Definition and characterization of novel HLA-*A02-restricted CD8+ T cell epitopes derived from JCV polyomavirus with clinical relevance

Oncotarget

Volumn 8, Issue 2, 2017, Pages 2485-2500

  Mani, Jiju ^a   Wang, Lei ^a   Hückelhoven, Angela G ^a   Schmitt, Anita ^a   Gedvilaite, Alma ^b   Jin, Nan ^a,c   Kleist, Christian ^a   Ho, Anthony D ^a   Schmitt, Michael ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b VILNIUS UNIVERSITY   (Lithuania)

^c SOUTHEAST UNIVERSITY   (China)

Author keywords

Immunotherapy; JCV; Progressive multifocal leukoencephalopathy; T cell epitopes; Virus like particles

Indexed keywords

EPITOPE; GAMMA INTERFERON; HLA A ANTIGEN; PROTEIN VP1; HLA A2 ANTIGEN; HLA-A*02:01 ANTIGEN; VIRAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BK VIRUS; CD8+ T LYMPHOCYTE; CELL KILLING; CELL SPECIFICITY; CONTROLLED STUDY; CROSS REACTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSPOT ASSAY; EPITOPE MAPPING; FLOW CYTOMETRY; HUMAN; HUMAN CELL; JC VIRUS; LYMPHOCYTE FUNCTION; NORMAL HUMAN; PEPTIDE ANALYSIS; VIRUS LIKE AGENT; CHEMISTRY; IMMUNOLOGY; METABOLISM;

AMINO ACID SEQUENCE; BK VIRUS; CD8-POSITIVE T-LYMPHOCYTES; CROSS REACTIONS; EPITOPE MAPPING; EPITOPES, T-LYMPHOCYTE; HLA-A2 ANTIGEN; HUMANS; JC VIRUS; VIRAL STRUCTURAL PROTEINS;

EID: 85009786646     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12387     Document Type: Article

References (62)

1. Mani J, Jin N, Schmitt M. Cellular immunotherapy for patients with reactivation of JC and BK polyomaviruses after transplantation. Cytotherapy. 2014; 16: 1325-35. doi: 10.1016/j.jcyt.2014.04.003
2. 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: 676-84
3. Gheuens S, Pierone G, Peeters P, Koralnik IJ. Progressive multifocal leukoencephalopathy in individuals with minimal or occult immunosuppression. J Neurol Neurosurg Psychiatry. 2010; 81: 247-54. doi: 10.1136/jnnp.2009.187666
4. Langer-Gould A, Atlas SW, Green AJ, Bollen AW, Pelletier D. Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. N Engl J Med. 2005; 353: 375-81. doi: 10.1056/NEJMoa051847
5. Molloy ES, Calabrese LH. Therapy: Targeted but not trouble-free: efalizumab and PML. Nat Rev Rheumatol. 2009; 5: 418-9. doi: 10.1038/nrrheum.2009.142
6. Schmidt-Hieber M, Schwender J, Heinz WJ, Zabelina T, Kuhl JS, Mousset S, Schuttrumpf S, Junghanss C, Silling G, Basara N, Neuburger S, Thiel E, Blau IW. Viral encephalitis after allogeneic stem cell transplantation: a rare complication with distinct characteristics of different causative agents. Haematologica. 2011; 96: 142-9. doi: 10.3324/haematol.2010.029876
7. Koralnik IJ, Du Pasquier RA, Kuroda MJ, Schmitz JE, Dang X, Zheng Y, Lifton M, Letvin NL. Association of prolonged survival in HLA-A2+ progressive multifocal leukoencephalopathy patients with a CTL response specific for a commonly recognized JC virus epitope. J Immunol. 2002; 168: 499-504
8. Krymskaya L, Sharma MC, Martinez J, Haq W, Huang EC, Limaye AP, Diamond DJ, Lacey SF. Cross-reactivity of T lymphocytes recognizing a human cytotoxic T-lymphocyte epitope within BK and JC virus VP1 polypeptides. J Virol. 2005; 79: 11170-8. doi: 10.1128/JVI.79.17.11170-11178.2005
9. Sharma MC, Zhou W, Martinez J, Krymskaya L, Srivastava T, Haq W, Diamond DJ, Lacey SF. Cross-reactive CTL recognizing two HLA-A*02-restricted epitopes within the BK virus and JC virus VP1 polypeptides are frequent in immunocompetent individuals. Virology. 2006; 350: 128-36. doi: 10.1016/j.virol.2006.02.040
10. Du Pasquier RA, Kuroda MJ, Schmitz JE, Zheng Y, Martin K, Peyerl FW, Lifton M, Gorgone D, Autissier P, Letvin NL, Koralnik IJ. Low frequency of cytotoxic T lymphocytes against the novel HLA-A*0201-restricted JC virus epitope VP1(p36) in patients with proven or possible progressive multifocal leukoencephalopathy. J Virol. 2003; 77: 11918-26
11. Heslop HE, Ng CY, Li C, Smith CA, Loftin SK, Krance RA, Brenner MK, Rooney CM. Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat Med. 1996; 2: 551-5
12. Rooney CM, Smith CA, Ng CY, Loftin S, Li C, Krance RA, Brenner MK, Heslop HE. Use of gene-modified virusspecific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet. 1995; 345: 9-13
13. Walter EA, Greenberg PD, Gilbert MJ, Finch RJ, Watanabe KS, Thomas ED, Riddell SR. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N Engl J Med. 1995; 333: 1038-44. doi: 10.1056/NEJM199510193331603
14. Perruccio K, Tosti A, Burchielli E, Topini F, Ruggeri L, Carotti A, Capanni M, Urbani E, Mancusi A, Aversa F, Martelli MF, Romani L, Velardi A. Transferring functional immune responses to pathogens after haploidentical hematopoietic transplantation. Blood. 2005; 106: 4397-406. doi: 10.1182/blood-2005-05-1775
15. Einsele H, Roosnek E, Rufer N, Sinzger C, Riegler S, Loffler J, Grigoleit U, Moris A, Rammensee HG, Kanz L, Kleihauer A, Frank F, Jahn G, et al. Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood. 2002; 99: 3916-22
16. Leen AM, Myers GD, Sili U, Huls MH, Weiss H, Leung KS, Carrum G, Krance RA, Chang CC, Molldrem JJ, Gee AP, Brenner MK, Heslop HE, et al. Monoculture-derived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat Med. 2006; 12: 1160-6. doi: 10.1038/nm1475
17. Leen AM, Christin A, Myers GD, Liu H, Cruz CR, Hanley PJ, Kennedy-Nasser AA, Leung KS, Gee AP, Krance RA, Brenner MK, Heslop HE, Rooney CM, et al. Cytotoxic T lymphocyte therapy with donor T cells prevents and treats adenovirus and Epstein-Barr virus infections after haploidentical and matched unrelated stem cell transplantation. Blood. 2009; 114: 4283-92. doi: 10.1182/blood-2009-07-232454
18. Balduzzi A, Lucchini G, Hirsch HH, Basso S, Cioni M, Rovelli A, Zincone A, Grimaldi M, Corti P, Bonanomi S, Biondi A, Locatelli F, Biagi E, et al. Polyomavirus JC-targeted T-cell therapy for progressive multiple leukoencephalopathy in a hematopoietic cell transplantation recipient. Bone Marrow Transplant. 2011; 46: 987-92. doi: 10.1038/bmt.2010.221
19. Feuchtinger T, Opherk K, Bethge WA, Topp MS, Schuster FR, Weissinger EM, Mohty M, Or R, Maschan M, Schumm M, Hamprecht K, Handgretinger R, Lang P, et al. Adoptive transfer of pp65-specific T cells for the treatment of chemorefractory cytomegalovirus disease or reactivation after haploidentical and matched unrelated stem cell transplantation. Blood. 2010; 116: 4360-7. doi: 10.1182/blood-2010-01-262089
20. Peggs KS, Thomson K, Samuel E, Dyer G, Armoogum J, Chakraverty R, Pang K, Mackinnon S, Lowdell MW. Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virusspecific immunity following stem cell transplantation. Clin Infect Dis. 2011; 52: 49-57. doi: 10.1093/cid/ciq042
21. Icheva V, Kayser S, Wolff D, Tuve S, Kyzirakos C, Bethge W, Greil J, Albert MH, Schwinger W, Nathrath M, Schumm M, Stevanovic S, Handgretinger R, et al. Adoptive transfer of epstein-barr virus (EBV) nuclear antigen 1-specific t cells as treatment for EBV reactivation and lymphoproliferative disorders after allogeneic stemcell transplantation. J Clin Oncol. 2013; 31: 39-48. doi: 10.1200/JCO.2011.39.8495
22. Uhlin M, Okas M, Gertow J, Uzunel M, Brismar TB, Mattsson J. A novel haplo-identical adoptive CTL therapy as a treatment for EBV-associated lymphoma after stem cell transplantation. Cancer Immunol Immunother. 2010; 59: 473-7. doi: 10.1007/s00262-009-0789-1
23. Schmitt A, Tonn T, Busch DH, Grigoleit GU, Einsele H, Odendahl M, Germeroth L, Ringhoffer M, Ringhoffer S, Wiesneth M, Greiner J, Michel D, Mertens T, et al. Adoptive transfer and selective reconstitution of streptamerselected cytomegalovirus-specific CD8+ T cells leads to virus clearance in patients after allogeneic peripheral blood stem cell transplantation. Transfusion. 2011; 51: 591-9. doi: 10.1111/j.1537-2995.2010.02940.x
24. Sasnauskas K, Bulavaite A, Hale A, Jin L, Knowles WA, Gedvilaite A, Dargeviciute A, Bartkeviciute D, Zvirbliene A, Staniulis J, Brown DW, Ulrich R. Generation of recombinant virus-like particles of human and non-human polyomaviruses in yeast Saccharomyces cerevisiae. Intervirology. 2002; 45: 308-17
25. Willinger T, Freeman T, Hasegawa H, McMichael AJ, Callan MF. Molecular signatures distinguish human central memory from effector memory CD8 T cell subsets. J Immunol. 2005; 175: 5895-903
26. Jelcic I, Aly L, Binder TM, Jelcic I, Bofill-Mas S, Planas R, Demina V, Eiermann TH, Weber T, Girones R, Sospedra M, Martin R. T cell epitope mapping of JC polyoma virusencoded proteome reveals reduced T cell responses in HLADRB1* 04:01+ donors. J Virol. 2013; 87: 3393-408. doi: 10.1128/JVI.02803-12
27. Sospedra M, Schippling S, Yousef S, Jelcic I, Bofill-Mas S, Planas R, Stellmann JP, Demina V, Cinque P, Garcea R, Croughs T, Girones R, Martin R. Treating progressive multifocal leukoencephalopathy with interleukin 7 and vaccination with JC virus capsid protein VP1. Clin Infect Dis. 2014; 59: 1588-92. doi: 10.1093/cid/ciu682
28. Hammer MH, Brestrich G, Andree H, Engelmann E, Rosenberger C, Tillmann H, Zwinger S, Babel N, Nickel P, Volk HD, Reinke P. HLA type-independent method to monitor polyoma BK virus-specific CD4 and CD8 T-cell immunity. Am J Transplant. 2006; 6: 625-31. doi: 10.1111/j.1600-6143.2005.01221.x
29. Comoli P, Hirsch HH, Ginevri F. Cellular immune responses to BK virus. Curr Opin Organ Transplant. 2008; 13: 569-74. doi: 10.1097/MOT.0b013e3283186b93
30. Sester M, Leboeuf C, Schmidt T, Hirsch HH. The ABC of virus-specific T-cell immunity in solid organ transplantation. Am J Transplant. 2015. doi: 10.1111/ajt.13684
31. Chang D, Fung CY, Ou WC, Chao PC, Li SY, Wang M, Huang YL, Tzeng TY, Tsai RT. Self-assembly of the JC virus major capsid protein, VP1, expressed in insect cells. J Gen Virol. 1997; 78 ( Pt 6): 1435-9
32. Chen PL, Wang M, Ou WC, Lii CK, Chen LS, Chang D. Disulfide bonds stabilize JC virus capsid-like structure by protecting calcium ions from chelation. FEBS Lett. 2001; 500: 109-13
33. Teunissen EA, de Raad M, Mastrobattista E. Production and biomedical applications of virus-like particles derived from polyomaviruses. J Control Release. 2013; 172: 305-21. doi: 10.1016/j.jconrel.2013.08.026
34. Nicol JT, Touze A, Robinot R, Arnold F, Mazzoni E, Tognon M, Coursaget P. Seroprevalence and cross-reactivity of human polyomavirus 9. Emerg Infect Dis. 2012; 18: 1329-32. doi: 10.3201/eid1808.111625
35. Viscidi RP, Rollison DE, Viscidi E, Clayman B, Rubalcaba E, Daniel R, Major EO, Shah KV. Serological crossreactivities between antibodies to simian virus 40, BK virus, and JC virus assessed by virus-like-particle-based enzyme immunoassays. Clin Diagn Lab Immunol. 2003; 10: 278-85
36. Drake DR, 3rd, Moser JM, Hadley A, Altman JD, Maliszewski C, Butz E, Lukacher AE. Polyomavirus-infected dendritic cells induce antiviral CD8(+) T lymphocytes. J Virol. 2000; 74: 4093-101
37. Li J, Melenhorst J, Hensel N, Rezvani K, Sconocchia G, Kilical Y, Hou J, Curfman B, Major E, Barrett AJ. 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: 2951-60. doi: 10.1099/vir.0.82094-0
38. Koralnik IJ, Du Pasquier RA, Letvin NL. JC virus-specific cytotoxic T lymphocytes in individuals with progressive multifocal leukoencephalopathy. J Virol. 2001; 75: 3483-7. doi: 10.1128/JVI.75.7.3483-3487.2001
39. Tan CS, Broge TA, Jr., Ngo L, Gheuens S, Viscidi R, Bord E, Rosenblatt J, Wong M, Avigan D, Koralnik IJ. Immune reconstitution after allogeneic hematopoietic stem cell transplantation is associated with selective control of JC virus reactivation. Biol Blood Marrow Transplant. 2014; 20: 992-9. doi: 10.1016/j. bbmt.2014.03.018
40. Monaco MC, Major EO. Immune System Involvement in the Pathogenesis of JC Virus Induced PML: What is Learned from Studies of Patients with Underlying Diseases and Therapies as Risk Factors. Front Immunol. 2015; 6:159. doi: 10.3389/fimmu.2015.00159
41. Aly L, Yousef S, Schippling S, Jelcic I, Breiden P, Matschke J, Schulz R, Bofill-Mas S, Jones L, Demina V, Linnebank M, Ogg G, Girones R, et al. Central role of JC virusspecific CD4+ lymphocytes in progressive multi-focal leucoencephalopathy-immune reconstitution inflammatory syndrome. Brain. 2011; 134: 2687-702. doi: 10.1093/brain/awr206
42. van Aalderen MC, Remmerswaal EB, Heutinck KM, ten Brinke A, Pircher H, van Lier RA, ten Berge IJ. Phenotypic and functional characterization of circulating polyomavirus BK VP1-specific CD8+ T cells in healthy adults. J Virol. 2013; 87: 10263-72. doi: 10.1128/JVI.01540-13
43. 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: 640-4. doi: 10.1111/j.1469-0691.2004.00882.x
44. Koralnik IJ, Boden D, Mai VX, Lord CI, Letvin NL. JC virus DNA load in patients with and without progressive multifocal leukoencephalopathy. Neurology. 1999; 52: 253-60
45. Kraemer C, Evers S, Nolting T, Arendt G, Husstedt IW. Cidofovir in combination with HAART and survival in AIDS-associated progressive multifocal leukoencephalopathy. J Neurol. 2008; 255: 526-31. doi: 10.1007/s00415-008-0731-z
46. Du Pasquier RA, Kuroda MJ, Zheng Y, Jean-Jacques J, Letvin NL, Koralnik IJ. A prospective study demonstrates an association between JC virus-specific cytotoxic T lymphocytes and the early control of progressive multifocal leukoencephalopathy. Brain. 2004; 127: 1970-8. doi: 10.1093/brain/awh215
47. Marzocchetti A, Tompkins T, Clifford DB, Gandhi RT, Kesari S, Berger JR, Simpson DM, Prosperi M, De Luca A, Koralnik IJ. Determinants of survival in progressive multifocal leukoencephalopathy. Neurology. 2009; 73: 1551-8. doi: 10.1212/WNL.0b013e3181c0d4a1
48. Sundqvist E, Buck D, Warnke C, Albrecht E, Gieger C, Khademi M, Lima Bomfim I, Fogdell-Hahn A, Link J, Alfredsson L, Sondergaard HB, Hillert J, International Multiple Sclerosis Genetics C, et al. JC polyomavirus infection is strongly controlled by human leucocyte antigen class II variants. PLoS Pathog. 2014; 10: e1004084. doi: 10.1371/journal.ppat.1004084
49. Schalich J, Vytvytska O, Zauner W, Fischer MB, Buschle M, Aichinger G, Klade CS. Analysis of the human cytomegalovirus pp65-directed T-cell response in healthy HLA-A2-positive individuals. Biol Chem. 2008; 389: 551-9
50. Trivedi D, Williams RY, O'Reilly RJ, Koehne G. Generation of CMV-specific T lymphocytes using protein-spanning pools of pp65-derived overlapping pentadecapeptides for adoptive immunotherapy. Blood. 2005; 105: 2793-801. doi: 10.1182/blood-2003-05-1433
51. Homann D, Lewicki H, Brooks D, Eberlein J, Mallet-Designe V, Teyton L, Oldstone MB. Mapping and restriction of a dominant viral CD4+ T cell core epitope by both MHC class I and MHC class II. Virology. 2007; 363: 113-23. doi: 10.1016/j.virol.2006.12.025
52. Wu C, Zanker D, Valkenburg S, Tan B, Kedzierska K, Zou QM, Doherty PC, Chen W. Systematic identification of immunodominant CD8+ T-cell responses to influenza A virus in HLA-A2 individuals. Proc Natl Acad Sci U S A. 2011; 108: 9178-83. doi: 10.1073/pnas.1105624108
53. Slifka MK, Whitton JL. Activated and memory CD8+ T cells can be distinguished by their cytokine profiles and phenotypic markers. J Immunol. 2000; 164: 208-16
54. Lima MA, Marzocchetti A, Autissier P, Tompkins T, Chen Y, Gordon J, Clifford DB, Gandhi RT, Venna N, Berger JR, Koralnik IJ. Frequency and phenotype of JC virus-specific CD8+ T lymphocytes in the peripheral blood of patients with progressive multifocal leukoencephalopathy. J Virol. 2007; 81: 3361-8. doi: 10.1128/JVI.01809-06
55. Barker JN, Doubrovina E, Sauter C, Jaroscak JJ, Perales MA, Doubrovin M, Prockop SE, Koehne G, O'Reilly RJ. Successful treatment of EBV-associated posttransplantation lymphoma after cord blood transplantation using third-party EBV-specific cytotoxic T lymphocytes. Blood. 2010; 116: 5045-9. doi: 10.1182/blood-2010-04-281873
56. Leen AM, Bollard CM, Mendizabal AM, Shpall EJ, Szabolcs P, Antin JH, Kapoor N, Pai SY, Rowley SD, Kebriaei P, Dey BR, Grilley BJ, Gee AP, et al. Multicenter study of banked third-party virus-specific T cells to treat severe viral infections after hematopoietic stem cell transplantation. Blood. 2013; 121: 5113-23. doi: 10.1182/blood-2013-02-486324
57. Yang W, Beaudoin EL, Lu L, Du Pasquier RA, Kuroda MJ, Willemsen RA, Koralnik IJ, Junghans RP. Chimeric immune receptors (CIRs) specific to JC virus for immunotherapy in progressive multifocal leukoencephalopathy (PML). Int Immunol. 2007; 19: 1083-93. doi: 10.1093/intimm/dxm076
58. Jin N, Malcherek G, Mani J, Zurleit R, Schmitt A, Chen B, Freund M, Ho AD, Schmitt M. Suppression of cytomegalovirus-specific CD8(+)T cells by everolimus. Leuk Lymphoma. 2014; 55: 1144-50. doi: 10.3109/10428194.2013.822496
59. Jung T, Schauer U, Heusser C, Neumann C, Rieger C. Detection of intracellular cytokines by flow cytometry. J Immunol Methods. 1993; 159: 197-207
60. Matsumura S, Kita H, He XS, Ansari AA, Lian ZX, Van De Water J, Yamamoto K, Tsuji T, Coppel RL, Kaplan M, Gershwin ME. Comprehensive mapping of HLA-A0201-restricted CD8 T-cell epitopes on PDC-E2 in primary biliary cirrhosis. Hepatology. 2002; 36: 1125-34. doi: 10.1053/jhep.2002.36161
61. Neri S, Mariani E, Meneghetti A, Cattini L, Facchini A. Calcein-acetyoxymethyl cytotoxicity assay: standardization of a method allowing additional analyses on recovered effector cells and supernatants. Clin Diagn Lab Immunol. 2001; 8: 1131-5. doi: 10.1128/CDLI.8.6.1131-1135.2001
62. Dang X, Wuthrich C, Gordon J, Sawa H, Koralnik IJ. JC virus encephalopathy is associated with a novel agnoprotein-deletion JCV variant. PLoS One. 2012; 7: e35793. doi: 10.1371/journal.pone.0035793