Primary human immunodeficiency virus type 1-specific CD8+ T-cell responses induced by myeloid dendritic cells

Journal of Virology

Volumn 83, Issue 12, 2009, Pages 6288-6299

  Colleton, Bonnie A ^a,c   Huang, Xiao Li ^a   Melhem, Nada M ^a,d   Fan, Zheng ^a   Borowski, Luann ^a   Rappocciolo, Giovanna ^a   Rinaldo, Charles R ^a,b  

^a UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; GAG PROTEIN; GAMMA INTERFERON; INTERLEUKIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MACROPHAGE MIGRATION INHIBITION FACTOR; MACROPHAGE MIGRATION INHIBITION FACTOR 1 BETA; NEF PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; HLA A ANTIGEN; HLA A*0201 ANTIGEN; HLA-A*0201 ANTIGEN;

ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INFLUENZA VIRUS A; LANGERHANS CELL; LEYDIG CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; NORMAL HUMAN; PRIORITY JOURNAL; SKIN CELL; STEM CELL; UMBILICAL CORD BLOOD; ADULT; CELL CULTURE; CYTOLOGY; FETUS BLOOD; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; NEWBORN; VIROLOGY;

HUMAN HERPESVIRUS 4; HUMAN IMMUNODEFICIENCY VIRUS 1; INFLUENZA A VIRUS;

ADULT; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DENDRITIC CELLS; FETAL BLOOD; HIV INFECTIONS; HIV-1; HLA-A ANTIGENS; HUMANS; INFANT, NEWBORN; LANGERHANS CELLS; LYMPHOCYTE ACTIVATION; MYELOID CELLS;

EID: 66149097719     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02611-08     Document Type: Article

References (62)

1. Appay, V., R. A. van Lier, F. Sallusto, and M. Roederer. 2008. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 73:975-983.
2. Betts, M. R., M. C. Nason, S. M. West, S. C. De Rosa, S. A. Migueles, J. Abraham, M. M. Lederman, J. M. Benito, P. A. Goepfert, M. Connors, M. Roederer, and R. A. Koup. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107:4781-4789. (Pubitemid 43882629)
3. Bevan, M. J. 2004. Helping the CD8(+) T-cell response. Nat. Rev. Immunol. 4:595-602.
4. Brewig, N., A. Kissenpfennig, B. Malissen, A. Veit, T. Bickert, B. Fleischer, S. Mostbock, and U. Ritter. 2009. Priming of CD8+ and CD4+ T cells in experimental leishmaniasis is initiated by different dendritic cell subtypes. J. Immunol. 182:774-783.
5. Brossart, P., F. Grunebach, G. Stuhler, V. L. Reichardt, R. Mohle, L. Kanz, and W. Brugger. 1998. Generation of functional human dendritic cells from adherent peripheral blood monocytes by CD40 ligation in the absence of granulocyte-macrophage colony-stimulating factor. Blood 92:4238-4247. (Pubitemid 28544340)
6. Cao, T., H. Ueno, C. Glaser, J. W. Fay, A. K. Palucka, and J. Banchereau. 2007. Both Langerhans cells and interstitial DC cross-present melanoma antigens and efficiently activate antigen-specific CTL. Eur. J. Immunol. 37:2657-2667.
7. Castelli, F. A., D. Houitte, G. Munier, N. Szely, A. Lecoq, J. P. Briand, S. Muller, and B. Maillere. 2008. Immunoprevalence of the CD4+ T-cell response to HIV Tat and Vpr proteins is provided by clustered and disperse epitopes, respectively. Eur. J. Immunol. 38:2821-2831.
8. Caux, C., C. Massacrier, B. Vanbervliet, B. Dubois, B. de Saint-Vis, C. Dezutter-Dambuyant, C. Jacquet, D. Schmitt, and J. Banchereau. 1997. CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to GM-CSF+TNF alpha. Adv. Exp. Med. Biol. 417:21-25.
9. Comoli, P., F. Ginevri, R. Maccario, C. Frasson, U. Valente, S. Basso, M. Labirio, G. C. Huang, E. Verrina, F. Baldanti, F. Perfumo, and F. Locatelli. 2006. Successful in vitro priming of EBV-specific CD8+ T cells endowed with strong cytotoxic function from T cells of EBV-seronegative children. Am. J. Transplant. 6:2169-2176.
10. Currier, J. R., E. G. Kuta, E. Turk, L. B. Earhart, L. Loomis-Price, S. Janetzki, G. Ferrari, D. L. Birx, and J. H. Cox. 2002. A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J. Immunol. Methods 260:157-172. (Pubitemid 34132882)
11. Deeks, S. G., and B. D. Walker. 2007. Human immunodeficiency virus controllers: mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 27:406-416. (Pubitemid 47418678)
12. de Witte, L., A. Nabatov, and T. B. Geijtenbeek. 2008. Distinct roles for DC-SIGN+-dendritic cells and Langerhans cells in HIV-1 transmission. Trends Mol. Med. 14:12-19.
13. de Witte, L., A. Nabatov, M. Pion, D. Fluitsma, M. A. de Jong, T. de Gruijl, V. Piguet, Y. van Kooyk, and T. B. Geijtenbeek. 2007. Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat. Med. 13:367-371.
14. Draenert, R., M. Altfeld, C. Brander, N. Basgoz, C. Corcoran, A. G. Wurcel, D. R. Stone, S. A. Kalams, A. Trocha, M. M. Addo, P. J. Goulder, and B. D. Walker. 2003. Comparison of overlapping peptide sets for detection of antiviral CD8 and CD4 T cell responses. J. Immunol. Methods 275:19-29. (Pubitemid 36351539)
15. Dubey, S., J. Clair, T. M. Fu, L. Guan, R. Long, R. Mogg, K. Anderson, K. B. Collins, C. Gaunt, V. R. Fernandez, L. Zhu, L. Kierstead, S. Thaler, S. B. Gupta, W. Straus, D. Mehrotra, T. W. Tobery, D. R. Casimiro, and J. W. Shiver. 2007. Detection of HIV vaccine-induced cell-mediated immunity in HIV-seronegative clinical trial participants using an optimized and validated enzyme-linked immunospot assay. J. Acquir. Immune Defic. Syndr. 45:20-27.
16. Fan, Z., X. L. Huang, P. Kalinski, S. Young, and C. R. Rinaldo, Jr. 2007. Dendritic cell function during chronic hepatitis C virus and human immunodeficiency virus type 1 infection. Clin. Vaccine Immunol. 14:1127-1137.
17. Fuhrmann, S., M. Streitz, P. Reinke, H. D. Volk, and F. Kern. 2008. T cell response to the cytomegalovirus major capsid protein (UL86) is dominated by helper cells with a large polyfunctional component and diverse epitope recognition. J. Infect. Dis. 197:1455-1458.
18. + T lymphocytes in healthy seropositive donors. J. Virol. 74:8140-8150.
19. Gruber, A., J. Kan-Mitchell, K. L. Kuhen, T. Mukai, and F. Wong-Staal. 2000. Dendritic cells transduced by multiply deleted HIV-1 vectors exhibit normal phenotypes and functions and elicit an HIV-specific cytotoxic Tlymphocyte response in vitro. Blood 96:1327-1333. (Pubitemid 30658460)
20. Hamann, D., P. A. Baars, M. H. Rep, B. Hooibrink, S. R. Kerkhof-Garde, M. R. Klein, and R. A. van Lier. 1997. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186:1407-1418.
21. Hart, J. P., M. D. Gunn, and S. V. Pizzo. 2004. A CD91-positive subset of CD11c+ blood dendritic cells: characterization of the APC that functions to enhance adaptive immune responses against CD91-targeted antigens. J. Immunol. 172:70-78. (Pubitemid 38020457)
22. Hoji, A., N. C. Connolly, W. G. Buchanan, and C. R. Rinaldo, Jr. 2007. CD27 and CD57 expression reveals atypical differentiation of human immunodeficiency virus type 1-specific memory CD8+ T cells. Clin. Vaccine Immunol. 14:74-80.
23. Huang, X. L., Z. Fan, L. Borowski, and C. R. Rinaldo. 2008. Maturation of dendritic cells for enhanced activation of anti-HIV-1 CD8(+) T cell immunity. J. Leukoc. Biol. 83:1530-1540.
24. Huang, X. L., Z. Fan, B. A. Colleton, R. Buchli, H. Li, W. H. Hildebrand, and C. R. Rinaldo, Jr. 2005. Processing and presentation of exogenous HLA class I peptides by dendritic cells from human immunodeficiency virus type 1-infected persons. J. Virol. 79:3052-3062.
25. Huang, X. L., Z. Fan, L. Zheng, L. Borowski, H. Li, E. K. Thomas, W. H. Hildebrand, X. Q. Zhao, and C. R. Rinaldo, Jr. 2003. Priming of human immunodeficiency virus type 1 (HIV-1)-specific CD8+ T cell responses by dendritic cells loaded with HIV-1 proteins. J. Infect. Dis. 187:315-319.
26. Janssen, E. M., E. E. Lemmens, T. Wolfe, U. Christen, M. G. von Herrath, and S. P. Schoenberger. 2003. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421:852-856.
27. Jonuleit, H., U. Kuhn, G. Muller, K. Steinbrink, L. Paragnik, E. Schmitt, J. Knop, and A. H. Enk. 1997. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur. J. Immunol. 27:3135-3142.
28. Kan-Mitchell, J., M. Bajcz, K. L. Schaubert, D. A. Price, J. M. Brenchley, T. E. Asher, D. C. Douek, H. L. Ng, O. O. Yang, C. R. Rinaldo, Jr., J. M. Benito, B. Bisikirska, R. Hegde, F. M. Marincola, C. Boggiano, D. Wilson, J. Abrams, S. E. Blondelle, and D. B. Wilson. 2006. Degeneracy and repertoire of the human HIV-1 Gag p17(77-85) CTL response. J. Immunol. 176:6690-6701.
29. Kan-Mitchell, J., B. Bisikirska, F. Wong-Staal, K. L. Schaubert, M. Bajcz, and M. Bereta. 2004. The HIV-1 HLA-A2-SLYNTVATL is a help-independent CTL epitope. J. Immunol. 172:5249-5261. (Pubitemid 38542022)
30. Kawamura, T., Y. Koyanagi, Y. Nakamura, Y. Ogawa, A. Yamashita, T. Iwamoto, M. Ito, A. Blauvelt, and S. Shimada. 2008. Significant virus replication in Langerhans cells following application of HIV to abraded skin: relevance to occupational transmission of HIV. J. Immunol. 180:3297-3304.
31. 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. (Pubitemid 38686777)
32. Klechevsky, E., R. Morita, M. Liu, Y. Cao, S. Coquery, L. Thompson-Snipes, F. Briere, D. Chaussabel, G. Zurawski, A. K. Palucka, Y. Reiter, J. Banchereau, and H. Ueno. 2008. Functional specializations of human epidermal langerhans cells and CD14+ dermal dendritic cells. Immunity 29:497-510.
33. Lapenta, C., S. M. Santini, M. Spada, S. Donati, F. Urbani, D. Accapezzato, D. Franceschini, M. Andreotti, V. Barnaba, and F. Belardelli. 2006. IFN-alpha-conditioned dendritic cells are highly efficient in inducing cross-priming CD8(+) T cells against exogenous viral antigens. Eur. J. Immunol. 36:2046-2060.
34. Li, W., D. K. Krishnadas, R. Kumar, D. L. Tyrrell, and B. Agrawal. 2008. Priming and stimulation of hepatitis C virus-specific CD4+ and CD8+ T cells against HCV antigens NS4, NS5a or NS5b from HCV-naive individuals: implications for prophylactic vaccine. Int. Immunol. 20:89-104.
35. Li, W., D. K. Krishnadas, J. Li, D. L. Tyrrell, and B. Agrawal. 2006. Induction of primary human T cell responses against hepatitis C virus-derived antigens NS3 or core by autologous dendritic cells expressing hepatitis C virus antigens: potential for vaccine and immunotherapy. J. Immunol. 176:6065-6075.
36. Lore, K., W. C. Adams, M. J. Havenga, M. L. Precopio, L. Holterman, J. Goudsmit, and R. A. Koup. 2007. Myeloid and plasmacytoid dendritic cells are susceptible to recombinant adenovirus vectors and stimulate polyfunctional memory T cell responses. J. Immunol. 179:1721-1729.
37. Mailliard, R. B., A. Wankowicz-Kalinska, Q. Cai, A. Wesa, C. M. Hilkens, M. L. Kapsenberg, J. M. Kirkwood, W. J. Storkus, and P. Kalinski. 2004. Alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res. 64:5934-5937. (Pubitemid 39129387)
38. Makedonas, G., and M. R. Betts. 2006. Polyfunctional analysis of human T cell responses: importance in vaccine immunogenicity and natural infection. Springer Semin. Immunopathol. 28:209-219.
39. Marchant, A., and M. Goldman. 2005. T cell-mediated immune responses in human newborns: ready to learn? Clin. Exp. Immunol. 141:10-18.
40. Meddows-Taylor, S., S. Shalekoff, L. Kuhn, G. E. Gray, and C. T. Tiemessen. 2007. Development of a whole blood intracellular cytokine staining assay for mapping CD4(+) and CD8(+) T-cell responses across the HIV-1 genome. J. Virol. Methods 144:115-121.
41. Mehta-Damani, A., S. Markowicz, and E. G. Engleman. 1995. Generation of antigen-specific CD4+ T cell lines from naive precursors. Eur. J. Immunol. 25:1206-1211.
42. Newberg, M. H., K. J. McEvers, D. A. Gorgone, M. A. Lifton, S. H. Baumeister, R. S. Veazey, J. E. Schmitz, and N. L. Letvin. 2006. Immunodomination in the evolution of dominant epitope-specific CD8+ T lymphocyte responses in simian immunodeficiency virus-infected rhesus monkeys. J. Immunol. 176:319-328. (Pubitemid 43023277)
43. Oh, S., L. P. Perera, M. Terabe, L. Ni, T. A. Waldmann, and J. A. Berzofsky. 2008. IL-15 as a mediator of CD4+ help for CD8+ T cell longevity and avoidance of TRAIL-mediated apoptosis. Proc. Natl. Acad. Sci. USA 105:5201-5206.
44. Papagno, L., C. A. Spina, A. Marchant, M. Salio, N. Rufer, S. Little, T. Dong, G. Chesney, A. Waters, P. Easterbrook, P. R. Dunbar, D. Shepherd, V. Cerundolo, V. Emery, P. Griffiths, C. Conlon, A. J. McMichael, D. D. Richman, S. L. Rowland-Jones, and V. Appay. 2004. Immune activation and CD8+ T-cell differentiation towards senescence in HIV-1 infection. PLoS Biol. 2:E20. (Pubitemid 39234556)
45. Park, K. D., L. Marti, J. Kurtzberg, and P. Szabolcs. 2006. In vitro priming and expansion of cytomegalovirus-specific Th1 and Tc1 T cells from naive cord blood lymphocytes. Blood 108:1770-1773.
46. Precopio, M. L., M. R. Betts, J. Parrino, D. A. Price, E. Gostick, D. R. Ambrozak, T. E. Asher, D. C. Douek, A. Harari, G. Pantaleo, R. Bailer, B. S. Graham, M. Roederer, and R. A. Koup. 2007. Immunization with vaccinia virus induces polyfunctional and phenotypically distinctive CD8(+) T cell responses. J. Exp. Med. 204:1405-1416.
47. Prlic, M., M. A. Williams, and M. J. Bevan. 2007. Requirements for CD8 T-cell priming, memory generation and maintenance. Curr. Opin. Immunol. 19:315-319.
48. Ratzinger, G., J. Baggers, M. A. de Cos, J. Yuan, T. Dao, J. L. Reagan, C. Munz, G. Heller, and J. W. Young. 2004. Mature human Langerhans cells derived from CD34+ hematopoietic progenitors stimulate greater cytolytic T lymphocyte activity in the absence of bioactive IL-12p70, by either single peptide presentation or cross-priming, than do dermal-interstitial or monocyte-derived dendritic cells. J. Immunol. 173:2780-2791. (Pubitemid 39063140)
49. Rinaldo, C. R. 2009. Dendritic cell-based human immunodeficiency virus vaccine. J. Intern. Med. 265:138-158.
50. Rinaldo, C. R., Jr., and P. Piazza. 2004. Virus infection of dendritic cells: portal for host invasion and host defense. Trends Microbiol. 12:337-345. (Pubitemid 38829654)
51. Romani, N., S. Gruner, D. Brang, E. Kampgen, A. Lenz, B. Trockenbacher, G. Konwalinka, P. O. Fritsch, R. M. Steinman, and G. Schuler. 1994. Proliferating dendritic cell progenitors in human blood. J. Exp. Med. 180:83-93.
52. Salio, M., N. Dulphy, J. Renneson, M. Herbert, A. McMichael, A. Marchant, and V. Cerundolo. 2003. Efficient priming of antigen-specific cytotoxic T lymphocytes by human cord blood dendritic cells. Int. Immunol. 15:1265-1273.
53. Salio, M., D. Shepherd, P. R. Dunbar, M. Palmowski, K. Murphy, L. Wu, and V. Cerundolo. 2001. Mature dendritic cells prime functionally superior melan-A-specific CD8+ lymphocytes as compared with nonprofessional APC. J. Immunol. 167:1188-1197. (Pubitemid 32703112)
54. 19-27 epitope. J. Immunol. 178:7756-7766.
55. Schlienger, K., N. Craighead, K. P. Lee, B. L. Levine, and C. H. June. 2000. Efficient priming of protein antigen-specific human CD4(+) T cells by monocyte-derived dendritic cells. Blood 96:3490-3498.
56. Tomiyama, H., H. Takata, T. Matsuda, and M. Takiguchi. 2004. Phenotypic classification of human CD8+ T cells reflecting their function: inverse correlation between quantitative expression of CD27 and cytotoxic effector function. Eur. J. Immunol. 34:999-1010.
57. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3:133-146.
58. Tschachler, E., V. Groh, M. Popovic, D. L. Mann, K. Konrad, B. Safai, L. Eron, F. DiMarzo Veronese, K. Wolff, and G. Stingl. 1987. Epidermal Langerhans cells - a target for HTLV-III/LAV infection. J. Investig. Dermatol. 88:233-237.
59. Turville, S. G., P. U. Cameron, A. Handley, G. Lin, S. Pohlmann, R. W. Doms, and A. L. Cunningham. 2002. Diversity of receptors binding HIV on dendritic cell subsets. Nat. Immunol. 3:975-983.
60. Wilson, C. C., W. C. Olson, T. Tuting, C. R. Rinaldo, M. T. Lotze, and W. J. Storkus. 1999. HIV-1-specific CTL responses primed in vitro by blood-derived dendritic cells and Th1-biasing cytokines. J. Immunol. 162:3070-3078. (Pubitemid 29309338)
61. Yuan, J., J. B. Latouche, J. Hodges, A. N. Houghton, G. Heller, M. Sadelain, I. Riviere, and J. W. Young. 2006. Langerhans-type dendritic cells genetically modified to express full-length antigen optimally stimulate CTLs in a CD4- dependent manner. J. Immunol. 176:2357-2365. (Pubitemid 43201684)
62. Zarling, A. L., J. G. Johnson, R. W. Hoffman, and D. R. Lee. 1999. Induction of primary human CD8+ T lymphocyte responses in vitro using dendritic cells. J. Immunol. 162:5197-5204. (Pubitemid 29307124)