Effects of complement activation on allograft injury

Current Opinion in Organ Transplantation

Volumn 20, Issue 4, 2015, Pages 468-475

  Sheen, Joong Hyuk ^a   Heeger, Peter S ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Antibody mediated rejection; complement; ischemia reperfusion; T cells

Indexed keywords

ALLOANTIBODY; COMPLEMENT;

ALLOGRAFT; ALLOIMMUNITY; ANTIBODY MEDIATED REJECTION; CELL EXPANSION; COMPLEMENT ACTIVATION; GRAFT REJECTION; GRAFT SURVIVAL; HUMAN; NONHUMAN; REPERFUSION; REPERFUSION INJURY; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ALLOTRANSPLANTATION; ANIMAL; IMMUNOLOGY;

ALLOGRAFTS; ANIMALS; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; GRAFT REJECTION; GRAFT SURVIVAL; HUMANS; TRANSPLANTATION, HOMOLOGOUS;

EID: 84941343964     PISSN: 10872418     EISSN: 15317013     Source Type: Journal    
DOI: 10.1097/MOT.0000000000000216     Document Type: Review

References (86)

1. Patel R, Terasaki PI. Significance of the positive crossmatch test in kidney transplantation. N Engl J Med 1969; 280:735-739.
2. Baldwin WM 3rd, Valujskikh A, Fairchild RL. Antibody-mediated rejection: emergence of animal models to answer clinical questions. Am J Transplant 2010; 10:1135-1142.
3. Walport MJ. Complement. First of two parts. N Engl J Med 2001; 344:1058-1066.
4. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010; 11:785-797.
5. Peake PW, O'Grady S, Pussell BA, Charlesworth JA. C3a is made by proximal tubular HK-2 cells and activates them via the C3a receptor. Kidney Int 1999; 56:1729-1736.
6. Lalli PN, Strainic MG, Yang M, et al. Locally produced C5a binds to T cellexpressed C5aR to enhance effector T-cell expansion by limiting antigeninduced apoptosis. Blood 2008; 112:1759-1766.
7. Siedlecki A, Irish W, Brennan DC. Delayed graft function in the kidney transplant. Am J Transplant 2011; 11:2279-2296.
8. Park P, Haas M, Cunningham PN, et al. Inhibiting the complement system does not reduce injury in renal ischemia reperfusion. J Am Soc Nephrol 2001; 12:1383-1390.
9. Zhou W, Farrar CA, Abe K, et al. Predominant role for C5b-9 in renal ischemia/reperfusion injury. J Clin Invest 2000; 105:1363-1371.
10. Thurman JM, Ljubanovic D, Edelstein CL, et al. Lack of a functional alternative complement pathway ameliorates ischemic acute renal failure in mice. J Immunol 2003; 170:1517-1523.
11. De Vries B, Matthijsen RA, Wolfs TG, et al. Inhibition of complement factor C5 protects against renal ischemia-reperfusion injury: inhibition of late apoptosis and inflammation. Transplantation 2003; 75:375-382.
12. Farrar CA, Zhou W, Lin T, Sacks SH. Local extravascular pool of C3 is a determinant of postischemic acute renal failure. FASEB J 2006; 20:217-226.
13. Atkinson C, Floerchinger B, Qiao F, et al. Donor brain death exacerbates complement-dependent ischemia/reperfusion injury in transplanted hearts. Circulation 2013; 127:1290-1299.
14. Peng Q, Li K, Smyth LA, et al. C3a and C5a promote renal ischemiareperfusion injury. J Am Soc Nephrol 2012; 23:1474-1485.
15. Thurman JM. Triggers of inflammation after renal ischemia/reperfusion. Clin Immunol 2007; 123:7-13.
16. Fuquay R, Renner B, Kulik L, et al. Renal ischemia-reperfusion injury amplifies the humoral immune response. J Am Soc Nephrol 2013; 24:1063-1072.
17. Raedler H, Vieyra MB, Leisman S, et al. Anticomplement component C5 mAb synergizes with CTLA4Ig to inhibit alloreactive T cells and prolong cardiac allograft survival in mice. Am J Transplant 2011; 11:1397-1406.
18. Raedler H, Yang M, Lalli PN, et al. Primed CD8(\+) T-cell responses to allogeneic endothelial cells are controlled by local complement activation. Am J Transplant 2009; 9:1784-1795.
19. Asgari E, Farrar CA, Lynch N, et al. Mannan-binding lectin-associated serine protease 2 is critical for the development of renal ischemia reperfusion injury and mediates tissue injury in the absence of complement C4. FASEB J 2014; 9:3996-4003.
20. Zhang M, Carroll MC. Natural IgM-mediated innate autoimmunity: a new target for early intervention of ischemia-reperfusion injury. Expert Opin Biol Ther 2007; 7:1575-1582.
21. Haas MS, Alicot EM, Schuerpf F, et al. Blockade of self-reactive IgM significantly reduces injury in a murine model of acute myocardial infarction. Cardiovasc Res 2010; 87:618-627.
22. Saidi RF, Rajeshkumar B, Shariftabrizi A, et al. Human C1 inhibitor attenuates liver ischemia-reperfusion injury and promotes liver regeneration. J Surg Res 2014; 187:660-666.
23. Tillou X, Poirier N, Le Bas-Bernardet S, et al. Recombinant human C1-inhibitor prevents acute antibody-mediated rejection in alloimmunized baboons. Kidney Int 2010; 78:152-159.
24. Sommer W, Tudorache I, Kuhn C, et al. C1-esterase-inhibitor for primary graft dysfunction in lung transplantation. Transplantation 2014; 97:1185-1191.
25. Sacks SH, Zhou W. The role of complement in the early immune response to transplantation. Nat Rev Immunol 2012; 12:431-442.
26. Patel H, Smith RA, Sacks SH, Zhou W. Therapeutic strategy with a membranelocalizing complement regulator to increase the number of usable donor organs after prolonged cold storage. J Am Soc Nephrol 2006; 17:1102-1111.
27. Pratt JR, Basheer SA, Sacks SH. Local synthesis of complement component C3 regulates acute renal transplant rejection. Nat Med 2002; 8:582-587.
28. Heeger PS, Lalli PN, Lin F, et al. Decay-accelerating factor modulates induction of T cell immunity. J Exp Med 2005; 201:1523-1530.
29. Strainic MG, Liu J, Huang D, et al. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4\+T cells. Immunity 2008; 28:425-435.
30. Nataf S, Davoust N, Ames RS, Barnum SR. Human T cells express the C5a receptor and are chemoattracted to C5a. J Immunol 1999; 162:4018-4023.
31. Pavlov V, Raedler H, Yuan S, et al. Donor deficiency of decay-accelerating factor accelerates murine T cell-mediated cardiac allograft rejection. J Immunol 2008; 181:4580-4589.
32. Medof ME, Kinoshita T, Nussenzweig V. Inhibition of complement activation on the surface of cells after incorporation of decay-accelerating factor (DAF) into their membranes. J Exp Med 1984; 160:1558-1578.
33. Kwan WH, Hashimoto D, Paz-Artal E, et al. Antigen-presenting cell-derived complement modulates graft-versus-host disease. J Clin Invest 2012; 122:2234-2238.
34. Gueler F, Rong S, Gwinner W, et al. Complement 5a receptor inhibition improves renal allograft survival. J Am Soc Nephrol 2008; 19:2302-2312.
35. Cravedi P, Leventhal J, Lakhani P, et al. Immune cell-derived C3a and C5a costimulate human T cell alloimmunity. Am J Transplant 2013; 13:2530-2539.
36. Li K, Fazekasova H, Wang N, et al. Expression of complement components, receptors and regulators by human dendritic cells. Mol Immunol 2011; 48 (9-10):1121-1127.
37. Ghannam A, Fauquert JL, Thomas C, et al. Human complement C3 deficiency: Th1 induction requires T cell-derived complement C3a and CD46 activation. Mol Immunol 2014; 58:98-107.
38. Ma Q, Li D, Carreno R, et al. Complement component C3 mediates Th1/Th17 polarization in human T-cell activation and cutaneous GVHD. Bone Marrow Transplant 2014; 49:972-976.
39. Liszewski MK, Kolev M, Le Friec G, et al. Intracellular complement activation sustains T cell homeostasis and mediates effector differentiation. Immunity 2013; 39:1143-1157.
40. Asgari E, Le Friec G, Yamamoto H, et al. C3a modulates IL-1beta secretion in human monocytes by regulating ATP efflux and subsequent NLRP3 inflammasome activation. Blood 2013; 122:3473-3481.
41. Roncarolo MG, Battaglia M. Regulatory T-cell immunotherapy for tolerance to self antigens and alloantigens in humans. Nat Rev Immunol 2007; 7:585-598.
42. Strainic MG, Shevach EM, An F, et al. Absence of signaling into CD4(\+) cells via C3aR and C5aR enables autoinductive TGF-beta1 signaling and induction of Foxp3(\+) regulatory T cells. Nat Immunol 2013; 14:162-171.
43. van der Touw W, Cravedi P, Kwan WH, et al. Cutting edge: receptors for C3a and C5a modulate stability of alloantigen-reactive induced regulatory T cells. J Immunol 2013; 190:5921-5925.
44. Kwan WH, van der Touw W, Paz-Artal E, et al. Signaling through C5a receptor and C3a receptor diminishes function of murine natural regulatory T cells. J Exp Med 2013; 210:257-268.
45. Cardone J, Le Friec G, Vantourout P, et al. Complement regulator CD46 temporally regulates cytokine production by conventional and unconventional T cells. Nat Immunol 2010; 11:862-871.
46. Pepys MB. Role of complement in induction of antibody production in vivo. Effect of cobra factor and other C3-reactive agents on thymus-dependent and thymus-independent antibody responses. J Exp Med 1974; 140:126-145.
47. Fang Y, Xu C, Fu YX, et al. Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigenspecific IgG response. J Immunol 1998; 160:5273-5279.
48. Dempsey PW, Allison ME, Akkaraju S, et al. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 1996; 271:348-350.
49. Marsh JE, Farmer CK, Jurcevic S, et al. The allogeneic T and B cell response is strongly dependent on complement components C3 and C4. Transplantation 2001; 72:1310-1318.
50. Tangye SG, Ma CS, Brink R, Deenick EK. The good, the bad and the ugly: TFH cells in human health and disease. Nat Rev Immunol 2013; 13:412-426.
51. Wang H, Arp J, Liu W, et al. Inhibition of terminal complement components in presensitized transplant recipients prevents antibody-mediated rejection leading to long-term graft survival and accommodation. J Immunol 2007; 179:4451-4463.
52. Valenzuela NM, McNamara JT, Reed EF. Antibody-mediated graft injury: complement-dependent and complement-independent mechanisms. Curr Opin Organ Transplant 2014; 19:33-40.
53. Stegall MD, Chedid MF, Cornell LD. The role of complement in antibodymediated rejection in kidney transplantation. Nat Rev Nephrol 2012; 8:670-678.
54. Akiyoshi T, Hirohashi T, Alessandrini A, et al. Role of complement and NK cells in antibody mediated rejection. Hum Immunol 2012; 73:1226-1232.
55. Jane-Wit D, Manes TD, Yi T, et al. Alloantibody and complement promote T cell-mediated cardiac allograft vasculopathy through noncanonical nuclear factor-kappaB signaling in endothelial cells. Circulation 2013; 128:2504-2516.
56. Stegall MD, Diwan T, Raghavaiah S, et al. Terminal complement inhibition decreases antibody-mediated rejection in sensitized renal transplant recipients. Am J Transplant 2011; 11:2405-2413.
57. Locke JE, Magro CM, Singer AL, et al. The use of antibody to complement protein C5 for salvage treatment of severe antibody-mediated rejection. Am J Transplant 2009; 9:231-235.
58. Burbach M, Suberbielle C, Brocheriou I, et al. Report of the inefficacy of eculizumab in two cases of severe antibody-mediated rejection of renal grafts. Transplantation 2014; 98:1056-1059.
59. Mauriello CT, Pallera HK, Sharp JA, et al. A novel peptide inhibitor of classical and lectin complement activation including ABO incompatibility. Mol Immunol 2013; 53 (1-2):132-139.
60. Sharp JA, Whitley PH, Cunnion KM, Krishna NK. Peptide inhibitor of complement c1, a novel suppressor of classical pathway activation: mechanistic studies and clinical potential. Front Immunol 2014; 5:406.
61. Freitas MC, Rebellato LM, Ozawa M, et al. The role of immunoglobulin-G subclasses and C1q in de novo HLA-DQ donor-specific antibody kidney transplantation outcomes. Transplantation 2013; 95:1113-1119.
62. Crespo M, Torio A, Mas V, et al. Clinical relevance of pretransplant anti-HLA donor-specific antibodies: Does C1q-fixation matter Transpl Immunol 2013; 29:28-33.
63. Picascia A, Infante T, Napoli C. Luminex and antibody detection in kidney transplantation. Clin Exp Nephrol 2012; 16:373-381.
64. Loupy A, Lefaucheur C, Vernerey D, et al. Complement-binding anti-HLA antibodies and kidney-allograft survival. N Engl J Med 2013; 369:1215-1226.
65. Zeevi A, Lunz J, Feingold B, et al. Persistent strong anti-HLA antibody at high titer is complement binding and associated with increased risk of antibodymediated rejection in heart transplant recipients. J Heart Lung Transplant 2013; 32:98-105.
66. Witt CA, Gaut JP, Yusen RD, et al. Acute antibody-mediated rejection after lung transplantation. J Heart Lung Transplant 2013; 32:1034-1040.
67. Crespo M, Torio A, Mas V, et al. Clinical relevance of pretransplant anti-HLA donor-specific antibodies: does C1q-fixation matter Transpl Immunol 2013; 29 (1-4):28-33.
68. Peacock S, Kosmoliaptsis V, Bradley AJ, Taylor CJ. Questioning the added value of Luminex single antigen beads to detect C1q binding donor HLAspecific antibodies. Transplantation 2014; 98:384-386.
69. Nankivell BJ, Kuypers DR. Diagnosis and prevention of chronic kidney allograft loss. Lancet 2011; 378:1428-1437.
70. Kaneku HK, Terasaki PI. Thirty year trend in kidney transplants: UCLA and UNOS Renal Transplant Registry. Clin Transpl 2006; 1-27.
71. Cravedi P, Perico N, Remuzzi G. Nonimmune interventions to protect kidney allografts in the long term. Kidney Int Suppl 2010; 119:S71-S75.
72. Sheerin NS, Risley P, Abe K, et al. Synthesis of complement protein C3 in the kidney is an important mediator of local tissue injury. FASEB J 2008; 22:1065-1072.
73. Tang Z, Lu B, Hatch E, et al. C3a mediates epithelial-to-mesenchymal transition in proteinuric nephropathy. J Am Soc Nephrol 2009; 20:593-603.
74. Zhou X, Fukuda N, Matsuda H, et al. Complement 3 activates the renal reninangiotensin system by induction of epithelial-to-mesenchymal transition of the nephrotubulus in mice. Am J Physiol Renal Physiol 2013; 305:F957-F967.
75. Renner B, Klawitter J, Goldberg R, et al. Cyclosporine induces endothelial cell release of complement-activating microparticles. J Am Soc Nephrol 2013; 24:1849-1862.
76. Curci C, Castellano G, Stasi A, et al. Endothelial-to-mesenchymal transition and renal fibrosis in ischaemia/reperfusion injury are mediated by complement anaphylatoxins and Akt pathway. Nephrol Dial Transplant 2014; 29:799-808.
77. Suzuki H, Lasbury ME, Fan L, et al. Role of complement activation in obliterative bronchiolitis postlung transplantation. J Immunol 2013; 191:4431-4439.
78. Khan MA, Maasch C, Vater A, et al. Targeting complement component 5a promotes vascular integrity and limits airway remodeling. Proc Natl Acad Sci USA 2013; 110:6061-6066.
79. Khan MA, Nicolls MR. Complement-mediated microvascular injury leads to chronic rejection. Adv Exp Med Biol 2013; 735:233-246.
80. Jeong JC, Hwang YH, Kim H, et al. Association of complement 5 genetic polymorphism with renal allograft outcomes in Korea. Nephrol Dial Transplant 2011; 26:3378-3385.
81. Brown KM, Kondeatis E, Vaughan RW, et al. Influence of donor C3 allotype on late renal-transplantation outcome. N Engl J Med 2006; 354:2014-2023.
82. Varagunam M, Yaqoob MM, Dohler B, Opelz G. C3 polymorphisms and allograft outcome in renal transplantation. N Engl J Med 2009; 360:874-880.
83. Bay JT, Schejbel L, Madsen HO, et al. Low C4 gene copy numbers are associated with superior graft survival in patients transplanted with a deceased donor kidney. Kidney Int 2013; 84:562-569.
84. Nakorchevsky A, Hewel JA, Kurian SM, et al. Molecular mechanisms of chronic kidney transplant rejection via large-scale proteogenomic analysis of tissue biopsies. J Am Soc Nephrol 2010; 21:362-373.
85. Banz Y, Rieben R. Role of complement and perspectives for intervention in ischemia-reperfusion damage. Ann Med 2012; 44:205-217.
86. Chen G, Chen S, Chen X. Role of complement and perspectives for intervention in transplantation. Immunobiology 2013; 218:817-827.