Impaired direct priming of CD8 T cells by donor-derived cytomegalovirus following kidney transplantation

Journal of the American Society of Nephrology

Volumn 24, Issue 10, 2013, Pages 1698-1708

  Shabir, Shazia ^a,b   Kaul, Baksho ^a,b   Pachnio, Annette ^b   Banham, Gemma D ^a,b   Smith, Helen ^b   Chand, Sourabh ^a,b   Jham, Seema ^a,b   Harper, Lorraine ^b   Ball, Simon ^a,b   Rahbar, Afsar ^c   Söderberg Nauclér, Cecilia ^c   Moss, Paul ^b   Borrows, Richard ^a,b  

^a QUEEN ELIZABETH HOSPITAL   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BASILIXIMAB; CORTICOSTEROID; HLA ANTIGEN CLASS 1; MYCOPHENOLIC ACID; TACROLIMUS;

ADULT; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; FEMALE; HLA MATCHING; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; INFECTION RISK; KIDNEY ALLOGRAFT; KIDNEY DONOR; KIDNEY TRANSPLANTATION; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROSPECTIVE STUDY;

EID: 84885078992     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013040340     Document Type: Article

References (37)

1. Moss P, Khan N: CD8 (+) T-cell immunity to cytomegalovirus. Hum Immunol 65: 456-464, 2004
2. Polić B, Hengel H, Krmpotić A, Trgovcich J, Pavić I, Luccaronin P, Jonjić S, Koszinowski UH: Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J ExpMed 188: 1047-1054, 1998
3. Pahl-Seibert MF, Juelch M, Podlech J, Thomas D, Deegen P, Reddehase MJ, Holtappels R: Highly protective in vivo function of cytomegalovirus IE1 epitope-specific memory CD8 T cells purified by T-cell receptorbased cell sorting. J Virol 79: 5400-5413, 2005
4. Grundy JE, Lui SF, Super M, Berry NJ, Sweny P, Fernando ON, Moorhead J, Griffiths PD. Symptomatic cytomegalovirus infection in seropositive kidney recipients: Reinfection with donor virus rather than reactivation of recipient virus. Lancet 1988. 16;2(8603):132-5.
5. Kliem V, Fricke L, Wollbrink T, Burg M, Radermacher J, Rohde F: Improvement in long-term renal graft survival due to CMV prophylaxis with oral ganciclovir: Results of a randomized clinical trial. Am J Transplant 8: 975-983, 2008
6. Witzke O, Hauser IA, Bartels M, Wolf G, Wolters H, Nitschke M; VIPP Study Group: Valganciclovir prophylaxis versus preemptive therapy in cytomegalovirus-positive renal allograft recipients: 1-year results of a randomized clinical trial. Transplantation 93: 61-68, 2012
7. Atabani SF, Smith C, Atkinso NC, Aldridge RW, Rodriguez-Perálvarez M, Rolando N, Harber M, Jones G, O'Riordan A, Burroughs AK, Thorburn D, O'Beirne J, Milne RS, Emery VC, Griffiths PD: Cytomegalovirus replication kinetics in solid organ transplant recipients managed by preemptive therapy. Am J Transplant 12: 2457-2464, 2012
8. Manuel O, Asberg A, Pang X, Rollag H, Emery VC, Preiksaitis JK, Kumar D, Pescovitz MD, Bignamini AA, Hartmann A, Jardine AG, Humar A: Impact of genetic polymorphisms in cytomegalovirus glycoprotein B on outcomes in solid-organ transplant recipients with cytomegalovirus disease. Clin Infect Dis 49: 1160-1166, 2009
9. Ishibashi K, Tokumoto T, Shirakawa H, Hashimoto K, Ikuta K, Kushida N, Yanagida T, Shishido K, Aikawa K, Toma H, Inoue N, Yamaguchi O, Tanabe K, Suzutani T: Lack of antibodies against the antigen domain 2 epitope of cytomegalovirus (CMV) glycoprotein B is associated with CMV disease after renal transplantation in recipients having the same glycoprotein H serotypes as their donors. Transpl Infect Dis 13: 318-323, 2011
10. Schnitzler MA, Lowell JA, Hmiel SP, Hardinger KL, Liapis H, Ceriotti CS, Brennan DC: Cytomegalovirus disease after prophylaxis with oral ganciclovir in renal transplantation: The importance of HLA-DR matching. J Am Soc Nephrol 14: 780-785, 2003
11. Pouteil-Noble C, Bétuel H, Raffaele P, Megri K, Louvier C, Lefrançois N, Bosshard S, Dubernard JM, Aymard M, Touraine JL: [Influence of HLA compatibility on cytomegalovirus infection in kidney transplantation]. Presse Med 20: 2022-2024, 1991
12. Blancho G, Josien R, Douillard D, Bignon JD, Cesbron A, Soulillou JP: The influence of HLA A-B-DR matching on cytomegalovirus disease after renal transplantation. Evidence that HLA-DR7-matched recipients are more susceptible to cytomegalovirus disease. Transplantation 54: 871-874, 1992
13. Kraat YJ, Christiaans MH, Nieman FH, van den Berg-Loonen PM, van Hooff JP, Bruggeman CA: Increased frequency of CMV infection in HLA-DR7 matched renal allograft recipients. Lancet 341: 494-495, 1993
14. Smyth LA, Hervouet C, Hayday T, Becker PD, Ellis R, Lechler RI, Lombardi G, Klavinskis LS: Acquisition of MHC: peptide complexes by dendritic cells contributes to the generation of antiviral CD8+ T cell immunity in vivo. J Immunol 189: 2274-2282, 2012
15. Wakim LM, Bevan MJ: Cross-dressed dendritic cells drivememory CD8+ T-cell activation after viral infection. Nature 471: 629-632, 2011
16. Snyder CM, Allan JE, Bonnett EL, Doom CM, Hill AB: Cross-presentation of a spread-defective MCMV is sufficient to prime the majority of virus-specific CD8+ T cells. PLoS ONE 5: e9681, 2010
17. Munks MW, Pinto AK, Doom CM, Hill AB: Viral interference with antigen presentation does not alter acute or chronic CD8 T cell immunodominance in murine cytomegalovirus infection. J Immunol 178: 7235-7241, 2007
18. Walton SM, Mandaric S, Torti N, Zimmermann A, Hengel H, Oxenius A: Absence of cross-presenting cells in the salivary gland and viral immune evasion confine cytomegalovirus immune control to effector CD4 T cells. PLoS Pathog 7: e1002214, 2011
19. Andrews DM, Andoniou CE, Granucci F, Ricciardi-Castagnoli P, Degli-Esposti MA: Infection of dendritic cells by murine cytomegalovirus induces functional paralysis. Nat Immunol 2: 1077-1084, 2001
20. Loewendorf A, Krüger C, Borst EM, Wagner M, Just U, Messerle M: Identification of a mouse cytomegalovirus gene selectively targeting CD86 expression on antigen-presenting cells. JVirol 78: 13062-13071, 2004
21. Benedict CA, Loewendorf A, Garcia Z, Blazar BR, Janssen EM: Dendritic cell programming by cytomegalovirus stunts naive T cell responses via the PD-L1/PD-1 pathway. J Immunol 180: 4836-4847, 2008
22. Gredmark S, Söderberg-Nauclér C: Human cytomegalovirus inhibits differentiation of monocytes into dendritic cells with the consequence of depressed immunological functions. J Virol 77: 10943-10956, 2003
23. Jenkins C, Garcia W, Godwin MJ, Spencer JV, Stern JL, Abendroth A, Slobedman B: Immunomodulatory properties of a viral homolog of human interleukin-10 expressed by human cytomegalovirus during the latent phase of infection. J Virol 82: 3736-3750, 2008
24. Liapis H, Storch GA, Hill DA, Rueda J, Brennan DC: CMV infection of the renal allograft is much more common than the pathology indicates: A retrospective analysis of qualitative and quantitative buffy coat CMVPCR, renal biopsy pathology and tissue CMV-PCR. Nephrol Dial Transplant 18: 397-402, 2003
25. Boudreault AA, Xie H, Rakita RM, Scott JD, Davis CL, Boeckh M, Limaye AP: Risk factors for late-onset cytomegalovirus disease in donor seropositive/recipient seronegative kidney transplant recipients who receive antiviral prophylaxis. Transpl Infect Dis 13: 244-249, 2011
26. Grundy JE, Ayles HM, McKeating JA, Butcher RG, Griffiths PD, Poulter LW: Enhancement of class I HLA antigen expression by cytomegalovirus: Role in amplification of virus infection. J Med Virol 25: 483-495, 1988
27. Hosenpud JD, Chou SW, Wagner CR: Cytomegalovirus-induced regulation of major histocompatibility complex class I antigen expression in human aortic smooth muscle cells. Transplantation 52: 896-903, 1991
28. Grundy JE, McKeating JA, Ward PJ, Sanderson AR, Griffiths PD: Beta 2 microglobulin enhances the infectivity of cytomegalovirus and when bound to the virus enables class I HLA molecules to be used as a virus receptor. J Gen Virol 68: 793-803, 1987
29. Waldman WJ, Knight DA: Cytokine-mediated induction of endothelial adhesion molecule and histocompatibility leukocyte antigen expression by cytomegalovirus-activated T cells. Am J Pathol 148: 105-119, 1996
30. Simon CO, Holtappels R, Tervo HM, Böhm V, Däubner T, Oehrlein-Karpi SA, Kühnapfel B, Renzaho A, Strand D, Podlech J, Reddehase MJ, Grzimek NK: CD8 T cells control cytomegalovirus latency by epitopespecific sensing of transcriptional reactivation. J Virol 80: 10436-10456, 2006
31. Holtappels R, Gillert-Marien D, Thomas D, Podlech J, Deegen P, Herter S, Oehrlein-Karpi SA, Strand D, Wagner M, Reddehase MJ: Cytomegalovirus encodes a positive regulator of antigen presentation. J Virol 80: 7613-7624, 2006
32. Ishibashi K, Tokumoto T, Tanabe K, Shirakawa H, Hashimoto K, Kushida N, Yanagida T, Inoue N, Yamaguchi O, Toma H, Suzutani T: Association of the outcome of renal transplantation with antibody response to cytomegalovirus strain-specific glycoprotein H epitopes. Clin Infect Dis 45: 60-67, 2007
33. Sylwester AW, Mitchell BL, Edgar JB, Taormina C, Pelte C, Ruchti F, Sleath PR, Grabstein KH, Hosken NA, Kern F, Nelson JA, Picker LJ: Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med 202: 673-685, 2005
34. Holtappels R, Simon CO, Munks MW, Thomas D, Deegen P, Kühnapfel B, Däubner T, Emde SF, Podlech J, Grzimek NK, Oehrlein-Karpi SA, Hill AB, Reddehase MJ: Subdominant CD8 T-cell epitopes account for protection against cytomegalovirus independent of immunodomination. J Virol 82: 5781-5796, 2008
35. Farci P, Shimoda A, Coiana A, Diaz G, Peddis G, Melpolder JC, Strazzera A, Chien DY, Munoz SJ, Balestrieri A, Purcell RH, Alter HJ: The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288: 339-344, 2000
36. Cantisán S, Lara R, Montejo M, Redel J, Rodríguez-Benot A, Gutiérrez-Aroca J, González-Padilla M, Bueno L, Rivero A, Solana R, Torre-Cisneros J: Pretransplant interferon-g secretion by CMV-specific CD8+ T cells informs the risk of CMV replication after transplantation. Am J Transplant 13: 738-745, 2013
37. Kratky W, Reis e Sousa C, Oxenius A, Spörri R: Direct activation of antigenpresenting cells is required for CD8+ T-cell priming and tumor vaccination. Proc Natl Acad Sci U S A 108: 17414-17419, 2011