phenotype determines outcome following liver transplantation. Transpl Int 2011;24:619-626.
81. Cameron GD, Julie W, Ann C, Nizar Y, Nicholas HB, Brian K. Haptoglobin phenotype correlates with development of cardiac transplant vasculopathy. J Heart Lung Transplant 2004;23:43-49.
82. Eigenbrod T, Park J-H, Harder J, Iwakura Y, Núñez G. Cutting edge: critical role for mesothelial cells in necrosis-induced inflammation through the recognition of IL-1α released from dying cells. J Immunol 2008;181:8194-8198.
83. Chen C-J, et al. MyD88-dependent IL-1 receptor signaling is essential for gouty inflammation stimulated by monosodium urate crystals. J Clin Invest 2006;116:2262-2271.
84. Rao DA, et al. Interleukin (IL)-1 promotes allogeneic T cell intimal infiltration and IL-17 production in a model of human artery rejection. J Exp Med 2008;205:3145-3158.
85. Ishii D, Schenk AD, Baba S, Fairchild RL. Role of TNFα in early chemokine production and leukocyte infiltration into heart allografts. Am J Transplant 2010;10:59-68.
86. Shen H, Goldstein DR. IL-6 and TNF-α synergistically inhibit allograft acceptance. J Am Soc Nephrol 2009;20:1032-1040.
87. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006;124:783.
88. Dostert C, Pétrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008;320:674-677.
89. Gasse P, et al. Uric acid is a danger signal activating NALP3 inflammasome in lung injury inflammation and fibrosis. Am J Resp Crit Care Med 2009;179:903-913.
90. Allen IC, et al. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 2009;30:556-565.
91. Tobin JOH, Warrell MJ, Morris PJ. Cytomegalovirus infection and renal transplantation. Lancet 1979;313:926.
92. Steinmuller D. The enigma of skin allograft rejection. Transplant Rev 1998;12:8-9.
93. Smith C, Pilgrim H, Steinmuller D. The survival of skin allografts and xenografts in germ-free mice. Transplantation 1972;13:38-41.
94. Chong A, Alegre M. The impact of infection and tissue damage in solid-organ transplantation. Nat Rev Immunol 2012;12:459-471.
95. Adams AB, et al. Heterologous immunity provides a potent barrier to transplantation tolerance. J Clin Invest 2003;111:1887-1895.
96. Wang T, et al. Prevention of allograft tolerance by bacterial infection with Listeria monocytogenes. J Immunol 2008;180:5991-5999.
97. Wang T, et al. Infection with the intracellular bacterium, Listeria monocytogenes overrides established tolerance in a mouse cardiac allograft model. Am J Transplant 2010;10:1524-1533.
98. Ahmed EB, Wang T, Daniels M, Alegre ML, Chong AS. IL-6 induced by Staphylococcus aureus infection prevents the induction of skin allograft acceptance in mice. Am J Transplant 2011;11:936-946.
99. Noris M, et al. The toll-IL-1R member Tir8/SIGIRR negatively regulates adaptive immunity against kidney grafts. J Immunol 2009;183:4249-4260.
100. Kobayashi K, Hernandez LD, Galan JE, Janeway CA, Jr., Medzhitov R, Flavell RA. IRAK-M is a negative regulator of toll-like receptor signaling. Cell 2002;110:191-202.
101. Deng JC, et al. Sepsis-induced suppression of lung innate immunity is mediated by IRAK-M. J Clin Invest 2006;116:2532-2542.
102. Li W, et al. Intravital 2-photon imaging of leukocyte trafficking in beating heart. J Clin Invest 2012;122:2499-2508.
103. Lammermann T, et al. Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 2013;498:371-375.
104. Mócsai A. Diverse novel functions of neutrophils in immunity, inflammation, and beyond. J Exp Med 2013;210:1283-1299.
105. Holmes GR, et al. Repelled from the wound, or randomly dispersed? Reverse migration behaviour of neutrophils characterized by dynamic modelling. J R Soc Interface 2012;9:3229-3239.
106. Thorp E, Subramanian M, Tabas I. The role of macrophages and dendritic cells in the clearance of apoptotic cells in advanced atherosclerosis. Eur J Immunol 2011;41:2515-2518.
107. Stables MJ, et al. Transcriptomic analyses of murine resolution-phase macrophages. Blood 2011;118:e192-e208.
108. Serhan CN, Chiang N, Van Dyke T. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 2008;8:349-361.
109. MacKenzie KF, et al. PGE(2) induces macrophage IL-10 production and a regulatory-like phenotype via a protein kinase A-SIK-CRTC3 pathway. J Immunol 2013;190:565-577.
110. Ogawa M, Suzuki J-I, Kosuge H, Takayama K, Nagai R, Isobe M. The mechanism of anti-inflammatory effects of prostaglandin E2 receptor 4 activation in murine cardiac transplantation. Transplantation 2009;87:1645-1653.
111. Domingo-Gonzalez R, Katz S, Serezani CH, Moore TA, Levine AM, Moore BB. Prostaglandin E2-induced changes in alveolar macrophage scavenger receptor profiles differentially alter phagocytosis of Pseudomonas aeruginosa and Staphylococcus aureus post-bone marrow transplant. J Immunol 2013;190:5809-5817.
112. Stables MJ, Gilroy DW. Old and new generation lipid mediators in acute inflammation and resolution. Prog Lipid Res 2011;50:35-51.
113. Serhan CN. Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am J Pathol 2010;177:1576-1591.
114. Levy BD, et al. The endogenous pro-resolving mediators lipoxin A4 and resolvin E1 preserve organ function in allograft rejection. Prostaglandins Leukot Essent Fatty Acids 2011;84:43-50.
115. Fullerton JN, O'Brien AJ, Gilroy DW. Pathways mediating resolution of inflammation: when enough is too much. J Pathol 2013;231:8-20.