Frequency and phenotype of JC virus-specific CD8+ T lymphocytes in the peripheral blood of patients with progressive multifocal leukoencephalopathy

Journal of Virology

Volumn 81, Issue 7, 2007, Pages 3361-3368

  Lima, Marco A ^a,b   Marzocchetti, Angela ^a   Autissier, Patrick ^a   Tompkins, Troy ^a   Chen, Yiping ^a   Gordon, Jennifer ^c   Clifford, David B ^d   Gandhi, Rajesh T ^e   Venna, Nagagopal ^e   Berger, Joseph R ^f   Koralnik, Igor J ^a,e  

^a HARVARD MEDICAL SCHOOL   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c TEMPLE UNIVERSITY   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; PROTEIN P 36; PROTEIN P100; PROTEIN VP1; TETRAMER; UNCLASSIFIED DRUG; VIRUS DNA;

ACUTE PHASE RESPONSE; ADULT; AGED; ARTICLE; BK VIRUS; BLOOD; BLOOD SAMPLING; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; EFFECTOR CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNOTHERAPY; JC VIRUS; MEMORY CELL; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; POLYOMA VIRUS; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; QUANTITATIVE ANALYSIS; STAINING; STATISTICAL SIGNIFICANCE; URINALYSIS; VIREMIA; VIRUS DETECTION; VIRUS LOAD;

ADULT; AGED; ANTIGENS, CD45; BK VIRUS; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; JC VIRUS; LEUKOCYTE COUNT; LEUKOENCEPHALOPATHY, PROGRESSIVE MULTIFOCAL; MIDDLE AGED; PHENOTYPE; RECEPTORS, CHEMOKINE; TIME FACTORS; VIRAL STRUCTURAL PROTEINS; VIRUS REPLICATION;

BK POLYOMAVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; JC POLYOMAVIRUS;

EID: 33947364338     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01809-06     Document Type: Article

References (38)

1. Antinori, A., A. Ammassari, M. L. Giancola, A. Cingolani, S. Grisetti, R. Murri, L. Alba, B. Ciancio, F. Soldani, D. Larussa, G. Ippolito, and A. De Luca. 2001. Epidemiology and prognosis of AIDS-associated progressive multifocal leukoencephalopathy in the HAART era. J. Neurovirol. 7:323-328.
2. Appay, V., P. R. Dunbar, M. Callan, P. Klenerman, G. M. Gillespie, L. Papagno, G. S. Ogg, A. King, F. Lechner, C. A. Spina, S. Little, D. V. Havlir, D. D. Richman, N. Gruener, G. Pape, A. Waters, P. Easterbrook, M. Salio, V. Cerundolo, A. J. McMichael, and S. L. Rowland-Jones. 2002. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8:379-385.
3. Berger, J. R., and I. J. Koralnik. 2005. Progressive multifocal leukoencephalopathy and natalizumab - unforeseen consequences. N. Engl. J. Med. 353: 414-416.
4. Champagne, P., G. S. Ogg, A. S. King, C. Knabenhans, K. Ellefsen, M. Nobile, V. Appay, G. P. Rizzardi, S. Fleury, M. Lipp, R. Forster, S. Rowland-Jones, R. P. Sekaly, A. J. McMichael, and G. Pantaleo. 2001. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410:106-111.
5. Chen, Y., J. Trofe, J. Gordon, R. A. Du Pasquier, P. Roy-Chaudhury, M. J. Kuroda, E. S. Woodle, K. Khalili, and I. J. Koralnik. 2006. Interplay of cellular and humoral immune responses against BK virus in kidney transplant recipients with polyomavirus nephropathy. J. Virol. 80:3495-3505.
6. Cinque, P., I. J. Koralnik, and D. B. Clifford. 2003. The evolving face of human immunodeficiency virus-related progressive multifocal leukoencephalopathy: defining a consensus terminology. J. Neurovirol. 9(Suppl. 1):88-92.
7. Du Pasquier, R. A., P. Autissier, Y. Zheng, J. Jean-Jacques, and I. J. Koralnik. 2005. Presence of JC virus-specific CTL in the cerebrospinal fluid of PML patients: rationale for immune-based therapeutic strategies. AIDS 19:2069-2076.
8. p36 in patients with proven or possible progressive multifocal leukoencephalopathy. J. Virol. 77:11918-11926.
9. Du Pasquier, R. A., M. J. Kuroda, Y. Zheng, J. Jean-Jacques, N. L. Letvin, and I. J. Koralnik. 2004. A prospective study demonstrates an association between JC virus-specific cytotoxic T lymphocytes and the early control of progressive multifocal leukoencephalopathy. Brain 127:1970-1978.
10. Du Pasquier, R. A., J. E. Schmitz, J. Jean-Jacques, Y. Zheng, J. Gordon, K. Khalili, N. L. Letvin, and I. J. Koralnik. 2004. Detection of JC virus-specific cytotoxic T lymphocytes in healthy individuals. J. Virol. 78:10206-10210.
11. Elphick, G. F., W. Querbes, J. A. Jordan, G. V. Gee, S. Eash, K. Manley, A. Dugan, M. Stanifer, A. Bhatnagar, W. K. Kroeze, B. L. Roth, and W. J. Atwood. 2004. The human polyomavirus, JCV, uses serotonin receptors to infect cells. Science 306:1380-1383.
12. Garcia-Suarez, J., D. de Miguel, I. Krsnik, H. Banas, I. Arribas, and C. Burgaleta. 2005. Changes in the natural history of progressive multifocal leukoencephalopathy in HIV-negative lymphoproliferative disorders: impact of novel therapies. Am. J. Hematol. 80:271-281.
13. Geginat, J., A. Lanzavecchia, and F. Sallusto. 2003. Proliferation and differentiation potential of human CD8+ memory T-cell subsets in response to antigen or homeostatic cytokines. Blood 101:4260-4266.
14. Gray, C. M., J. Lawrence, J. M. Schapiro, J. D. Altman, M. A. Winters, M. Crompton, M. Loi, S. K. Kundu, M. M. Davis, and T. C. Merigan. 1999. Frequency of class I HLA-restricted anti-HIV CD8+ T cells in individuals receiving highly active antiretroviral therapy (HAART). J. Immunol. 162: 1780-1788.
15. Hauser, S. L., and H. L. Weiner. 2006. Natalizumab: immune effects and implications for therapy. Ann. Neurol. 59:731-732.
16. Kleinschmidt-DeMasters, B. K., and K. L. Tyler. 2005. Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N. Engl. J. Med. 353:369-374.
17. Koralnik, I. J. 2006. Progressive multifocal leukoencephalopathy revisited: has the disease outgrown its name? Ann. Neurol. 60:162-173.
18. Koralnik, I. J., D. Boden, V. X. Mai, C. I. Lord, and N. L. Letvin. 1999. JC virus DNA load in patients with and without progressive multifocal leukoencephalopathy. Neurology 52:253-260.
19. Koralnik, I. J., R. A. Du Pasquier, M. J. Kuroda, J. E. Schmitz, X. Dang, Y. Zheng, M. Lifton, and N. L. Letvin. 2002. 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. 168:499-504.
20. Krymskaya, L., M. C. Sharma, J. Martinez, W. Haq, E. C. Huang, A. P. Limaye, D. J. Diamond, and S. F. Lacey. 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.
21. Langer-Gould, A., S. W. Atlas, A. J. Green, A. W. Bollen, and D. Pelletier. 2005. Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. N. Engl. J. Med. 353:375-381.
22. Reference deleted.
23. Miller, N. R., E. O. Major, and W. C. Wallen. 1983. Transfection of human fetal glial cells with molecularly cloned JCV DNA. Prog. Clin. Biol. Res. 105:29-40.
24. Niino, M., C. Bodner, M. L. Simard, S. Alatab, D. Gano, H. J. Kim, M. Trigueiro, D. Racicot, C. Guerette, J. P. Antel, A. Fournier, F. Grand'maison, and A. Bar-Or. 2006. Natalizumab effects on immune cell responses in multiple sclerosis. Ann. Neurol. 59:748-754.
25. Polo, C., J. L. Perez, A. Mielnichuck, C. G. Fedele, J. Niubo, and A. Tenorio. 2004. Prevalence and patterns of polyomavirus urinary excretion in immunocompetent adults and children. Clin. Microbiol. Infect. 10:640-644.
26. Power, C., J. G. Gladden, W. Halliday, M. R. Del Bigio, A. Nath, W. Ni, E. O. Major, J. Blanchard, and M. Mowat. 2000. AIDS- and non-AIDS-related PML association with distinct p53 polymorphism. Neurology 54:743-746.
27. Rice, G. P., H. P. Hartung, and P. A. Calabresi. 2005. Anti-alpha4 integrin therapy for multiple sclerosis: mechanisms and rationale. Neurology 64: 1336-1342.
28. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22:745-763.
29. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708-712.
30. Sharma, M. C., W. Zhou, J. Martinez, L. Krymskaya, T. Srivastava, W. Haq, D. J. Diamond, and S. F. Lacey. 2006. 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 350: 128-136.
31. Singhal, S., J. C. Shaw, J. Ainsworth, M. Hathaway, G. M. Gillespie, H. Paris, K. Ward, D. Pillay, P. A. Moss, and D. J. Mutimer. 2000. Direct visualization and quantitation of cytomegalovirus-specific CD8+ cytotoxic T-lymphocytes in liver transplant patients. Transplantation 69:2251-2259.
32. Tan, L. C., N. Gudgeon, N. E. Annels, P. Hansasuta, C. A. O'Callaghan, S. Rowland-Jones, A. J. McMichael, A. B. Rickinson, and M. F. Callan. 1999. A re-evaluation of the frequency of CD8+ T cells specific for EBV in healthy virus carriers. J. Immunol. 162:1827-1835.
33. Van Assche, G., M. Van Ranst, R. Sciot, B. Dubois, S. Vermeire, M. Noman, J. Verbeeck, K. Geboes, W. Robberecht, and P. Rutgeerts. 2005. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease. N. Engl. J. Med. 353:362-368.
34. van Lier, R. A., I. J. ten Berge, and L. E. Gamadia. 2003. Human CD8(+) T-cell differentiation in response to viruses. Nat. Rev. Immunol. 3:931-939.
35. Weber, T., C. Trebst, S. Frye, P. Cinque, L. Vago, C. J. Sindic, W. J. Schulz-Schaeffer, H. A. Kretzschmar, W. Enzensberger, G. Hunsmann, and W. Luke. 1997. Analysis of the systemic and intrathecal humoral immune response in progressive multifocal leukoencephalopathy. J. Infect. Dis. 176: 250-254.
36. Weber, T., F. Weber, H. Petry, and W. Luke. 2001. Immune response in progressive multifocal leukoencephalopathy: an overview. J. Neurovirol. 7:311-317.
37. Wherry, E. J., and R. Ahmed. 2004. Memory CD8 T-cell differentiation during viral infection. J. Virol. 78:5535-5545.
38. Wuthrich, C., S. Kesari, W. K. Kim, K. Williams, R. Gelman, D. Elmeric, U. De Girolami, J. T. Joseph, T. Hedley-Whyte, and I. J. Koralnik. 2006. Characterization of lymphocytic infiltrates in progressive multifocal leukoencephalopathy: co-localization of CD8(+) T cells with JCV-infected glial cells. J. Neurovirol. 12:116-128.