Cytolytic CD4+ T cells in viral immunity

Expert Review of Vaccines

Volumn 9, Issue 12, 2010, Pages 1453-1463

  Soghoian, Damien Z ^a   Streeck, Hendrik ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

cytolytic CD4+ T cells; HIV; vaccines; viral infection

Indexed keywords

CD11B ANTIGEN; CD57 ANTIGEN; CHEMOKINE RECEPTOR CCR7; DNA VACCINE; GRANZYME A; HLA ANTIGEN CLASS 1; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 13; INTERLEUKIN 4; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DS2; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; LYMPHOCYTE RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NATURAL KILLER CELL RECEPTOR NKG2D; RECOMBINANT GP160 SUBUNIT VACCINE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL TRIAL; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DRUG DESIGN; EFFECTOR CELL; EPSTEIN BARR VIRUS; HELPER CELL; HEPATITIS C VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IMMUNOSTIMULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; T FOLLICULAR HELPER CELL; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; TH2 CELL; TH21 CELL; TH9 CELL; VIRUS IMMUNITY; VIRUS INFECTION; VIRUS REPLICATION; WEST NILE FLAVIVIRUS;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; HIV INFECTIONS; HUMANS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC; VIRUS DISEASES;

EID: 78649510318     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.10.132     Document Type: Review

References (119)

1. Claman HN, Chaperon EA. Immunologic complementation between thymus and marrow cells-a model for the two-cell theory of immunocompetence. Transplant Rev. 1, 92-113 (1969).
2. Geha RS, Schneeberger E, Rosen FS, Merler E. Interaction of human thymus-derived and non-thymus-derived lymphocytes in vitro. Induction of proliferation and antibody synthesis in B lymphocytes by a soluble factor released from antigen-stimulated T lymphocytes. J. Exp. Med. 138(5), 1230-1247 (1973).
3. Reinherz EL, Schlossman SF. The differentiation and function of human T lymphocytes. Cell 19(4), 821-827 (1980).
4. Reinherz EL, Kung PC, Goldstein G, Schlossman SF. Separation of functional subsets of human T cells by a monoclonal antibody. Proc. Natl Acad. Sci. USA 76(8), 4061-4065 (1979).
5. Feighery C, Stastny P. HLA-D region-associated determinants serve as targets for human cell-mediated lysis. J. Exp. Med. 149(2), 485-494 (1979).
6. + effector T cells recognize products of different major histocompatibility complex regions. Proc. Natl Acad. Sci. USA 79(14), 4395-4399 (1982).
7. +. Proc. Natl Acad. Sci. USA 79(7), 2365-2369 (1982).
8. + T lymphocytes in culture. Nature 308(5957), 365-367 (1984).
9. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Defnition according to profles of lymphokine activities and secreted proteins. J. Immunol. 136(7), 2348-2357 (1986).
10. + T cells. Nature 417(6884), 95-98 (2002).
11. Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations. Annu. Rev. Immunol. 28, 445-489 (2010).
12. Szabo SJ, Sullivan BM, Peng SL, Glimcher LH. Molecular mechanisms regulating Th1 immune responses. Annu. Rev. Immunol. 21, 713-758 (2003).
13. Paul WE, Zhu J. How are T(H)2-type immune responses initiated and amplifed? Nat. Rev. Immunol. 10(4), 225-235 (2010).
14. Fazilleau N, Mark L, McHeyzer-Williams LJ, McHeyzer-Williams MG. Follicular helper T cells: lineage and location. Immunity 30(3), 324-335 (2009).
15. King C, Tangye SG, Mackay CR. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu. Rev. Immunol. 26, 741-766 (2008).
16. Yi JS, Du M, Zajac AJ. A vital role for interleukin-21 in the control of a chronic viral infection. Science 324(5934), 1572-1576 (2009).
17. Elsaesser H, Sauer K, Brooks DG. IL-21 is required to control chronic viral infection. Science 324(5934), 1569-1572 (2009).
18. + T cell function. J. Virol. DOI:10.1128/JVI.02030-10 (2010) (Epub ahead of print).
19. + T cells. J. Exp. Med. 205(6), 1369-1379 (2008).
20. Annunziato F, Cosmi L, Santarlasci V et al. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204(8), 1849-1861 (2007).
21. Bettelli E, Carrier Y, Gao W et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441(7090), 235-238 (2006).
22. + T helper cells. Cell 126(6), 1121-1133 (2006).
23. Jiang H, Chess L. Regulation of immune responses by T cells. N. Engl. J. Med. 354(11), 1166-1176 (2006).
24. Wing K, Fehervari Z, Sakaguchi S. Emerging possibilities in the development and function of regulatory T cells. Int. Immunol. 18(7), 991-1000 (2006).
25. + T cells specifc for an MHC class II promiscuous epitope. J. Immunol. 169(4), 2172-2179 (2002).
26. Aslan N, Yurdaydin C, Wiegand J et al. Cytotoxic CD4 T cells in viral hepatitis. J. Viral Hepat. 13(8), 505-514 (2006).
27. + T-cell response in different phases of HIV infection. AIDS 24(7), 947-957 (2010).
28. Jellison ER, Kim S-K, Welsh RM. Cutting edge: MHC class II-restricted killing in vivo during viral infection. J. Immunol. 174(2), 614-618 (2005).
29. + Th1 clones with both cytotoxic and helper activity mediate protective humoral immunity against a lethal poliovirus infection in transgenic mice expressing the human poliovirus receptor. J. Exp. Med. 181(4), 1285-1292 (1995).
30. + T helper type 2 T lymphocytes do not promote recovery from experimental virus infection. J. Exp. Med. 180(4), 1273-1282 (1994).
31. Brien JD, Uhrlaub JL, Nikolich-Zugich J. West Nile virus-specifc CD4 T cells exhibit direct antiviral cytokine secretion and cytotoxicity and are suffcient for antiviral protection. J. Immunol. 181(12), 8568-8575 (2008).
32. Landais E, Saulquin X, Scotet E et al. Direct killing of Epstein-Barr virus (EBV)-infected B cells by CD4 T cells directed against the EBV lytic protein BHRF1. Blood 103(4), 1408-1416 (2004).
33. + Th1 cells kill Burkitt's lymphoma cells. J. Immunol. 169(3), 1593-1603 (2002).
34. + T-cell clones for an intracellular pathogen. Hum. Immunol. 69(8), 475-483 (2008).
35. + cytotoxic T lymphocyte clones display a Th1 cytokine profle and use a fas-independent pathway for specifc tumor cell lysis. J. Invest. Dermatol. 115(1), 74-80 (2000).
36. + CTLs ex vivo. J. Immunol. 168(11), 5954-5958 (2002).
37. + T cells in human cytomegalovirus infection. Hum. Immunol. 65(5), 486-492 (2004).
38. + T cells specifc for human cytomegalovirus. Eur. J. Immunol. 36(12), 3198-3206 (2006).
39. + T cells. J. Exp. Med. 197(4), 437-449 (2003).
40. van Bergen J, Thompson A, van der Slik A, Ottenhoff TH, Gussekloo J, Koning F. Phenotypic and functional characterization of CD4 T cells expressing killer Ig-like receptors. J. Immunol. 173(11), 6719-6726 (2004).
41. + CTL function: similarities and differences between NKG2D and CD28 costimulation. J. Immunol. 175(5), 2825-2833 (2005).
42. Roberts AI, Lee L, Schwarz E et al. NKG2D receptors induced by IL-15 costimulate CD28-negative effector CTL in the tissue micro environment. J. Immunol. 167(10), 5527-5530 (2001).
43. Snyder MR, Weyand CM, Goronzy JJ. The double life of NK receptors: stimulation or co-stimulation? Trends Immunol. 25(1), 25-32 (2004
44. + T cells. Curr. Opin. Immunol. 20(3), 339-343 (2008).
45. Grossman WJ, Verbsky JW, Tollefsen BL, Kemper C, Atkinson JP, Ley TJ. Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 104(9), 2840-2848 (2004).
46. Grossman WJ, Verbsky JW, Barchet W, Colonna M, Atkinson JP, Ley TJ. Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity 21(4), 589-601 (2004).
47. + T cells lyse antigen-presenting B cells by Fas-Fas ligand interaction in an epitope-specifc manner. J. Immunol. 171(9), 4604-4612 (2003).
48. + T cells induce perforin-dependent dendritic cell death in tumor-draining lymph nodes. Immunity 32(2), 266-278 (2010).
49. Green DR, Ferguson TA. The role of Fas ligand in immune privilege. Nat. Rev. Mol. Cell Biol. 2(12), 917-924 (2001).
50. Trapani JA, Smyth MJ. Functional signifcance of the perforin/granzyme cell death pathway. Nat. Rev. Immunol. 2(10), 735-747 (2002).
51. + T cell-mediated cytotoxicity. J. Immunol. 152(3), 1127-1133 (1994).
52. + cytotoxic T-cell-mediated pathogenesis during virus infection. Proc. Natl Acad. Sci. USA 93(25), 14730-14735 (1996).
53. Stuller KA, Cush SS, Flano E. Persistent herpesvirus infection induces a CD4 T cell response containing functionally distinct effector populations. J. Immunol. 184(7), 3850-3856 (2010).
54. + T lymphocytes with cellular maturation. J. Exp. Med. 203(13), 2865-2877 (2006).
55. Stuller KA, Flano E. CD4 T cells mediate killing during persistent gammaherpesvirus 68 infection. J. Virol. 83(9), 4700-4703 (2009).
56. + cytotoxic T lymphocytes in ex vivo expanded therapeutic Epstein-Barr virus-specifc T-cell cultures. Blood 99(9), 3302-3309 (2002).
57. + T cells kill intracellular Mycobacterium tuberculosis by a perforin and Fas/Fas ligand-independent mechanism. J. Immunol. 167(5), 2734-2742 (2001).
58. Lum JJ, Pilon AA, Sanchez-Dardon J et al. Induction of cell death in human immunodefciency virus-infected macrophages and resting memory CD4 T cells by TRAIL/Apo2l. J. Virol. 75(22), 11128-11136 (2001).
59. Sedger LM, Shows DM, Blanton RA et al. IFN-g mediates a novel antiviral activity through dynamic modulation of TRAIL and TRAIL receptor expression. J. Immunol. 163(2), 920-926 (1999).
60. + T cell killing of antigen-presenting macrophages. J. Immunol. 164(6), 2897-2904 (2000).
61. + T cell-mediated cytotoxicity. J. Immunol. 162(5), 2639-2647 (1999).
62. + T cells during mycobacterial infection to promote apoptosis by inducing components of the intracellular apoptosis machinery and by inducing extracellular proapoptotic signals. J. Immunol. 179(2), 939-949 (2007).
63. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM. Suppression of TNF-a-induced apoptosis by NF-kB. Science 274(5288), 787-789 (1996).
64. Wang L, Du F, Wang X. TNF-a induces two distinct caspase-8 activation pathways. Cell 133(4), 693-703 (2008).
65. Kim PK, Zamora R, Petrosko P, Billiar TR. The regulatory role of nitric oxide in apoptosis. Int. Immunopharmacol. 1(8), 1421-1441 (2001).
66. Graubert TA, DiPersio JF, Russell JH, Ley TJ. Perforin/granzyme-dependent and independent mechanisms are both important for the development of graft-versus-host disease after murine bone marrow transplantation. J. Clin. Invest. 100(4), 904-911 (1997).
67. Shresta S, Pham CT, Thomas DA, Graubert TA, Ley TJ. How do cytotoxic lymphocytes kill their targets? Curr. Opin. Immunol. 10(5), 581-587 (1998).
68. + T lymphocytes: analysis using the combination of hereditary per for in-defcient effector cells and Fas-defcient target cells. J. Immunol. 170(4), 2205-2213 (2003).
69. + T cells. Cell. Immunol 257(1-2), 69-79 (2009).
70. Brown DM, Dilzer AM, Meents DL, Swain SL. CD4 T cell-mediated protection from lethal infuenza: perforin and antibody-mediated mechanisms give a one-two punch. J. Immunol. 177(5), 2888-2898 (2006).
71. + T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6(12), 1236-1244 (2005).
72. + T cell differentiation: choosing a path through T-bet. Immunity 27(2), 180-182 (2007).
73. + lineages. J. Immunol. 179(11), 7406-7414 (2007).
74. Suto A, Wurster AL, Reiner SL, Grusby MJ. IL-21 inhibits IFN-g production in developing Th1 cells through the repression of Eomesodermin expression. J. Immunol. 177(6), 3721-3727 (2006).
75. + T cell function by the transcription factor Eomesodermin. Science 302(5647), 1041-1043 (2003).
76. + CTL and NK cells. Am. J. Transplant. 8(3), 627-636 (2008).
77. Cruz-Guilloty F, Pipkin ME, Djuretic IM et al. Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs. J. Exp. Med. 206(1), 51-59 (2009).
78. Kohu K, Ohmori H, Wong WF et al. The Runx3 transcription factor augments Th1 and down-modulates Th2 phenotypes by interacting with and attenuating GATA3. J. Immunol. 183(12), 7817-7824 (2009).
79. Yagi R, Junttila IS, Wei G et al. The transcription factor GATA3 actively represses RUNX3 protein-regulated production of interferon-g. Immunity 32(4), 507-517 (2010).
80. Brown DM. Cytolytic CD4 cells: direct mediators in infectious disease and malignancy. Cell Immunol. 262(2), 89-95 (2010).
81. + T cells independently of its effects on survival and proliferation. J. Immunol. 175(12), 8003-8010 (2005).
82. Zhang J, Scordi I, Smyth MJ, Lichtenheld MG. Interleukin 2 receptor signaling regulates the perforin gene through signal transducer and activator of transcription (Stat)5 activation of two enhancers. J. Exp. Med. 190(9), 1297-1308 (1999).
83. Ye W, Young JD, Liu CC. Interleukin-15 induces the expression of mRNAs of cytolytic mediators and augments cytotoxic activities in primary murine lymphocytes. Cell Immunol. 174(1), 54-62 (1996).
84. White L, Krishnan S, Strbo N et al. Differential effects of IL-21 and IL-15 on perforin expression, lysosomal degranulation, and proliferation in CD8 T cells of patients with human immunodefciency virus-1 (HIV). Blood 109(9), 3873-3880 (2007).
85. Ebert EC. Interleukin 21 up-regulates perforin-mediated cytotoxic activity of human intra-epithelial lymphocytes. Immunology 127(2), 206-215 (2009).
86. Picker LJ, Reed-Inderbitzin EF, Hagen SI et al. IL-15 induces CD4 effector memory T cell production and tissue emigration in nonhuman primates. J. Clin. Invest. 116(6), 1514-1524 (2006).
87. + T cells in multiple tissues during acute SIV infection. Nature 434(7037), 1093-1097 (2005).
88. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361(23), 2209-2220 (2009).
89. + T cells are detectable in most individuals with active HIV-1 infection, but decline with prolonged viral suppression. Nat. Med. 5(5), 518-525 (1999).
90. + T cell responses associated with control of viremia. Science 278(5342), 1447-1450 (1997).
91. Sethi KK, Naher H, Stroehmann I. Phenotypic heterogeneity of cerebrospinal fuid-derived HIV-specifc and HLA-restricted cytotoxic T-cell clones. Nature 335(6186), 178-181 (1988).
92. + cytolytic T lymphocytes isolated from seronegative humans immunized with candidate HIV-1 vaccines. J. Exp. Med. 176(6), 1531-1542 (1992).
93. + cytolytic T lymphocyte responses to a human immunodefciency virus type 1 gp160 subunit vaccine. J. Infect. Dis. 168(1), 92-100 (1993).
94. + T cell response that includes cytolytic T lymphocytes. J. Immunol. 150(10), 4672-4686 (1993).
95. + human CTL clones induced by candidate AIDS vaccines. J. Immunol. 153(6), 2787-2799 (1994).
96. + T-cells: the holy grail? Clin. Exp. Immunol. 138(1), 10-13 (2004).
97. Musey L, Hughes J, Schacker T, Shea T, Corey L, McElrath MJ. Cytotoxic-T-cell responses, viral load, and disease progression in early human immunodefciency virus type 1 infection. N. Engl. J. Med. 337(18), 1267-1274 (1997).
98. + T cells. J. Virol. 78(16), 8844-8851 (2004).
99. + cytotoxic T-lymphocytes. AIDS 6(7), 643-649 (1992).
100. Heinkelein M, Euler-Konig I, Klinker H, Ruckle-Lanz H, Jassoy C. Lysis of human immunodefciency virus type 1 antigen-expressing cells by CD4 and CD8 T cells ex vivo. J. Infect. Dis. 174(1), 209-213 (1996).
101. Chea S, Dale CJ, De Rose R, Ramshaw I A, Kent SJ. Enhanced cellular immunity in macaques following a novel peptide immunotherapy J. Virol. 79(6), 3748-3757 (2005).
102. + T cells recognize and inhibit SIV replication in infected macrophages early after infection. Proc. Natl Acad. Sci. USA 106(24), 9791-9796 (2009).
103. + T cells and macrophages. J. Virol. 83(15), 7668-7677 (2009).
104. Streeck H, Li B, Poon AF et al. Immune-driven recombination and loss of control after HIV superinfection. J. Exp. Med. 205(8), 1789-1796 (2008).
105. Kuroda MJ. Macrophages: do they impact AIDS progression more than CD4 T cells? J. Leukoc. Biol. 87(4), 569-573 (2010).
106. Schmid D, Pypaert M, Munz C. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 26(1), 79-92 (2007).
107. Goulder PJ, Phillips RE, Colbert RA et al Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3(2), 212-217 (1997).
108. + T-cell-epitope escape mutant virus selected in vivo. Nat. Med. 7(7), 795-800 (2001).
109. Eckels DD, Zhou H, Bian TH, Wang H. Identifcation of antigenic escape variants in an immunodominant epitope of hepatitis C virus. Int. Immunol. 11(4), 577-583 (1999).
110. Rychert J, Saindon S, Placek S, Daskalakis D, Rosenberg E. Sequence variation occurs in CD4 epitopes during early HIV infection. J. Acquir. Immune Defc. Syndr. 46(3), 261-267 (2007).
111. Schwartz O, Marechal V, Le Gall S, Lemonnier F, Heard JM. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2(3), 338-342 (1996).
112. Benlahrech A, Harris J, Meiser A et al. Adenovirus vector vaccination induces expansion of memory CD4 T cells with a mucosal homing phenotype that are readily susceptible to HIV-1. Proc. Natl Acad. Sci. USA 106(47), 19940-19945 (2009).
113. Mattapallil JJ, Douek DC, Buckler-White A et al. Vaccination preserves CD4 memory T cells during acute simian immunodefciency virus challenge. J. Exp. Med. 203(6), 1533-1541 (2006).
114. +-T-cell responses by a chimeric antigen construct: potential therapeutic vaccine for EBV-positive nasopharyngeal carcinoma. J. Virol. 78(2), 768-778 (2004).
115. Ribeiro SP, Rosa DS, Fonseca SG et al. A vaccine encoding conserved promiscuous HIV CD4 epitopes induces broad T cell responses in mice transgenic to multiple common HLA class II molecules. PLoS ONE 5(6), e11072 (2010).
116. + T cells induced by a DNA vaccine: immunological consequences of epitope-specifc lysosomal targeting. J. Virol. 75(21), 10421-10430 (2001).
117. Moingeon P, Haensler J, Lindberg A. Towards the rational design of Th1 adjuvants. Vaccine 19(31), 4363-4372 (2001).
118. + T-cell-mediated immunopathological disease. J. Virol. 71(12), 9672-9678 (1997).
119. + T-cell response to Epstein-Barr virus: T-cell-mediated activation of resting B cells and induction of viral BZLF1 expression. J. Virol. 74(14), 6675-6679 (2000).