Dendritic cells exposed to MVA-based HIV-1 vaccine induce highly functional HIV-1-specific CD8+ T cell responses in HIV-1-infected individuals

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Climent, Núria ^a,b   Guerra, Susana ^c,d   García, Felipe ^a,b   Rovira, Cristina ^a,b   Miralles, Laia ^a,b   Gómez, Carmen Elena ^c   Piqué, Núria ^e   Gil, Cristina ^a,b   Gatell, José María ^a,b   Esteban, Mariano ^c   Gallart, Teresa ^a,b  

^a HOSPITAL CLÍNIC   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^e UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; DENDRITIC CELL VACCINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; SECONDARY LYMPHOID TISSUE CHEMOKINE; TUMOR NECROSIS FACTOR ALPHA; CHEMOKINE; CYTOKINE;

ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; COCULTURE; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE RELEASE; CYTOTOXICITY; DENDRITIC CELL; DRUG SCREENING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LYMPHOCYTE PROLIFERATION; MODIFIED VACCINIA VIRUS ANKARA; MODIFIED VACCINIA VIRUS ANKARA CLADE B; T LYMPHOCYTE ACTIVATION; VACCINIA VIRUS; VIRUS GENE; ENVELOPE GENE; FLOW CYTOMETRY; GENE VECTOR; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; METABOLISM; MONOCYTE; POXVIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AIDS VACCINES; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHEMOKINES; CYTOKINES; DENDRITIC CELLS; FLOW CYTOMETRY; GENES, ENV; GENETIC VECTORS; HIV ANTIGENS; HIV INFECTIONS; HIV-1; HUMANS; MONOCYTES; POXVIRIDAE;

EID: 79956200639     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019644     Document Type: Article

References (86)

1. Richman DD, Margolis DM, Delaney M, Greene WC, Hazuda D, et al. (2009) The Challenge of Finding a Cure for HIV Infection. Science 323: 1304-1307.
2. McMichael AJ, Hanke T, (2003) HIV vaccines 1983-2003. Nat Med 9: 874-880.
3. Virgin HW, Walker BD, (2010) Immunology and the elusive AIDS vaccine. Nature 464: 224-231.
4. Koff WC, (2010) Accelerating HIV vaccine development. Nature 464: 161-162.
5. McElrath MJ, Haynes BF, (2010) Induction of immunity to human immunodeficiency virus type-1 by vaccination. Immunity 33: 542-554.
6. Flynn NM, Forthal DN, Harro CD, Judson FN, Mayer KH, et al. (2005) Placebo-controlled phase 3 trial of a recombinant glycoprotein 120 vaccine to prevent HIV-1 infection. J Infect Dis 191: 654-665.
7. Pitisuttithum P, Gilbert P, Gurwith M, Heyward W, Martin M, et al. (2006) Randomized, double-blind, placebo-controlled efficacy trial of a bivalent recombinant glycoprotein 120 HIV-1 vaccine among injection drug users in Bangkok, Thailand. J Infect Dis 194: 1661-1671.
8. Korber BT, Letvin NL, Haynes BF, (2009) T-cell vaccine strategies for human immunodeficiency virus, the virus with a thousand faces. J Virol 83: 8300-8314.
9. McMichael AJ, (2006) HIV vaccines. Annu Rev Immunol 24: 227-255.
10. Buchbinder SP, Mehrotra DV, Duerr A, Fitzgerald DW, Mogg R, et al. (2008) Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 372: 1881-1893.
11. McElrath MJ, De Rosa SC, Moodie Z, Dubey S, Kierstead L, et al. (2008) HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet 372: 1894-1905.
12. Gray G, Buchbinder S, Duerr A, (2010) Overview of STEP and Phambili trial results: two phase IIb test-of-concept studies investigating the efficacy of MRK adenovirus type 5 gag/pol/nef subtype B HIV vaccine. Curr Opin HIV AIDS 5: 357-361.
13. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, et al. (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361: 2209-2220.
14. Hanke T, Goonetilleke N, McMichael AJ, Dorrell L, (2007) Clinical experience with plasmid DNA- and modified vaccinia virus Ankara-vectored human immunodeficiency virus type 1 clade A vaccine focusing on T-cell induction. J Gen Virol 88: 1-12.
15. Esteban M, (2009) Attenuated poxvirus vectors MVA and NYVAC as promising vaccine candidates against HIV/AIDS. Hum Vaccin 5: 867-871.
16. Pantaleo G, Esteban M, Jacobs B, Tartaglia J, (2010) Poxvirus vector-based HIV vaccines. Current Opinion in HIV and AIDS 5: 391-396.
17. Zhang X, Cassis-Ghavami F, Eller M, Currier J, Slike BM, et al. (2007) Direct comparison of antigen production and induction of apoptosis by canarypox virus- and modified vaccinia virus ankara-human immunodeficiency virus vaccine vectors. J Virol 81: 7022-7033.
18. Guerra S, Najera JL, Gonzalez JM, Lopez-Fernandez LA, Climent N, et al. (2007) Distinct gene expression profiling after infection of immature human monocyte-derived dendritic cells by the attenuated poxvirus vectors MVA and NYVAC. J Virol 81: 8707-8721.
19. Najera JL, Gomez CE, Garcia-Arriaza J, Sorzano CO, Esteban M, (2010) Insertion of vaccinia virus C7L host range gene into NYVAC-B genome potentiates immune responses against HIV-1 antigens. PLoS One 5: e11406.
20. Brandler S, Lepelley A, Desdouits M, Guivel-Benhassine F, Ceccaldi PE, et al. (2010) Preclinical studies of a modified vaccinia virus Ankara-based HIV candidate vaccine: antigen presentation and antiviral effect. J Virol 84: 5314-5328.
21. Amara RR, Villinger F, Altman JD, Lydy SL, O'Neil SP, et al. (2001) Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292: 69-74.
22. Barouch DH, Santra S, Kuroda MJ, Schmitz JE, Plishka R, et al. (2001) Reduction of simian-human immunodeficiency virus 89.6P viremia in rhesus monkeys by recombinant modified vaccinia virus Ankara vaccination. J Virol 75: 5151-5158.
23. Gudmundsdotter L, Nilsson C, Brave A, Hejdeman B, Earl P, et al. (2009) Recombinant Modified Vaccinia Ankara (MVA) effectively boosts DNA-primed HIV-specific immune responses in humans despite pre-existing vaccinia immunity. Vaccine 27: 4468-4474.
24. Dorrell L, Williams P, Suttill A, Brown D, Roberts J, et al. (2007) Safety and tolerability of recombinant modified vaccinia virus Ankara expressing an HIV-1 gag/multiepitope immunogen (MVA.HIVA) in HIV-1-infected persons receiving combination antiretroviral therapy. Vaccine 25: 3277-3283.
25. Peters BS, Jaoko W, Vardas E, Panayotakopoulos G, Fast P, et al. (2007) Studies of a prophylactic HIV-1 vaccine candidate based on modified vaccinia virus Ankara (MVA) with and without DNA priming: Effects of dosage and route on safety and immunogenicity. Vaccine 25: 2120-2127.
26. Gomez CE, Najera JL, Krupa M, Esteban M, (2008) The poxvirus vectors MVA and NYVAC as gene delivery systems for vaccination against infectious diseases and cancer. Curr Gene Ther 8: 97-120.
27. Guerra S, Lopez-Fernandez LA, Conde R, Pascual-Montano A, Harshman K, et al. (2004) Microarray analysis reveals characteristic changes of host cell gene expression in response to attenuated modified vaccinia virus Ankara infection of human HeLa cells. J Virol 78: 5820-5834.
28. Mooij P, Balla-Jhagjhoorsingh SS, Koopman G, Beenhakker N, van Haaften P, et al. (2008) Differential CD4+ versus CD8+ T-cell responses elicited by different poxvirus-based human immunodeficiency virus type 1 vaccine candidates provide comparable efficacies in primates. J Virol 82: 2975-2988.
29. Garcia F, Climent N, Gil C, Plana M, Lambert A, et al. (2010) A therapeutic dendritic cell-based vaccine for HIV-1 infection. J Infect Dis 203: 473-478.
30. Garcia F, Lejeune M, Climent N, Gil C, Alcami J, et al. (2005) Therapeutic immunization with dendritic cells loaded with heat-inactivated autologous HIV-1 in patients with chronic HIV-1 infection. J Infect Dis 191: 1680-1685.
31. Rinaldo CR, (2009) Dendritic cell-based human immunodeficiency virus vaccine. J Intern Med 265: 138-158.
32. Drake CG, (2010) Prostate cancer as a model for tumour immunotherapy. Nat Rev Immunol 10: 580-593.
33. Johnson LA, Sampson JH, (2010) Immunotherapy approaches for malignant glioma from 2007 to 2009. Curr Neurol Neurosci Rep 10: 259-266.
34. Lapenta C, Santini SM, Logozzi M, Spada M, Andreotti M, et al. (2003) Potent immune response against HIV-1 and protection from virus challenge in hu-PBL-SCID mice immunized with inactivated virus-pulsed dendritic cells generated in the presence of IFN-alpha. J Exp Med 198: 361-367.
35. Aline F, Brand D, Bout D, Pierre J, Fouquenet D, et al. (2007) Generation of specific Th1 and CD8+ T-cell responses by immunization with mouse CD8+ dendritic cells loaded with HIV-1 viral lysate or envelope glycoproteins. Microbes Infect 9: 536-543.
36. Gomez CE, Najera JL, Jimenez EP, Jimenez V, Wagner R, et al. (2007) Head-to-head comparison on the immunogenicity of two HIV/AIDS vaccine candidates based on the attenuated poxvirus strains MVA and NYVAC co-expressing in a single locus the HIV-1BX08 gp120 and HIV-1(IIIB) Gag-Pol-Nef proteins of clade B. Vaccine 25: 2863-2885.
37. Ramirez JC, Gherardi MM, Esteban M, (2000) Biology of attenuated modified vaccinia virus Ankara recombinant vector in mice: virus fate and activation of B- and T-cell immune responses in comparison with the Western Reserve strain and advantages as a vaccine. J Virol 74: 923-933.
38. Liu J, Hellerstein M, McDonnel M, Amara RR, Wyatt LS, et al. (2007) Dose-response studies for the elicitation of CD8 T cells by a DNA vaccine, used alone or as the prime for a modified vaccinia Ankara boost. Vaccine 25: 2951-2958.
39. Lore K, Smed-Sorensen A, Vasudevan J, Mascola JR, Koup RA, (2005) Myeloid and plasmacytoid dendritic cells transfer HIV-1 preferentially to antigen-specific CD4+ T cells. J Exp Med 201: 2023-2033.
40. Kemper C, Mitchell LM, Zhang L, Hourcade DE, (2008) The complement protein properdin binds apoptotic T cells and promotes complement activation and phagocytosis. Proc Natl Acad Sci U S A 105: 9023-9028.
41. Chahroudi A, Garber DA, Reeves P, Liu L, Kalman D, et al. (2006) Differences and similarities in viral life cycle progression and host cell physiology after infection of human dendritic cells with modified vaccinia virus Ankara and vaccinia virus. J Virol 80: 8469-8481.
42. Kim HJ, Kim HO, Lee K, Baek EJ, Kim HS, (2010) Two-step maturation of immature DCs with proinflammatory cytokine cocktail and poly(I:C) enhances migratory and T cell stimulatory capacity. Vaccine 28: 2877-2886.
43. Humrich JY, Thumann P, Greiner S, Humrich JH, Averbeck M, et al. (2007) Vaccinia virus impairs directional migration and chemokine receptor switch of human dendritic cells. Eur J Immunol 37: 954-965.
44. Guerra S, Gonzalez JM, Climent N, Reyburn H, Lopez-Fernandez LA, et al. (2010) Selective induction of host genes by MVA-B, a candidate vaccine against HIV/AIDS. J Virol 84: 8141-8152.
45. Zhang R, Xing M, Ji X, Gu L, Yang X, et al. (2010) Interferon-alpha and interleukin-6 in SLE serum induce the differentiation and maturation of dendritic cells derived from CD34+ hematopoietic precursor cells. Cytokine 50: 195-203.
46. Tovey MG, Lallemand C, Thyphronitis G, (2008) Adjuvant activity of type I interferons. Biol Chem 389: 541-545.
47. Longhi MP, Trumpfheller C, Idoyaga J, Caskey M, Matos I, et al. (2009) Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J Exp Med 206: 1589-1602.
48. Liu L, Chavan R, Feinberg MB, (2008) Dendritic cells are preferentially targeted among hematolymphocytes by Modified Vaccinia Virus Ankara and play a key role in the induction of virus-specific T cell responses in vivo. BMC Immunol 9: 15.
49. Delaloye J, Roger T, Steiner-Tardivel QG, Le Roy D, Knaup RM, et al. (2009) Innate immune sensing of modified vaccinia virus Ankara (MVA) is mediated by TLR2-TLR6, MDA-5 and the NALP3 inflammasome. PLoS Pathog 5: e1000480.
50. Henkel JS, Engelhardt JI, Siklos L, Simpson EP, Kim SH, et al. (2004) Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann Neurol 55: 221-235.
51. Berger EA, Murphy PM, Farber JM, (1999) Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 17: 657-700.
52. Karpov AV, (2001) Endogenous and exogenous interferons in HIV-infection. Eur J Med Res 6: 507-524.
53. Vendrame D, Sourisseau M, Perrin V, Schwartz O, Mammano F, (2009) Partial inhibition of human immunodeficiency virus replication by type I interferons: impact of cell-to-cell viral transfer. J Virol 83: 10527-10537.
54. Stylianou E, Yndestad A, Sikkeland LI, Bjerkeli V, Damas JK, et al. (2002) Effects of interferon-alpha on gene expression of chemokines and members of the tumour necrosis factor superfamily in HIV-infected patients. Clin Exp Immunol 130: 279-285.
55. Agostini C, Facco M, Siviero M, Carollo D, Galvan S, et al. (2000) CXC chemokines IP-10 and mig expression and direct migration of pulmonary CD8+/CXCR3+ T cells in the lungs of patients with HIV infection and T-cell alveolitis. Am J Respir Crit Care Med 162: 1466-1473.
56. Roberts L, Passmore JA, Williamson C, Little F, Bebell LM, et al. (2010) Plasma cytokine levels during acute HIV-1 infection predict HIV disease progression. AIDS 24: 819-831.
57. Saini M, Pearson C, Seddon B, (2009) Regulation of T cell-dendritic cell interactions by IL-7 governs T-cell activation and homeostasis. Blood 113: 5793-5800.
58. Carreno BM, Becker-Hapak M, Linette GP, (2009) CD40 regulates human dendritic cell-derived IL-7 production that, in turn, contributes to CD8(+) T-cell antigen-specific expansion. Immunol Cell Biol 87: 167-177.
59. Surh CD, Sprent J, (2008) Homeostasis of Naive and Memory T Cells. Immunity 29: 848-862.
60. Rochman Y, Spolski R, Leonard WJ, (2009) New insights into the regulation of T cells by gamma(c) family cytokines. Nat Rev Immunol 9: 480-490.
61. Promadej-Lanier N, Hanson DL, Srinivasan P, Luo W, Adams DR, et al. (2010) Resistance to Simian HIV infection is associated with high plasma interleukin-8, RANTES and Eotaxin in a macaque model of repeated virus challenges. J Acquir Immune Defic Syndr 53: 574-581.
62. Chertov O, Michiel DF, Xu L, Wang JM, Tani K, et al. (1996) Identification of defensin-1, defensin-2, and CAP37/azurocidin as T-cell chemoattractant proteins released from interleukin-8-stimulated neutrophils. J Biol Chem 271: 2935-2940.
63. Rodriguez-Garcia M, Climent N, Oliva H, Casanova V, Franco R, et al. (2010) Increased alpha-defensins 1-3 production by dendritic cells in HIV-infected individuals is associated with slower disease progression. PLoS One 5: e9436.
64. Curtsinger JM, Mescher MF, (2010) Inflammatory cytokines as a third signal for T cell activation. Current Opinion in Immunology 22: 333-340.
65. Wang Y, Chaudhri G, Jackson RJ, Karupiah G, (2009) IL-12p40 and IL-18 Play Pivotal Roles in Orchestrating the Cell-Mediated Immune Response to a Poxvirus Infection. J Immunol 183: 3324-3331.
66. Foulds KE, Wu Cy, Seder RA, (2006) Th1 memory: implications for vaccine development. Immunological Reviews 211: 58-66.
67. Clerici M, Shearer GM, (1993) A TH1→TH2 switch is a critical step in the etiology of HIV infection. Immunol Today 14: 107-111.
68. Ogg GS, Jin X, Bonhoeffer S, Dunbar PR, Nowak MA, et al. (1998) Quantitation of HIV-1-Specific Cytotoxic T Lymphocytes and Plasma Load of Viral RNA. Science 279: 2103-2106.
69. Migueles SA, Laborico AC, Shupert WL, Sabbaghian MS, Rabin R, et al. (2002) HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat Immunol 3: 1061-1068.
70. Zimmerli SC, Harari A, Cellerai C, Vallelian F, Bart PA, et al. (2005) HIV-1-specific IFN-gamma/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc Natl Acad Sci U S A 102: 7239-7244.
71. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, et al. (2006) HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107: 4781-4789.
72. Almeida JR, Sauce D, Price DA, Papagno L, Shin SY, et al. (2009) Antigen sensitivity is a major determinant of CD8+ T-cell polyfunctionality and HIV-suppressive activity. Blood 113: 6351-6360.
73. Freel SA, Lamoreaux L, Chattopadhyay PK, Saunders K, Zarkowsky D, et al. (2010) Phenotypic and functional profile of HIV-inhibitory CD8 T cells elicited by natural infection and heterologous prime/boost vaccination. J Virol 84: 4998-5006.
74. Cocchi F, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, et al. (1995) Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science 270: 1811-1815.
75. DeVico AL, Gallo RC, (2004) Control of HIV-1 infection by soluble factors of the immune response. Nat Rev Microbiol 2: 401-413.
76. Saez-Cirion A, Lacabaratz C, Lambotte O, Versmisse P, Urrutia A, et al. (2007) HIV controllers exhibit potent CD8 T cell capacity to suppress HIV infection ex vivo and peculiar cytotoxic T lymphocyte activation phenotype. Proc Natl Acad Sci U S A 104: 6776-6781.
77. Jenne L, Schuler G, Steinkasserer A, (2001) Viral vectors for dendritic cell-based immunotherapy. Trends Immunol 22: 102-107.
78. Gasteiger G, Kastenmuller W, Ljapoci R, Sutter G, Drexler I, (2007) Cross-priming of cytotoxic T cells dictates antigen requisites for modified vaccinia virus Ankara vector vaccines. J Virol 81: 11925-11936.
79. Greiner S, Humrich JY, Thuman P, Sauter B, Schuler G, et al. (2006) The highly attenuated vaccinia virus strain modified virus Ankara induces apoptosis in melanoma cells and allows bystander dendritic cells to generate a potent anti-tumoral immunity. Clin Exp Immunol 146: 344-353.
80. Reimann J, Schirmbeck R, (1999) Alternative pathways for processing exogenous and endogenous antigens that can generate peptides for MHC class I-restricted presentation. Immunol Rev 172: 131-152.
81. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, et al. (2009) Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461: 282-286.
82. Barat C, Gilbert C, Imbeault M, Tremblay MJ, (2008) Extracellular ATP reduces HIV-1 transfer from immature dendritic cells to CD4+ T lymphocytes. Retrovirology 5: 30.
83. Le Bon A, Etchart N, Rossmann C, Ashton M, Hou S, et al. (2003) Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat Immunol 4: 1009-1015.
84. Lapenta C, Santini S, Spada M, Donati S, Urbani F, et al. (2006) IFN-+{pipe}-conditioned dendritic cells are highly efficient in inducing cross-priming CD8+ T cells against exogenous viral antigens. Eur J Immunol 36: 2046-2060.
85. Garcia-Arriaza J, Najera JL, Gomez CE, Sorzano CO, Esteban M, (2010) Immunogenic profiling in mice of a HIV/AIDS vaccine candidate (MVA-B) expressing four HIV-1 antigens and potentiation by specific gene deletions. PLoS One 5: e12395.
86. Wherry EJ, Blattman JN, Murali-Krishna K, van der MR, Ahmed R, (2003) Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 77: 4911-4927.