Characterization of Immunodominant BK Polyomavirus 9mer Epitope T Cell Responses

American Journal of Transplantation

Volumn 16, Issue 4, 2016, Pages 1193-1206

  Cioni, M ^a   Leboeuf, C ^a   Comoli, P ^b   Ginevri, F ^c   Hirsch, H H ^a,d  

^a UNIVERSITY OF BASEL   (Switzerland)

^b FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^c G GASLINI INSTITUTE   (Italy)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; IMMUNOGLOBULIN G; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; HLA ANTIGEN;

ADOPTIVE TRANSFER; ADULT; ARTICLE; BINDING AFFINITY; BIOINFORMATICS; BK VIRUS; CD8+ T LYMPHOCYTE; CELL ASSAY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; EUROPE; HLA SYSTEM; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; MAJOR CLINICAL STUDY; NORMAL HUMAN; NORTH AMERICA; PREVALENCE; PRIORITY JOURNAL; T LYMPHOCYTE; VIREMIA; VIRUS LOAD; VIRUS REPLICATION; ADVERSE EFFECTS; CHILD; FEMALE; FOLLOW UP; IMMUNOLOGY; KIDNEY FAILURE, CHRONIC; KIDNEY TRANSPLANTATION; MALE; MIDDLE AGED; PHYSIOLOGY; POLYOMAVIRUS INFECTIONS; PROSPECTIVE STUDY; TUMOR VIRUS INFECTIONS; VIROLOGY;

BK VIRUS; CHILD; ENZYME-LINKED IMMUNOSPOT ASSAY; EPITOPES, T-LYMPHOCYTE; FEMALE; FOLLOW-UP STUDIES; HLA ANTIGENS; HUMANS; KIDNEY FAILURE, CHRONIC; KIDNEY TRANSPLANTATION; MALE; MIDDLE AGED; POLYOMAVIRUS INFECTIONS; PROSPECTIVE STUDIES; T-LYMPHOCYTES; TUMOR VIRUS INFECTIONS; VIRUS REPLICATION;

EID: 84959420344     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.13598     Document Type: Article

References (76)

1. Rinaldo CH, Hirsch HH., The human polyomaviruses: From orphans and mutants to patchwork family. APMIS 2013; 121: 681-684.
2. Pergam SA, Hirsch HH., Human adenovirus, polyomavirus, and parvovirus infections in patients undergoing hematopoietic stem-cell transplantation. In:, Forman SJ, Antin H, Appelbaum FR, editors. Thomas' Hematopoietic Cell Transplantation. 5th ed. Honoken, NJ: John Wiley & Sons Ltd.; 2016: 1090-1104.
3. Knowles WA, Pipkin P, Andrews N, et al., Population-based study of antibody to the human polyomaviruses BKV and JCV and the simian polyomavirus SV40. J Med Virol 2003; 71: 115-123.
4. Egli A, Infanti L, Dumoulin A, et al., Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis 2009; 199: 837-846.
5. Schmidt T, Adam C, Hirsch HH, et al., BK polyomavirus-specific cellular immune responses are age-dependent and strongly correlate with phases of virus replication. Am J Transplant 2014; 14: 1334-1345.
6. Chesters PM, Heritage J, McCance DJ., Persistence of DNA sequences of BK virus and JC virus in normal human tissues and in diseased tissues. J Infect Dis 1983; 147: 676-684.
7. Polo C, Perez JL, Mielnichuck A, Fedele CG, Niubo J, Tenorio A., Prevalence and patterns of polyomavirus urinary excretion in immunocompetent adults and children. Clin Microbiol Infect 2004; 10: 640-644.
8. Hirsch HH., BK virus: Opportunity makes a pathogen. Clin Infect Dis 2005; 41: 354-360.
9. Rinaldo CH, Tylden GD, Sharma BN., The human polyomavirus BK (BKPyV): Virological background and clinical implications. APMIS 2013; 121: 728-745.
10. Hirsch HH, Steiger J., Polyomavirus BK., Lancet Infect Dis 2003; 3: 611-623.
11. Binet I, Nickeleit V, Hirsch HH, et al., Polyomavirus disease under new immunosuppressive drugs: A cause of renal graft dysfunction and graft loss. Transplantation 1999; 67: 918-922.
12. Randhawa PS, Finkelstein S, Scantlebury V, et al., Human polyoma virus-associated interstitial nephritis in the allograft kidney. Transplantation 1999; 67: 103-109.
13. Drachenberg CB, Beskow CO, Cangro CB, et al., Human polyoma virus in renal allograft biopsies: Morphological findings and correlation with urine cytology. Hum Pathol 1999; 30: 970-977.
14. Cesaro S, Brugiolo A, Faraci M, et al., Incidence and treatment of hemorrhagic cystitis in children given hematopoietic stem cell transplantation: A survey from the Italian association of pediatric hematology oncology-bone marrow transplantation group. Bone Marrow Transplant 2003; 32: 925-931.
15. Erard V, Kim HW, Corey L, et al., BK DNA viral load in plasma: Evidence for an association with hemorrhagic cystitis in allogeneic hematopoietic cell transplant recipients. Blood 2005; 106: 1130-1132.
16. Giraud G, Bogdanovic G, Priftakis P, et al., The incidence of hemorrhagic cystitis and BK-viruria in allogeneic hematopoietic stem cell recipients according to intensity of the conditioning regimen. Haematologica 2006; 91: 401-404.
17. Svahn BM, Alvin O, Ringden O, Gardulf A, Remberger M., Costs of allogeneic hematopoietic stem cell transplantation. Transplantation 2006; 82: 147-153.
18. Zaia J, Baden L, Boeckh MJ, et al., Viral disease prevention after hematopoietic cell transplantation. Bone Marrow Transplant 2009; 44: 471-482.
19. Farasati NA, Shapiro R, Vats A, Randhawa P., Effect of leflunomide and cidofovir on replication of BK virus in an in vitro culture system. Transplantation 2005; 79: 116-118.
20. Bernhoff E, Gutteberg TJ, Sandvik K, Hirsch HH, Rinaldo CH., Cidofovir inhibits polyomavirus BK replication in human renal tubular cells downstream of viral early gene expression. Am J Transplant 2008; 8: 1413-1422.
21. Sharma BN, Li R, Bernhoff E, Gutteberg TJ, Rinaldo CH., Fluoroquinolones inhibit human polyomavirus BK (BKV) replication in primary human kidney cells. Antiviral Res 2011; 92: 115-123.
22. Bernhoff E, Tylden GD, Kjerpeseth LJ, Gutteberg TJ, Hirsch HH, Rinaldo CH., Leflunomide inhibition of BK virus replication in renal tubular epithelial cells. J Virol 2010; 84: 2150-2156.
23. Rinaldo CH, Gosert R, Bernhoff E, Finstad S, Hirsch HH., 1-O-hexadecyloxypropyl cidofovir (CMX001) effectively inhibits polyomavirus BK replication in primary human renal tubular epithelial cells. Antimicrob Agents Chemother 2010; 54: 4714-4722.
24. Knoll GA, Humar A, Fergusson D, et al., Levofloxacin for BK virus prophylaxis following kidney transplantation: A randomized clinical trial. JAMA 2014; 312: 2106-2114.
25. Hirsch HH, Knowles W, Dickenmann M, et al., Prospective study of polyomavirus type BK replication and nephropathy in renal-transplant recipients. N Engl J Med 2002; 347: 488-496.
26. Hirsch HH, Brennan DC, Drachenberg CB, et al., Polyomavirus-associated nephropathy in renal transplantation: Interdisciplinary analyses and recommendations. Transplantation 2005; 79: 1277-1286.
27. Hirsch HH, Randhawa P., BK polyomavirus in solid organ transplantation. Am J Transplant 2013; 13 (Suppl 4): 179-188.
28. KDIGO clinical practice guideline for the care of kidney transplant recipients. Am J Transplant 2009; 9 (Suppl 3): S1-155.
29. Brennan DC, Agha I, Bohl DL, et al., Incidence of BK with tacrolimus versus cyclosporine and impact of preemptive immunosuppression reduction. Am J Transplant 2005; 5: 582-594.
30. Ginevri F, Azzi A, Hirsch HH, et al., Prospective monitoring of polyomavirus BK replication and impact of pre-emptive intervention in pediatric kidney recipients. Am J Transplant 2007; 7: 2727-2735.
31. Schaub S, Hirsch HH, Dickenmann M, et al., Reducing immunosuppression preserves allograft function in presumptive and definitive polyomavirus-associated nephropathy. Am J Transplant 2010; 10: 2615-2623.
32. Sood P, Senanayake S, Sujeet K, et al., Management and outcome of BK viremia in renal transplant recipients: A prospective single-center study. Transplantation 2012; 94: 814-821.
33. Menter T, Mayr M, Schaub S, Mihatsch MJ, Hirsch HH, Hopfer H., Pathology of resolving polyomavirus-associated nephropathy. Am J Transplant 2013; 13: 1474-1483.
34. Comoli P, Azzi A, Maccario R, et al., Polyomavirus BK-specific immunity after kidney transplantation. Transplantation 2004; 78: 1229-1232.
35. Binggeli S, Egli A, Schaub S, et al., Polyomavirus BK-specific cellular immune response to VP1 and large T-antigen in kidney transplant recipients. Am J Transplant 2007; 7: 1131-1139.
36. Schachtner T, Muller K, Stein M, Diezemann C, Sefrin A, Babel N, et al., BK virus-specific immunity kinetics: a predictor of recovery from polyomavirus BK-associated nephropathy. Am J Transplant. 2011; 11 (11): 2443-2452.
37. Hirsch HH, Vincenti F, Friman S, et al., Polyomavirus BK replication in de novo kidney transplant patients receiving tacrolimus or cyclosporine: A prospective, randomized, multicenter study. Am J Transplant 2013; 13: 136-145.
38. Schold JD, Rehman S, Kayler LK, Magliocca J, Srinivas TR, Meier-Kriesche HU., Treatment for BK virus: Incidence, risk factors and outcomes for kidney transplant recipients in the United States. Transpl Int 2009; 22: 626-634.
39. Borni-Duval C, Caillard S, Olagne J, et al., Risk factors for BK virus infection in the era of therapeutic drug monitoring. Transplantation 2013; 95: 1498-1505.
40. Dharnidharka VR, Cherikh WS, Abbott KC., An OPTN analysis of national registry data on treatment of BK virus allograft nephropathy in the United States. Transplantation 2009; 87: 1019-1026.
41. Manitpisitkul W, Drachenberg C, Ramos E, et al., Maintenance immunosuppressive agents as risk factors for BK virus nephropathy: A case-control study. Transplantation 2009; 88: 83-88.
42. Geddes CC, Gunson R, Mazonakis E, et al., BK viremia surveillance after kidney transplant: Single-center experience during a change from cyclosporine-to lower-dose tacrolimus-based primary immunosuppression regimen. Transpl Infect Dis 2011; 13: 109-116.
43. Dadhania D, Snopkowski C, Ding R, et al., Epidemiology of BK virus in renal allograft recipients: Independent risk factors for BK virus replication. Transplantation 2008; 86: 521-528.
44. Awadallah Y, Duquesnoy R, Randhawa P, Shapiro R., HLA susceptibility to BKV infection. Am J Transplant 2006; 6: 640; author reply 641.
45. Ramos E, Drachenberg CB, Papadimitriou JC, et al., Clinical course of polyoma virus nephropathy in 67 renal transplant patients. J Am Soc Nephrol 2002; 13: 2145-2151.
46. Matas AJ, Smith JM, Skeans MA, et al., OPTN/SRTR 2013 annual data report: Kidney. Am J Transplant 2015; 15 (Suppl 2): 1-34.
47. Bohl DL, Storch GA, Ryschkewitsch C, et al., Donor origin of BK virus in renal transplantation and role of HLA C7 in susceptibility to sustained BK viremia. Am J Transplant 2005; 5: 2213-2221.
48. Sood P, Senanayake S, Sujeet K, et al., Donor and recipient BKV-specific IgG antibody and posttransplantation BKV infection: A prospective single-center study. Transplantation 2013; 95: 896-902.
49. Binggeli S, Egli A, Dickenmann M, Binet I, Steiger J, Hirsch HH., BKV replication and cellular immune responses in renal transplant recipients. Am J Transplant 2006: 2218-2219.
50. Weist BJ, Schmueck M, Fuehrer H, Sattler A, Reinke P, Babel N., The role of CD4(+) T cells in BKV-specific T cell immunity. Med Microbiol Immunol. 2014; 203: 395-408.
51. Provenzano M, Bracci L, Wyler S, et al., Characterization of highly frequent epitope-specific CD45RA+/CCR7+/- T lymphocyte responses against p53-binding domains of the human polyomavirus BK large tumor antigen in HLA-A∗0201+ BKV-seropositive donors. J Transl Med 2006; 4: 47.
52. Krymskaya L, Sharma MC, Martinez J, et al., Cross-reactivity of T lymphocytes recognizing a human cytotoxic T-lymphocyte epitope within BK and JC virus VP1 polypeptides. J Virol 2005; 79: 11170-11178.
53. Schachtner T, Stein M, Babel N, Reinke P., The loss of BKV-specific immunity from pretransplantation to posttransplantation identifies kidney transplant recipients at increased risk of BKV replication. Am J Transplant 2015; 15: 2159-2169.
54. Li J, Melenhorst J, Hensel N, et al., T-cell responses to peptide fragments of the BK virus T antigen: Implications for cross-reactivity of immune response to JC virus. J Gen Virol 2006; 87: 2951-2960.
55. Randhawa PS, Popescu I, Macedo C, et al., Detection of CD8+ T cells sensitized to BK virus large T antigen in healthy volunteers and kidney transplant recipients. Hum Immunol 2006; 67: 298-302.
56. Ramaswami B, Popescu I, Macedo C, et al., HLA-A01-, -A03-, and -A024-binding nanomeric epitopes in polyomavirus BK large T antigen. Hum Immunol 2009; 70: 722-728.
57. Kardas P, Sadeghi M, Weissbach FH, et al., Inter- and intralaboratory comparison of JC polyomavirus antibody testing using two different virus-like particle-based assays. Clin Vaccine Immunol 2014; 21: 1581-1588.
58. Kardas P, Leboeuf C, Hirsch HH., Optimizing JC and BK polyomavirus IgG testing for seroepidemiology and patient counseling. J Clin Virol 2015; 71: 28-33.
59. Welcome to SYFPEITHI. [cited 2016 Jan 1]. Available from: http://www.syfpeithi.de/0-Home.htm.
60. Schuler MM, Nastke MD, Stevanovikc S., SYFPEITHI: Database for searching and T-cell epitope prediction. Methods Mol Biol 2007; 409: 75-93.
61. Immune Epitope Database and Analysis Resource. [cited 2016 Jan 1]. Available from: http://www.iedb.org/home-v3.php.
62. Vita R, Zarebski L, Greenbaum JA, et al., The immune epitope database 2.0. Nucleic Acids Res 2010; 38: D854-D862.
63. Allele and Frequencies in Worldwide Populations. [cited 2016 Jan 1]. Available from: http://www.allelefrequencies.net/
64. Fishman JA., BK virus nephropathy-polyomavirus adding insult to injury. N Engl J Med. 2002; 347 (7): 527-530.
65. Ramos E, Drachenberg CB, Wali R, Hirsch HH., The decade of polyomavirus BK-associated nephropathy: State of affairs. Transplantation 2009; 87: 621-630.
66. Kuypers DR., Management of polyomavirus-associated nephropathy in renal transplant recipients. Nat Rev Nephrol 2012; 8: 390-402.
67. Comoli P, Hirsch HH, Ginevri F., Cellular immune responses to BK virus. Curr Opin Organ Transplant 2008; 13: 569-574.
68. Mueller K, Schachtner T, Sattler A, et al., BK-VP3 as a new target of cellular immunity in BK virus infection. Transplantation 2011; 91: 100-107.
69. Trydzenskaya H, Sattler A, Muller K, et al., Novel approach for improved assessment of phenotypic and functional characteristics of BKV-specific T-cell immunity. Transplantation 2011; 92: 1269-1277.
70. Gosert R, Rinaldo CH, Funk GA, et al., Polyomavirus BK with rearranged noncoding control region emerge in vivo in renal transplant patients and increase viral replication and cytopathology. J Exp Med 2008; 205: 841-852.
71. Sester M, Leboeuf C, Schmidt T, Hirsch HH., The ABC of virus-specific T-cell immunity in solid organ transplantation. Am J Transplant. 2015 Dec 23. doi: 10.1111/ajt.13684. [Epub ahead of print]
72. Wade JA, Hurley CK, Takemoto SK, et al., HLA mismatching within or outside of cross-reactive groups (CREGs) is associated with similar outcomes after unrelated hematopoietic stem cell transplantation. Blood 2007; 109: 4064-4070.
73. Masutani K, Ninomiya T, Randhawa P., HLA-A2, HLA-B44 and HLA-DR15 are associated with lower risk of BK viremia. Nephrol Dial Transplant 2013; 28: 3119-3126.
74. Chen Y, Trofe J, Gordon J, Autissier P, Woodle ES, Koralnik IJ., BKV and JCV large T antigen-specific CD8(+) T cell response in HLA A∗0201(+) kidney transplant recipients with polyomavirus nephropathy and patients with progressive multifocal leukoencephalopathy. J Clin Virol 2008; 42: 198-202.
75. Wilson JJ, Pack CD, Lin E, et al., CD8 T cells recruited early in mouse polyomavirus infection undergo exhaustion. J Immunol 2012; 188: 4340-4348.
76. Hofstetter AR, Ford ML, Sullivan LC, et al., MHC class Ib-restricted CD8 T cells differ in dependence on CD4 T cell help and CD28 costimulation over the course of mouse polyomavirus infection. J Immunol 2012; 188: 3071-3079.