Phenotypic and functional characterization of circulating polyomavirus BK VP1-specific CD8+ T cells in healthy adults

Journal of Virology

Volumn 87, Issue 18, 2013, Pages 10263-10272

  van Aalderen, Michiel C ^a,b   Remmerswaal, Ester B M ^a,b   Heutinck, Kirstin M ^a,b   Brinke, Anja ten ^c   Pircher, Hanspeter ^d   van Lier, René A W ^c   Berge, Ineke J M ten ^a,b  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b Renal Transplant Unit   (Netherlands)

^c SANQUIN RESEARCH   (Netherlands)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 INTEGRIN; CD27 ANTIGEN; CD45RA ANTIGEN; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR3; EOMESODERMIN; GAMMA INTERFERON; GRANZYME; GRANZYME B; GRANZYME K; HLA A ANTIGEN; HLA A02 ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 7 RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; NATURAL KILLER CELL LECTIN LIKE RECEPTOR; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY G1; TRANSCRIPTION FACTOR T BET; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BK VIRUS; CD8+ T LYMPHOCYTE; CELL SPECIFICITY; CELLULAR IMMUNITY; COMPLEX FORMATION; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOTOXICITY; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; INFLUENZA VIRUS; LYMPHOCYTE FUNCTION; MEMORY CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADOLESCENT; ADULT; BK VIRUS; BLOOD DONORS; CAPSID PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; IMMUNOPHENOTYPING; MIDDLE AGED; T-LYMPHOCYTE SUBSETS; YOUNG ADULT;

EID: 84883273108     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01540-13     Document Type: Article

References (43)

1. van Aalderen MC, Heutinck KM, Huisman C, Ten Berge IJ. 2012. BK virus infection in transplant recipients: clinical manifestations, treatment options and the immune response. Neth. J. Med. 70:172-183.
2. Schachtner T, Muller K, Stein M, Diezemann C, Sefrin A, Babel N, Reinke P. 2011. BKV-specific immunity kinetics: a predictor of recovery from polyomavirus BK-associated nephropathy. Am. J. Transplant. 11: 2443-2452.
3. Blyth E, Clancy L, Simms R, Gaundar S, O'connell P, Micklethwaite K, Gottlieb DJ. 2011. BK virus-specific T cells for use in cellular therapy show specificity to multiple antigens and polyfunctional cytokine responses. Transplantation 92:1077-1084.
4. Micklethwaite KP, Clancy L, Sandher U, Hansen AM, Blyth E, Antonenas V, Sartor MM, Bradstock KF, Gottlieb DJ. 2008. Prophylactic infusion of cytomegalovirus-specific cytotoxic T lymphocytes stimulated with Ad5f35pp65 gene-modified dendritic cells after allogeneic hemopoietic stem cell transplantation. Blood 112:3974-3981.
5. Appay V, Dunbar PR, Callan M, Klenerman P, Gillespie GM, Papagno L, Ogg GS, King A, Lechner F, Spina CA, Little S, Havlir DV, Richman DD, Gruener N, Pape G, Waters A, Easterbrook P, Salio M, Cerundolo V, McMichael AJ, Rowland-Jones SL. 2002. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8:379-385.
6. van Lier RA, Ten Berge IJ, Gamadia LE. 2003. Human CD8(+) T-cell differentiation in response to viruses. Nat. Rev. Immunol. 3:931-939.
7. Sharma MC, Zhou W, Martinez J, Krymskaya L, Srivastava T, Haq W, Diamond DJ, Lacey SF. 2006. Cross-reactive CTL recognizing two HLAA*02-restricted epitopes within the BK virus and JC virus VP1 polypeptides are frequent in immunocompetent individuals. Virology 350:128-136.
8. Li J, Melenhorst J, Hensel N, Rezvani K, Sconocchia G, Kilical Y, Hou J, Curfman B, Major E, Barrett AJ. 2006. 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. 87:2951-2960.
9. Tagaram HR, Watson AM, Lemonnier FA, Staveley-O'Carroll K, Tevethia SS, Schell TD. 2008. An SV40 VP1-derived epitope recognized by CD8+T cells is naturally processed and presented by HLA-A*0201 and cross-reactive with human polyomavirus determinants. Virology 376: 183-190.
10. Krymskaya L, Sharma MC, Martinez J, Haq W, Huang EC, Limaye AP, Diamond DJ, Lacey SF. 2005. Cross-reactivity of T lymphocytes recognizing a human cytotoxic T-lymphocyte epitope within BK and JC virus VP1 polypeptides. J. Virol. 79:11170-11178.
11. Chen Y, Trofe J, Gordon J, Du Pasquier RA, Roy-Chaudhury P, Kuroda MJ, Woodle ES, Khalili K, Koralnik IJ. 2006. Interplay of cellular and humoral immune responses against BK virus in kidney transplant recipients with polyomavirus nephropathy. J. Virol. 80:3495-3505.
12. Chen Y, Trofe J, Gordon J, Autissier P, Woodle ES, Koralnik IJ. 2008. 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. 42:198-202.
13. Provenzano M, Bracci L, Wyler S, Hudolin T, Sais G, Gosert R, Zajac P, Palu' G, Heberer M, Hirsch HH, Spagnoli GC. 2006. Characterization of highly frequent epitope-specific CD45RA+/CCR7+/γ 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. 4:47.
14. Voehringer D, Koschella M, Pircher H. 2002. Lack of proliferative capacity of human effector and memory T cells expressing killer cell lectinlike receptor G1 (KLRG1). Blood 100:3698-3702.
15. Lamoreaux L, Roederer M, Koup R. 2006. Intracellular cytokine optimization and standard operating procedure. Nat. Protoc. 1:1507-1516.
16. Hamann D, Baars PA, Rep MH, Hooibrink B, Kerkhof-Garde SR, Klein MR, van Lier RA. 1997. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186:1407-1418.
17. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708-712.
18. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4:1191-1198.
19. Vanchiere JA, Abudayyeh S, Copeland CM, Lu LB, Graham DY, Butel JS. 2009. Polyomavirus shedding in the stool of healthy adults. J. Clin. Microbiol. 47:2388-2391.
20. Behzad-Behbahani A, Klapper PE, Vallely PJ, Cleator GM, Bonington A. 2003. BKV-DNA and JCV-DNA in CSF of patients with suspected meningitis or encephalitis. Infection 31:374-378.
21. Robaina TF, Mendes GS, Benati FJ, Pena GA, Silva RC, Montes MA, Janini ME, Camara FP, Santos N. 2013. Shedding of polyomavirus in the saliva of immunocompetent individuals. J. Med. Virol. 85:144-148.
22. Uss E, Rowshani AT, Hooibrink B, Lardy NM, van Lier RA, Ten Berge IJ. 2006. CD103 is a marker for alloantigen-induced regulatory CD8+ T cells. J. Immunol. 177:2775-2783.
23. Ifergan I, Kebir H, Alvarez JI, Marceau G, Bernard M, Bourbonniere L, Poirier J, Duquette P, Talbot PJ, Arbour N, Prat A. 2011. Central nervous system recruitment of effector memory CD8+ T lymphocytes during neuroinflammation is dependent on alpha4 integrin. Brain 134: 3560-3577.
24. Kurachi M, Kurachi J, Suenaga F, Tsukui T, Abe J, Ueha S, Tomura M, Sugihara K, Takamura S, Kakimi K, Matsushima K. 2011. Chemokine receptor CXCR3 facilitates CD8(22) T cell differentiation into short-lived effector cells leading to memory degeneration. J. Exp. Med. 208:1605-1620.
25. Kunkel EJ, Boisvert J, Murphy K, Vierra MA, Genovese MC, Wardlaw AJ, Greenberg HB, Hodge MR, Wu L, Butcher EC, Campbell JJ. 2002. Expression of the chemokine receptors CCR4, CCR5, and CXCR3 by human tissue-infiltrating lymphocytes. Am. J. Pathol. 160:347-355.
26. Guarda G, Hons M, Soriano SF, Huang AY, Polley R, Martin-Fontecha A, Stein JV, Germain RN, Lanzavecchia A, Sallusto F. 2007. L-selectinnegative. Nat. Immunol. 8:743-752.
27. Szabo SJ, Sullivan BM, Stemmann C, Satoskar AR, Sleckman BP, Glimcher LH. 2002. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 295:338-342.
28. Pearce EL, Mullen AC, Martins GA, Krawczyk CM, Hutchins AS, Zediak VP, Banica M, DiCioccio CB, Gross DA, Mao CA, Shen H, Cereb N, Yang SY, Lindsten T, Rossant J, Hunter CA, Reiner SL. 2003. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302:1041-1043.
29. Intlekofer AM, Takemoto N, Wherry EJ, Longworth SA, Northrup JT, Palanivel VR, Mullen AC, Gasink CR, Kaech SM, Miller JD, Gapin L, Ryan K, Russ AP, Lindsten T, Orange JS, Goldrath AW, Ahmed R, Reiner SL. 2005. Effector and memory CD8+T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6:1236-1244.
30. Joshi NS, Cui W, Chandele A, Lee HK, Urso DR, Hagman J, Gapin L, Kaech SM. 2007. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281-295.
31. Takemoto N, Intlekofer AM, Northrup JT, Wherry EJ, Reiner SL. 2006. Cutting edge: IL-12 inversely regulates T-bet and eomesodermin expression during pathogen-induced CD8+ T cell differentiation. J. Immunol. 177:7515-7519.
32. Egli A, Infanti L, Dumoulin A, Buser A, Samaridis J, Stebler C, Gosert R, Hirsch HH. 2009. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J. Infect. Dis. 199:837-846.
33. Kling CL, Wright AT, Katz SE, McClure GB, Gardner JS, Williams JT, Meinerz NM, Garcea RL, Vanchiere JA. 2012. Dynamics of urinary polyomavirus shedding in healthy adult women. J. Med. Virol. 84:1459-1463.
34. Corallini A, Barbanti-Brodano G, Portolani M, Balboni PG, Grossi MP, Possati L, Honorati C, La PM, Mazzoni A, Caputo A, Veronesi U, Orefice S, Cardinali G. 1976. Antibodies to BK virus structural and tumor antigens in human sera from normal persons and from patients with various diseases, including neoplasia. Infect. Immun. 13:1684-1691.
35. Bodaghi S, Comoli P, Bosch R, Azzi A, Gosert R, Leuenberger D, Ginevri F, Hirsch HH. 2009. Antibody responses to recombinant polyomavirus BK large T and VP1 proteins in young kidney transplant patients. J. Clin. Microbiol. 47:2577-2585.
36. Langer-Gould A, Atlas SW, Green AJ, Bollen AW, Pelletier D. 2005. Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. N. Engl. J. Med. 353:375-381.
37. Van Assche G, Van RM, Sciot R, Dubois B, Vermeire S, Noman M, Verbeeck J, Geboes K, Robberecht W, Rutgeerts P. 2005. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease. N. Engl. J. Med. 353:362-368.
38. Naito T, Tanaka H, Naoe Y, Taniuchi I. 2011. Transcriptional control of T-cell development. Int. Immunol. 23:661-668.
39. Kaech SM, Cui W. 2012. Transcriptional control of effector and memory CD8(+) T cell differentiation. Nat. Rev. Immunol. 12:749-761.
40. Banerjee A, Gordon SM, Intlekofer AM, Paley MA, Mooney EC, Lindsten T, Wherry EJ, Reiner SL. 2010. Cutting edge: the transcription factor eomesodermin enables CD8+ T cells to compete for the memory cell niche. J. Immunol. 185:4988-4992.
41. Remmerswaal EB, Havenith SH, Idu MM, van Leeuwen EM, van Donselaar KA, van der Bom-Baylon N, Bemelman FJ, van Lier RA, Ten Berge IJ. 2012. Human virus-specific effector-type T cells accumulate in blood but not in lymph nodes. Blood 119:1702-1712.
42. Piet B, de Bree GJ, Smids-Dierdorp BS, van der Loos CM, Remmerswaal EB, von der Thusen JH, van Haarst JM, Eerenberg JP, BAten van der Bij W, Timens W, van Lier RA, Jonkers RE. 2011. CD8(+) T cells with an intraepithelial phenotype upregulate cytotoxic function upon influenza infection in human lung. J. Clin. Invest. 121:2254-2263.
43. van de Berg PJ, van Leeuwen EM, Ten Berge IJ, van Lier R. 2008. Cytotoxic human CD4(+) T cells. Curr. Opin. Immunol. 20:339-343.