Complement regulation of T-cell alloimmunity

Seminars in Nephrology

Volumn 33, Issue 6, 2013, Pages 565-574

  Cravedi, Paolo ^a   Van der Touw, William ^a   Heeger, Peter S ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Allograft rejection; Complement; Costimulation; T cells; Transplantation

Indexed keywords

CCX 168; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C3A RECEPTOR; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5 INHIBITOR; COMPLEMENT COMPONENT C5A RECEPTOR; COMPLEMENT COMPONENT C9; COMPLEMENT RECEPTOR; DECAY ACCELERATING FACTOR; ECULIZUMAB; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ALLOIMMUNITY; ANTIBODY MEDIATED REJECTION; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR IMMUNITY; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; DELAYED GRAFT FUNCTION; DRUG EFFECT; DRUG TARGETING; GRAFT VERSUS HOST REACTION; HEMOLYTIC UREMIC SYNDROME; HISTOCOMPATIBILITY; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREGULATION; KIDNEY TRANSPLANTATION; LYMPHOCYTE FUNCTION; NONHUMAN; PAROXYSMAL NOCTURNAL HEMOGLOBINURIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION;

ALLOGRAFT REJECTION; COMPLEMENT; COSTIMULATION; T CELLS; TRANSPLANTATION;

ANIMALS; ANTIGEN-PRESENTING CELLS; AUTOIMMUNITY; COMPLEMENT ACTIVATION; COMPLEMENT INACTIVATING AGENTS; COMPLEMENT SYSTEM PROTEINS; GRAFT REJECTION; HUMANS; LYMPHOCYTE ACTIVATION; MICE; T-LYMPHOCYTES;

EID: 84886290128     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2013.08.007     Document Type: Article

References (65)

1. Walport M.J. Complement. First of two parts. N Engl J Med 2001, 344:1058-1066.
2. Pratt J.R., Basheer S.A., Sacks S.H. Local synthesis of complement component C3 regulates acute renal transplant rejection. Nat Med 2002, 8:582-587.
3. Sheerin N.S., 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.
4. Tang Z., Lu B., Hatch E., Sacks S.H., Sheerin N.S. C3a mediates epithelial-to-mesenchymal transition in proteinuric nephropathy. J Am Soc Nephrol 2009, 20:593-603.
5. Heeger P.S., Lalli P.N., Lin F., et al. Decay-accelerating factor modulates induction of T cell immunity. J Exp Med 2005, 201:1523-1530.
6. Strainic M.G., 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.
7. Strainic M.G., Shevach E.M., An F., Lin F., Medof M.E. Absence of signaling into CD4(+) cells via C3aR and C5aR enables autoinductive TGF-beta1 signaling and induction of Foxp3(+) regulatory T cells. Nat Immunol 2012, 14:162-171.
8. Kwan W.H., van der Touw W., Paz-Artal E., Li M.O., Heeger P.S. Signaling through C5a receptor and C3a receptor diminishes function of murine natural regulatory T cells. J Exp Med 2013, 210:257-268.
9. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010, 11:785-797.
10. Medof M.E., 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.
11. Peake P.W., O'Grady S., Pussell B.A., Charlesworth J.A. C3a is made by proximal tubular HK-2 cells and activates them via the C3a receptor. Kidney Int 1999, 56:1729-1736.
12. Lalli P.N., Strainic M.G., Yang M., et al. Locally produced C5a binds to T cell-expressed C5aR to enhance effector T-cell expansion by limiting antigen-induced apoptosis. Blood 2008, 112:1759-1766.
13. Pepys M.B. Role of complement in the induction of immunological responses. Transplant Rev 1976, 32:93-120.
14. Dempsey P.W., Allison M.E., Akkaraju S., Goodnow C.C., Fearon D.T. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 1996, 271:348-350.
15. Bower J.F., Yang X., Sodroski J., Ross T.M. Elicitation of neutralizing antibodies with DNA vaccines expressing soluble stabilized human immunodeficiency virus type 1 envelope glycoprotein trimers conjugated to C3d. J Virol 2004, 78:4710-4719.
16. Gor D.O., Ding X., Li Q., Greenspan N.S. Genetic fusion of three tandem copies of murine C3d sequences to diphtheria toxin fragment B elicits a decreased fragment B-specific antibody response. Immunol Lett 2006, 102:38-49.
17. Liu J., Miwa T., Hilliard B., et al. The complement inhibitory protein DAF (CD55) suppresses T cell immunity in vivo. J Exp Med 2005, 201:567-577.
18. 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.
19. Liu J., Lin F., Strainic M.G., et al. IFN-gamma and IL-17 production in experimental autoimmune encephalomyelitis depends on local APC-T cell complement production. J Immunol 2008, 180:5882-5889.
20. Fang C., Miwa T., Shen H., Song W.C. Complement-dependent enhancement of CD8+ T cell immunity to lymphocytic choriomeningitis virus infection in decay-accelerating factor-deficient mice. J Immunol 2007, 179:3178-3186.
21. Lalli P.N., Strainic M.G., Lin F., Medof M.E., Heeger P.S. Decay accelerating factor can control T cell differentiation into IFN-gamma-producing effector cells via regulating local C5a-induced IL-12 production. J Immunol 2007, 179:5793-5802.
22. Li K., Anderson K.J., Peng Q., et al. Cyclic AMP plays a critical role in C3a-receptor-mediated regulation of dendritic cells in antigen uptake and T-cell stimulation. Blood 2008, 112:5084-5094.
23. Peng Q., Li K., Wang N., et al. Dendritic cell function in allostimulation is modulated by C5aR signaling. J Immunol 2009, 183:6058-6068.
24. Suresh M., Molina H., Salvato M.S., et al. Complement component 3 is required for optimal expansion of CD8 T cells during a systemic viral infection. J Immunol 2003, 170:788-794.
25. Bao L., Haas M., Pippin J., et al. Focal and segmental glomerulosclerosis induced in mice lacking decay-accelerating factor in T cells. J Clin Invest 2009, 119:1264-1274.
26. Hashimoto M., Hirota K., Yoshitomi H., et al. Complement drives Th17 cell differentiation and triggers autoimmune arthritis. J Exp Med 2010, 207:1135-1143.
27. Lin M., Yin N., Murphy B., et al. Immune cell-derived c3 is required for autoimmune diabetes induced by multiple low doses of streptozotocin. Diabetes 2010, 59:2247-2252.
28. Esposito A., Suedekum B., Liu J., et al. Decay accelerating factor is essential for successful corneal engraftment. Am J Transplant 2010, 10:527-534.
29. Krieger N.R., Yin D.P., Fathman C.G. CD4+ but not CD8+ cells are essential for allorejection. J Exp Med 1996, 184:2013-2018.
30. Ridge J.P., Di Rosa F., Matzinger P. A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell. Nature 1998, 393:474-478.
31. Schoenberger S.P., Toes R.E., van der Voort E.I., Offringa R., Melief C.J. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 1998, 393:480-483.
32. Vieyra M., Leisman S., Raedler H., et al. Complement regulates CD4 T-cell help to CD8 T cells required for murine allograft rejection. Am J Pathol 2011, 179:766-774.
33. Raedler H., Yang M., Lalli P.N., Medof M.E., Heeger P.S. Primed CD8(+) T-cell responses to allogeneic endothelial cells are controlled by local complement activation. Am J Transplant 2009, 9:1784-1795.
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. Raedler H., Vieyra M.B., Leisman S., et al. Anti-complement 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.
36. Josefowicz S.Z., Rudensky A. Control of regulatory T cell lineage commitment and maintenance. Immunity 2009, 30:616-625.
37. Gorantla V.S., Schneeberger S., Brandacher G., et al. T regulatory cells and transplantation tolerance. Transplant Rev (Orlando) 2010, 24:147-159.
38. Burrell B.E., Nakayama Y., Xu J., Brinkman C.C., Bromberg J.S. Regulatory T cell induction, migration, and function in transplantation. J Immunol 2012, 189:4705-4711.
39. Wan Y.Y., Flavell R.A. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 2007, 445:766-770.
40. Wang Y., Souabni A., Flavell R.A., Wan Y.Y. An intrinsic mechanism predisposes Foxp3-expressing regulatory T cells to Th2 conversion in vivo. J Immunol 2010, 185:5983-5992.
41. Huan J., Culbertson N., Spencer L., et al. Decreased FOXP3 levels in multiple sclerosis patients. J Neurosci Res 2005, 81:45-52.
42. Crellin N.K., Garcia R.V., Levings M.K. Altered activation of AKT is required for the suppressive function of human CD4+CD25+ T regulatory cells. Blood 2007, 109:2014-2022.
43. Sauer S., Bruno L., Hertweck A., et al. T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc Natl Acad Sci U S A 2008, 105:7797-7802.
44. Ouyang W., Beckett O., Ma Q., et al. Foxo proteins cooperatively control the differentiation of Foxp3+ regulatory T cells. Nat Immunol 2010, 11:618-627.
45. Ouyang W., Liao W., Luo C.T., et al. Novel Foxo1-dependent transcriptional programs control T(reg) cell function. Nature 2012, 491:554-559.
46. William van der Touw, Paolo Cravedi, Wing-hong Kwan, Estela Paz-Artal, Miriam Merad, Peter S. Heeger. Cutting Edge: Receptors for C3a and C5a modulate stability of alloantigen-reactive induced regulatory T cells. J Immunol 2013;190: 5921-5.
47. Li K., Fazekasova H., Wang N., et al. Functional modulation of human monocytes derived DCs by anaphylatoxins C3a and C5a. Immunobiology 2012, 217:65-73.
48. Li K., Fazekasova H., Wang N.Y., et al. Expression of complement components, receptors and regulators by human dendritic cells. Mol Immunol 2011, 48:1121-1127.
49. Martin U., Bock D., Arseniev L., et al. The human C3a receptor is expressed on neutrophils and monocytes, but not on B or T lymphocytes. J Exp Med 1997, 186:199-207.
50. Werfel T., Kirchhoff K., Wittmann M., et al. Activated human T lymphocytes express a functional C3a receptor. J Immunol 2000, 165:6599-6605.
51. Nataf S., Davoust N., Ames R.S., Barnum S.R. Human T cells express the C5a receptor and are chemoattracted to C5a. J Immunol 1999, 162:4018-4023.
52. Cravedi P, Leventhal J, Lakhani P, Ward SC, Donovan MJ, Heeger PS. Immune Cell-Derived C3a and C5a Costimulate Human T Cell Alloimmunity. Am J Transplant published online: 6 SEP 2013. DOI: 10.1111/ajt.12405.
53. Keslar K., Rodriguez E.R., Tan C.D., Starling R.C., Heeger P.S. Complement gene expression in human cardiac allograft biopsies as a correlate of histologic grade of injury. Transplantation 2008, 86:1319-1321.
54. Naesens M., Li L., Ying L., et al. Expression of complement components differs between kidney allografts from living and deceased donors. J Am Soc Nephrol 2009, 20:1839-1851.
55. Li K., Fazekasova H., Wang N., et al. Expression of complement components, receptors and regulators by human dendritic cells. Mol Immunol 2011, 48:1121-1127.
56. Brown K.M., Kondeatis E., Vaughan R.W., et al. Influence of donor C3 allotype on late renal-transplantation outcome. N Engl J Med 2006, 354:2014-2023.
57. Varagunam M., Yaqoob M.M., Dohler B., Opelz G. C3 polymorphisms and allograft outcome in renal transplantation. N Engl J Med 2009, 360:874-880.
58. Zuber J., Le Quintrec M., Sberro-Soussan R., et al. New insights into postrenal transplant hemolytic uremic syndrome. Nat Rev Nephrol 2011, 7:23-35.
59. Stegall M.D., 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.
60. Locke J.E., Magro C.M., Singer A.L., 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.
61. Zhou W., Farrar C.A., Abe K., et al. Predominant role for C5b-9 in renal ischemia/reperfusion injury. J Clin Invest 2000, 105:1363-1371.
62. Farrar C.A., Zhou W., Lin T., Sacks S.H. Local extravascular pool of C3 is a determinant of postischemic acute renal failure. FASEB J. 2006, 20:217-226.
63. Sacks S.H., Zhou W. The role of complement in the early immune response to transplantation. Nat Rev Immunol 2012, 12:431-442.
64. Kwan W.H., van der Touw W., Heeger P.S. Complement regulation of T cell immunity. Immunol Res 2012, 54:247-253.
65. Kwan W.H., Hashimoto D., Paz-Artal E., et al. Antigen-presenting cell-derived complement modulates graft-versus-host disease. J Clin Invest 2012, 122:2234-2238.