Comparisons of CD8 + T cells specific for human immunodeficiency virus, hepatitis C virus, and cytomegalovirus reveal differences in frequency, immunodominance, phenotype, and interleukin-2 responsiveness

Journal of Virology

Volumn 83, Issue 6, 2009, Pages 2728-2742

  Jagannathan, Prasanna ^a   Osborne, Christine M ^a   Royce, Cassandra ^a   Manion, Maura M ^a   Tilton, John C ^a   Li, Li ^b   Fischer, Steven ^b   Hallahan, Claire W ^a   Metcalf, Julia A ^a   McLaughlin, Mary ^a   Pipeling, Matthew ^c   McDyer, John F ^c   Manley, Thomas J ^d   Meier, Jeffery L ^e   Altman, John D ^f   Hertel, Laura ^g   Davey Jr , Richard T ^a   Connors, Mark ^a,b   Migueles, Stephen A ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

^e UNIVERSITY OF IOWA   (United States)

^f EMORY UNIVERSITY   (United States)

^g UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CD45RA ANTIGEN; CD45RO ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR7; CYTOMEGALOVIRUS ANTIGEN PP65; EPITOPE; GAG PROTEIN; GAMMA INTERFERON; HLA B57 ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; INTERLEUKIN 2; CD45 ANTIGEN; HLA B ANTIGEN; HLA B*5701 ANTIGEN, HUMAN; HLA-B*5701 ANTIGEN, HUMAN;

ARTICLE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOMEGALOVIRUS; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE RESPONSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VIREMIA; VIRUS INFECTION; CHEMISTRY; CYTOMEGALOVIRUS INFECTION; HEPATITIS C; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY;

CYTOMEGALOVIRUS; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS;

ANTIGENS, CD27; ANTIGENS, CD45; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; HEPACIVIRUS; HEPATITIS C; HIV; HIV INFECTIONS; HIV LONG-TERM SURVIVORS; HLA-B ANTIGENS; HUMANS; INTERLEUKIN-2;

EID: 62749134469     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02128-08     Document Type: Article

References (75)

1. Abrams, D. I., J. D. Bebchuk, E. T. Denning, R. T. Davey, L. Fox, H. C. Lane, J. Sampson, R. Verheggen, D. Zeh, and N. P. Markowitz. 2002. Randomized, open-label study of the impact of two doses of subcutaneous recombinant interleukin-2 on viral burden in patients with HIV-1 infection and CD4+ cell counts of > or = 300/mm3: CPCRA 059. J. Acquir. Immune Defic. Syndr. 29:221-231.
2. Accapezzato, D., V. Francavilla, M. Paroli, M. Casciaro, L. V. Chircu, A. Cividini, S. Abrignani, M. U. Mondelli, and V. Barnaba. 2004. Hepatic expansion of a virus-specific regulatory CD8(+) T cell population in chronic hepatitis C virus infection. J. Clin. Investig. 113:963-972.
3. Alatrakchi, N., V. Di Martino, V. Thibault, and B. Autran. 2002. Strong CD4 Th1 responses to HIV and hepatitis C virus in HIV-infected long-term non-progressors co-infected with hepatitis C virus. AIDS 16:713-717.
4. 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.
5. Arrode, G., J. S. Finke, H. Zebroski, F. P. Siegal, and R. M. Steinman. 2005. CD8+ T cells from most HIV-1-infected patients, even when challenged with mature dendritic cells, lack functional recall memory to HIV gag but not other viruses. Eur. J. Immunol. 35:159-170.
6. Bunce, M, C. M. O'Neill, M. C. Barnardo, P. Krausa, M. J. Browning, P. J. Morris, and K. I. Welsh. 1995. Phototyping: comprehensive DNA typing for HLA-A. B, C, DRB1, DRB3, DRB4, DRB5 & DQB1 by PCR with 144 primer mixes utilizing sequence-specific primers (PCR-SSP). Tissue Antigens 46:355-367.
7. Callan, M. F., L. Tan, N. Annels, G. S. Ogg, J. D. Wilson, C. A. O'Callaghan, N. Steven, A. J. McMichael, and A. B. Rickinson. 1998. Direct visualization of antigen-specific CD8+ T cells during the primary immune response to Epstein-Barr virus In vivo. J. Exp. Med. 187:1395-1402.
8. 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 CDS T lymphocytes. Nature 410:106-111.
9. Cortez, K. J., S. H. Fischer, G. A. Fahle, L. B. Calhoun, R. W. Childs, A. J. Barrett, and J. E. Bennett. 2003. Clinical trial of quantitative real-time polymerase chain reaction for detection of cytomegalovirus in peripheral blood of allogeneic hematopoietic stem-cell transplant recipients. J. Infect. Dis. 188:967-972.
10. Davey, R. T., Jr., R. L. Murphy, F. M. Graziano, S. L. Boswell, A. T. Pavia, M. Cancio, J. P. Nadler, D. G. Chaitt, R. L. Dewar, D. K. Sahner, A. M. Duliege, W. B. Capra, W. P. Leong, M. A. Giedlin, H. C. Lane, and J. O. Kahn. 2000. Immunologic and virologic effects of subcutaneous interleukin 2 in combination with antiretroviral therapy: a randomized controlled trial. JAMA 284:183-189.
11. *0201 restricted peptide-based vaccine against human cytomegalovirus infection. Blood 90:1751-1767.
12. Diepolder, H. M., R. Zachoval, R. M. Hoffmann, E. A. Wierenga, T. San-tantonio, M. C. Jung, D. Eichenlaub, and G. R. Pape. 1995. Possible mechanism involving T-lymphocyte response to non-structural protein 3 in viral clearance in acute hepatitis C virus infection. Lancet 346:1006-1007.
13. +-T-cell responses to human cytomegalovirus reveals broad and multispecific reactivities in healthy virus carriers. J. Virol. 77:5226-5240.
14. Ellefsen, K., A. Harari, P. Champagne, P. A. Bart, R. P. Sekaly, and G. Pantaleo. 2002. Distribution and functional analysis of memory antiviral CDS T cell responses in HIV-1 and cytomegalovirus infections. Eur. J. Immunol. 32:3756-3764.
15. Emery, V. C. 2001. Investigation of CMV disease in immunocompromised patients. J. Clin. Pathol. 54:84-88.
16. Faint, J. M, N. E. Annels, S. J. Curnow, P. Shields, D. Pilling, A. D. Hislop, L. Wu, A. N. Akbar, C. D. Buckley, P. A. Moss, D. H. Adams, A. B. Rickinson, and M. Salmon. 2001. Memory T cells constitute a subset of the human CD8+CD45RA+ pool with distinct phenotypic and migratory characteristics. J. Immunol. 167:212-220.
17. Gavin, M. A., M. J. Gilbert, S. R. Riddell, P. D. Greenberg, and M. J. Bevan. 1993. Alkali hydrolysis of recombinant proteins allows for the rapid identification of class I MHC-restricted CTL epitopes. J. Immunol. 151:3971-3980.
18. Gerna, G., E. Percivalle, D. Lilleri, L. Lozza, C. Fornara, G. Hahn, F. Baldanti, and M. G. Revello. 2005. Dendritic-cell infection by human cytomegalovirus is restricted to strains carrying functional UL131-128 genes and mediates efficient viral antigen presentation to CD8+ T cells. J. Gen. Virol. 86:275-284.
19. Goulder, P. J., M. Bunce, P. Krausa, K. Mclntyre, S. Crowley, B. Morgan, A. Edwards, P. Giangrande, R. E. Phillips, and A. J. McMichael. 1996. Novel, cross-restricted, conserved, and immunodominant cytotoxic T lymphocyte epitopes in slow progressors in HIV type 1 infection. AIDS Res. Hum. Retrovir. 12:1691-1698.
20. Grakoui, A., N. H. Shoukry, D. J. Woollard, J. H. Han, H. L. Hanson, J. Ghrayeb, K. K. Murthy, C. M. Rice, and C. M. Walker. 2003. HCV persistence and immune evasion in the absence of memory T cell help. Science 302:659-662.
21. Grigoleit, U., S. Riegler, H. Einsele, K. Laib Sampaio, G. Jahn, H. Hebart, P. Brossart, F. Frank, and C. Sinzger. 2002. Human cytomegalovirus induces a direct inhibitory effect on antigen presentation by monocyte-derived immature dendritic cells. Br. J. Haematol. 119:189-198.
22. He, X. S, B. Rehermann, F. X. Lopez-Labrador, J. Boisvert, R. Cheung, J. Mumm, H. Wedemeyer, M. Berenguer, T. L. Wright, M. M. Davis, and H. B. Greenberg. 1999. Quantitative analysis of hepatitis C virus-specific CD8(+) T cells in peripheral blood and liver using peptide-MHC tetramers. Proc. Natl. Acad. Sci. USA 96:5692-5697.
23. Hertel, L., V. G. Lacaille, H. Strobl, E. D. Mellins, and E. S. Mocarski. 2003. Susceptibility of immature and mature Langerhans cell-type dendritic cells to infection and immunomodulation by human cytomegalovirus. J. Virol. 77: 7563-7574.
24. Hislop, A. D., N. H. Gudgeon, M. F. Callan, C. Fazou, H. Hasegawa, M. Salmon, and A. B. Rickinson. 2001. EBV-specific CD8+ T cell memory: relationships between epitope specificity, cell phenotype, and immediate effector function. J. Immunol. 167:2019-2029.
25. Holl, V., M. Peressin, S. Schmidt, T. Decoville, S. Zolla-Pazner, A. M. Aubertin, and C. Moog. 2006. Efficient inhibition of HIV-1 replication in human immature monocyte-derived dendritic cells by purified anti-HIV-1 IgG without induction of maturation. Blood 107:4466-4474.
26. Holmes, K., B. Fowlkes, I. Schmid, and J. Giorgi. 1995. Preparation of cells and reagents for flow cytometry, p. 5.3.1-5.3.23. In J. Coligan, A. Kruisbeek, D. Margulies, E. Sheevac, and W. Strober (ed.), Current protocols in immunology, vol. 1. Green Publishing Associates, New York, NY.
27. Horton, H., I. Frank, R. Baydo, E. Jalbert, J. Penn, S. Wilson, J. P. McNevin, M. D. McSweyn, D. Lee, Y. Huang, S. C. De Rosa, and M. J. McElrath. 2006. Preservation of T cell proliferation restricted by protective HLA alleles is critical for immune control of HIV-1 infection. J. Immunol. 177:7406-7415.
28. + T cells is associated with diminished interleukin-2 (IL-2) production and is recovered by exogenous IL-2. J. Virol. 77:10900-10909.
29. Karlsson, A. C., J. N. Martin, S. R. Younger, B. M. Bredt, L. Epling, R. Ronquillo, A. Varma, S. G. Deeks, J. M. McCune, D. F. Nixon, and E. Sinclair. 2003. Comparison of the ELISPOT and cytokine flow cytometry assays for the enumeration of antigen-specific T cells. J. Immunol. Methods 283:141-153.
30. Kaslow, R. A., C. Rivers, J. Tang, T. J. Bender, P. A. Goepfert, R. El Habib, K. Weinhold, and M. J. Mulligan. 2001. Polymorphisms in HLA class I genes associated with both favorable prognosis of human immunodeficiency virus (HIV) type 1 infection and positive cytotoxic T-lymphocyte responses to ALVAC-HIV recombinant canarypox vaccines. J. Virol. 75:8681-8689.
31. Kern, F., T. Bunde, N. Faulhaber, F. Kiecker, E. Khatamzas, I. M. Rudaw-ski, A. Pruss, J. W. Gratama, R. Volkmer-Engert, R. Ewert, P. Reinke, H. D. Volk, and L. J. Picker. 2002. Cytomegalovirus (CMV) phosphoprotein 65 makes a large contribution to shaping the T cell repertoire in CMV-exposed individuals. J. Infect. Dis. 185:1709-1716.
32. +-T-cell response to human cytomegalovirus: the 72-kilodalton major immediate-early protein revisited. J. Virol. 73:8179-8184.
33. Khan, N, M. Cobbold, R. Keenan, and P. A. Moss. 2002. Comparative analysis of CD8+ T cell responses against human cytomegalovirus proteins pp65 and immediate early 1 shows similarities in precursor frequency, oligoclonality, and phenotype. J. Infect. Dis. 185:1025-1034.
34. Kiecker, F., M. Streitz, B. Ay, G. Cherepnev, H. D. Volk, R. Volkmer-Engert, and F. Kern. 2004. Analysis of antigen-specific T-cell responses with synthetic peptides - what kind of peptide for which purpose? Hum. Immunol. 65:523-536.
35. Kondo, E., Y. Akatsuka, K. Kuzushima, K. Tsujimura, S. Asakura, K. Ta-jima, Y. Kagami, Y. Kodera, M. Tanimoto, Y. Morishima, and T. Takahashi. 2004. Identification of novel CTL epitopes of CMV-pp65 presented by a variety of HLA alleles. Blood 103:630-638.
36. Large, M. K., D. J. Kittlesen, and Y. S. Hahn. 1999. Suppression of host immune response by the core protein of hepatitis C virus: possible implications for hepatitis C virus persistence. J. Immunol. 162:931-938.
37. Lasarte, J. J., M. Garcia-Granero, A. Lopez, N. Casares, N. Garcia, M. P. Civeira, F. Borras-Cuesta, and J. Prieto. 1998. Cellular immunity to hepatitis C virus core protein and the response to interferon in patients with chronic hepatitis C. Hepatology 28:815-822.
38. Lauer, G. M., T. N. Nguyen, C. L. Day, G. K. Robbins, T. Flynn, K. McGowan, E. S. Rosenberg, M. Lucas, P. Klenerman, R. T. Chung, and B. D. Walker. 2002. Human immunodeficiency virus type 1-hepatitis C virus coin-fection: intraindividual comparison of cellular immune responses against two persistent viruses. J. Virol. 76:2817-2826.
39. +-T-cell responses against hepatitis C virus reveals multiple unpredicted specificities. J. Virol. 76:6104-6113.
40. Lechner, F., D. K. Wong, P. R. Dunbar, R. Chapman, R. T. Chung, P. Dohrenwend, G. Robbins, R. Phillips, P. Klenerman, and B. D. Walker. 2000. Analysis of successful immune responses in persons infected with hepatitis C virus. J. Exp. Med. 191:1499-1512.
41. Lichterfeld, M., D. E. Kaufmann, X. G. Yu, S. K. Mui, M. M. Addo, M. N. Johnston, D. Cohen, G. K. Robbins, E. Pae, G. Alter, A. Wurcel, D. Stone, E. S. Rosenberg, B. D. Walker, and M. Altfeld. 2004. Loss of HIV-l-specific CD8+ T cell proliferation after acute HIV-1 infection and restoration by vaccine-induced HIV-1-specific CD4+ T cells. J. Exp. Med. 200:701-712.
42. Lichterfeld, M., G. Pantaleo, and M. Altfeld. 2005. Loss of HIV-1-specific T cell proliferation in chronic HIV-1 infection: cause or consequence of viral replication? AIDS 19:1225-1227.
43. Limmer, A., J. Ohl, C. Kurts, H. G. Ljunggren, Y. Reiss, M. Groettrup, F. Momburg, B. Arnold, and P. A. Knolle. 2000. Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat. Med. 6:1348-1354.
44. Longmate, J., J. York, C. La Rosa, R. Krishnan, M. Zhang, D. Senitzer, and D. J. Diamond. 2001. Population coverage by HLA class-I restricted cyto-toxic T-lymphocyte epitopes. Immunogenetics 52:165-173.
45. Lore, K., A. Smed-Sorensen, J. Vasudevan, J. R. Mascola, and R. A. Koup. 2005. Myeloid and plasmacytoid dendritic cells transfer HIV-1 preferentially to antigen-specific CD4+ T cells. J. Exp. Med. 201:2023-2033.
46. Mandelboim, O., H. T. Reyburn, M. Vales-Gomez, L. Pazmany, M. Colonna, G. Borsellino, and J. L. Strominger. 1996. Protection from lysis by natural killer cells of group 1 and 2 specificity is mediated by residue 80 in human histocompatibility leukocyte antigen C alleles and also occurs with empty major histocompatibility complex molecules. J. Exp. Med. 184:913-922.
47. Martin, M. P., X. Gao, J. H. Lee, G. W. Nelson, R. Detels, J. J. Goedert, S. Buchbinder, K. Hoots, D. Vlahov, J. Trowsdale, M. Wilson, S. J. O'Brien, and M. Carrington. 2002. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat. Genet. 31:429-434.
48. Migueles, S. A., and M. Connors. 2001. Frequency and function of HIV-specific CD8(+) T cells. Immunol. Lett. 79:141-150.
49. Migueles, S. A., A. C. Laborico, W. L. Shupert, M. S. Sabbaghian, R. Rabin, C. W. Hallahan, D. Van Baarle, S. Kostense, F. Miedema, M. McLaughlin, L. Ehler, J. Metcalf, S. Liu, and M. Connors. 2002. HIV-specific CD8+ T cell proliferation is coupled to perform expression and is maintained in nonprogressors. Nat. Immunol. 3:1061-1068.
50. *5701 is highly associated with restriction of virus replication in a subgroup of HIV-infected long term nonprogressors. Proc. Natl. Acad. Sci. USA 97:2709-2714.
51. Migueles, S. A., J. C. Tilton, and M. Connors. 2004. Advances in understanding immunologic control of HIV infection. Curr. HIV/AIDS Rep. 1:12-17.
52. Moutaftsi, M., A. M. Mehl, L. K. Borysiewicz, and Z. Tabi. 2002. Human cytomegalovirus inhibits maturation and impairs function of monocyte-de-rived dendritic cells. Blood 99:2913-2921.
53. Nastke, M. D., L. Herrgen, S. Walter, D. Wernet, H. G. Rammensee, and S. Stevanovic. 2005. Major contribution of codominant CDS and CD4 T cell epitopes to the human cytomegalovirus-specific T cell repertoire. Cell. Mol. Life Sci. 62:77-86.
54. Papagno, L., V. Appay, J. Sutton, T. Rostron, G. M. Gillespie, G. S. Ogg, A. King, A. T. Makadzanhge, A. Waters, C. Balotta, A. Vyakarnam, P. J. Easterbrook, and S. L. Rowland-Jones. 2002. Comparison between HIV-and CMV-specific T cell responses in long-term HIV infected donors. Clin. Exp. Immunol. 130:509-517.
55. Ravkov, E. V., C. M. Myrick, and J. D. Altaian. 2003. Immediate early effector functions of virus-specific CD8+CCR7+ memory cells in humans defined by HLA and CC chemokine ligand 19 tetramers. J. Immunol. 170: 2461-2468.
56. Reddehase, M. J. 2002. Antigens and immunoevasins: opponents in cytomegalovirus immune surveillance. Nat. Rev. Immunol. 2:831-844.
57. Retiere, C., V. Prod'homme, B. M. Imbert-Marcille, M. Bonneville, H. Vie, and M. M. Hallet. 2000. Generation of cytomegalovirus-specific human T-lymphocyte clones by using autologous B-lymphoblastoid cells with stable expression of pp65 or IE1 proteins: a tool to study the fine specificity of the antiviral response. J. Virol. 74:3948-3952.
58. Riegler, S., H. Hebart, H. Einsele, P. Brossart, G. Jahn, and C. Sinzger. 2000. Monocyte-derived dendritic cells are permissive to the complete rep-licative cycle of human cytomegalovirus. J. Gen. Virol. 81:393-399.
59. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179:1109-1118.
60. Sandberg, J. K., N. M. Fast, and D. F. Nixon. 2001. Functional heterogeneity of cytokines and cytolytic effector molecules in human CD8+ T lymphocytes. J. Immunol. 167:181-187.
61. Shoukry, N. H., A. Grakoui, M. Houghton, D. Y. Chien, J. Ghrayeb, K. A. Reimann, and C. M. Walker. 2003. Memory CD8+ T cells are required for protection from persistent hepatitis C virus infection. J. Exp. Med. 197:1645-1655.
62. + T cells during primary human immunodeficiency virus type 1 infection in individuals expressing protective HLA class I alleles. J. Virol. 81:7725-7731.
63. Sylwester, A. W., B. L. Mitchell, J. B. Edgar, C. Taormina, C. Pelte, F. Ruchti, P. R. Sleath, K. H. Grabstein, N. A. Hosken, F. Kern, J. A. Nelson, and L. J. Picker. 2005. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 202:673-685.
64. Takaki, A., M. Wiese, G. Maertens, E. Depla, U. Seifert, A. Liebetrau, J. L. Miller, M. P. Manns, and B. Rehermann. 2000. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat. Med. 6:578-582.
65. Thimme, R., D. Oldach, K. M. Chang, C. Steiger, S. C. Ray, and F. V. Chisari. 2001. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J. Exp. Med. 194:1395-1406.
66. + T cells are a consequence of antigen load. J. Virol. 81:2713-2725.
67. Unsoeld, H., S. Krautwald, D. Voehringer, U. Kunzendorf, and H. Pircher. 2002. Cutting edge: CCR7+ and CCR7- memory T cells do not differ in immediate effector cell function. J. Immunol. 169:638-641.
68. Valdez, H., N. L. Carlson, A. B. Post, R. Asaad, P. S. Heeger, M. M. Lederman, P. V. Lehmann, and D. D. Anthony. 2002. HIV long-term nonprogressors maintain brisk CDS T cell responses to other viral antigens. AIDS 16:1113-1118.
69. van Leeuwen, E. M., L. E. Gamadia, P. A. Baars, E. B. Remmerswaal, I. J. ten Berge, and R. A. van Lier. 2002. Proliferation requirements of cytomegalovirus-specific, effector-type human CD8+ T cells. J. Immunol. 169:5838-5843.
70. Wedemeyer, H., X. S. He, M. Nascimbeni, A. R. Davis, H. B. Greenberg, J. H. Hoofnagle, T. J. Liang, H. Alter, and B. Rehermann. 2002. Impaired effector function of hepatitis C virus-specific CD8+ T cells in chronic hepatitis C virus infection. J. Immunol. 169:3447-3458.
71. Weekes, M. P., M. R. Wills, K. Mynard, A. J. Carmichael, and J. G. Sissons. 1999. The memory cytotoxic T-lymphocyte (CTL) response to human cytomegalovirus infection contains individual peptide-specific CTL clones that have undergone extensive expansion in vivo. J. Virol. 73:2099-2108.
72. Wills, M. R., A. J. Carmichael, K. Mynard, X. Jin, M. P. Weekes, B. Plachter, and J. G. Sissons. 1996. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J. Virol. 70:7569-7579.
73. Wills, M. R., A. J. Carmichael, M. P. Weekes, K. Mynard, G. Okecha, R. Hicks, and J. G. Sissons. 1999. Human virus-specific CD8+ CTL clones revert from CD45ROhigh to CD45RAhigh in vivo: CD45RAhighCD8+ T cells comprise both naive and memory cells. J. Immunol. 162:7080-7087.
74. Wills, M. R., G. Okecha, M. P. Weekes, M. K. Gandhi, P. J. Sissons, and A. J. Carmichael. 2002. Identification of naive or antigen-experienced human CD8(+) T cells by expression of costimulation and chemokine receptors: analysis of the human cytomegalovirus-specific CD8(+) T cell response. J. Immunol. 168:5455-5464.
75. Zimmerli, S. C., A. Harari, C. Cellerai, F. Vallelian, P. A. Bart, and G. Pantaleo. 2005. HIV-1-specific IFN-gamma/IL-2-secreting CDS T cells support C D4-independent proliferation of HIV-1-specific CDS T cells. Proc. Natl. Acad. Sci. USA 102:7239-7244.