Loading dendritic cells with PLA-p24 nanoparticles or MVA expressing HIV genes induces HIV-1-specific T cell responses

Vaccine

Volumn 32, Issue 47, 2014, Pages 6266-6276

  Climent, Núria ^a,b   Munier, Séverine ^c   Piqué, Núria ^d   García, Felipe ^a,b   Pavot, Vincent ^c   Primard, Charlotte ^c   Casanova, Victor ^d   Gatell, José María ^a,b   Verrier, Bernard ^c   Gallart, Teresa ^a,b  

^a HOSPITAL CLÍNIC   (Spain)

^b Catalan Program for HIV Vaccine Development (HIVACAT)   (Spain)

^c INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cytokines; HIV core protein p24; HIV immunogens; Human CD4+ T and CD8+ T cells; Human monocytes derived dendritic cells; MVA; Polylactic acid (PLA) particles; Proliferation

Indexed keywords

GAG PROTEIN; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 2; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; NANOCARRIER; POLYLACTIC ACID P24 NANOCARRIER; UNCLASSIFIED DRUG; VIRUS VECTOR; CCL19 PROTEIN, HUMAN; IFNG PROTEIN, HUMAN; IL2 PROTEIN, HUMAN; LACTIC ACID; NANOPARTICLE; P24 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS TYPE 1; POLYLACTIC ACID; POLYMER; RECOMBINANT VACCINE;

ARTICLE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CYTOKINE RELEASE; CYTOTOXICITY ASSAY; DENDRITIC CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IMMUNOPHENOTYPING; MONOCYTE DERIVED DENDRITIC CELL; CELL CULTURE; CELL MOTION; COCULTURE; COMPARATIVE STUDY; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; VACCINIA VIRUS;

AIDS VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CCL19; COCULTURE TECHNIQUES; DENDRITIC CELLS; HIV ANTIGENS; HIV CORE PROTEIN P24; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-2; LACTIC ACID; NANOPARTICLES; POLYMERS; VACCINES, SYNTHETIC; VACCINIA VIRUS;

EID: 84907968851     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2014.09.010     Document Type: Article

References (69)

1. Munier C.M., Andersen C.R., Kelleher A.D. HIV vaccines: progress to date. Drugs 2011, 71:387-414.
2. Macagno A., Napolitani G., Lanzavecchia A., Sallusto F. Duration, combination and timing: the signal integration model of dendritic cell activation. Trends Immunol 2007, 28:227-233.
3. Steinman R.M. Decisions about dendritic cells: past, present, and future. Annu Rev Immunol 2012, 30:1-22.
4. García F., Routy J.P. Challenges in dendritic cells-based therapeutic vaccination in HIV-1 infection Workshop in dendritic cell-based vaccine clinical trials in HIV-1. Vaccine 2011, 29:6454-6463.
5. García F., Climent N., Guardo A.C., Gil C., León A., Autran B., et al. DCV2/MANON07-ORVACS Study Group. A dendritic cell-based vaccine elicits T cell responses associated with control of HIV-1 replication. Sci Transl Med 2013, 5:166ra2.
6. + T cell responses by dendritic cells loaded with HIV-1 proteins. J Infect Dis 2003, 187:315-319.
7. Connolly N.C., Whiteside T.L., Wilson C., Kondragunta V., Rinaldo C.R., Riddler S.A. Therapeutic immunization with human immunodeficiency virus type 1 (HIV-1) peptide-loaded dendritic cells is safe and induces immunogenicity in HIV-1-infected individuals. Clin Vaccine Immunol 2008, 15:284-292.
8. + T-cell responses elicited by different poxvirus-based human immunodeficiency virus type 1 vaccine candidates provide comparable efficacies in primates. J Virol 2008, 82:2975-2988.
9. Pion M., Serramia M.J., Diaz L., Bryszewska M., Gallart T., García F., et al. Phenotype and functional analysis of human monocytes-derived dendritic cells loaded with a carbosilane dendrimer. Biomaterials 2010, 31:8749-8758.
10. Aline F., Brand D., Pierre J., Roingeard P., Séverine M., Verrier B., et al. Dendritic cells loaded with HIV-1 p24 proteins adsorbed on surfactant-free anionic PLA nanoparticles induce enhanced cellular immune responses against HIV-1 after vaccination. Vaccine 2009, 27:5284-5291.
11. Geissmann F., Manz M.G., Jung S., Sieweke M.H., Merad M., Ley K. Development of monocytes, macrophages, and dendritic cells. Science 2010, 327:656-661.
12. Cheong C., Matos I., Choi J.H., Dandamudi D.B., Shrestha E., Longhi M.P., et al. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell 2010, 143:416-429.
13. García F., Lejeune M., Climent N., Gil C., Alcamí J., Morente V., et al. Therapeutic immunization with dendritic cells loaded with heat-inactivated autologous HIV-1 in patients with chronic HIV-1 infection. J Infect Dis 2005, 191:1680-1685.
14. Climent N., Guerra S., García F., Rovira C., Miralles L., Gómez C.E., et al. 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 2011, 6:e19644.
15. Gómez C.E., Nájera J.L., Perdiguero B., García-Arriaza J., Sorzano C.O., Jiménez V., et al. The HIV/AIDS vaccine candidate MVA-B administered as a single immunogen in humans triggers robust, polyfunctional, and selective effector memory T cell responses to HIV-1 antigens. J Virol 2011, 85:11468-11478.
16. Shegokar R., Singh K.K. Stavudine entrapped lipid nanoparticles for targeting lymphatic HIV reservoirs. Pharmazie 2011, 66:264-271.
17. das Neves J., Amiji M.M., Bahia M.F., Sarmento B. Nanotechnology-based systems for the treatment and prevention of HIV/AIDS. Adv Drug Delivery Rev 2010, 62:458-477.
18. Lanao J.M., Briones E., Colino C.I. Recent advances in delivery systems for anti-HIV1 therapy. J Drug Target 2007, 15:21-36.
19. Qiao Y., Huang Y., Qiu C., Yue X., Deng L., Wan Y., et al. The use of PEGylated poly[2-(N,N-dimethylamino) ethyl methacrylate] as a mucosal DNA delivery vector and the activation of innate immunity and improvement of HIV-1-specific immune responses. Biomaterials 2010, 31:115-123.
20. Akagi T., Wang X., Uto T., Baba M., Akashi M. Protein direct delivery to dendritic cells using nanoparticles based on amphiphilic poly(amino acid) derivatives. Biomaterials 2007, 28:3427-3436.
21. Lamalle-Bernard D., Munier S., Compagnon C., Charles M.H., Kalyanaraman V.S., Delair T., et al. Coadsorption of HIV-1 p24 and gp120 proteins to surfactant-free anionic PLA nanoparticles preserves antigenicity and immunogenicity. J Controlled Release 2006, 115:57-67.
22. Guillon C., Mayol K., Terrat C., Compagnon C., Primard C., Charles M.H., et al. Formulation of HIV-1 Tat and p24 antigens by PLA nanoparticles or MF59 impacts the breadth, but not the magnitude, of serum and faecal antibody responses in rabbits. Vaccine 2007, 25:7491-7501.
23. Locher C.P., Putnam D., Langer R., Witt S.A., Ashlock B.M. Enhancement of a human immunodeficiency virus env DNA vaccine using a novel polycationic nanoparticle formulation. Immunol Lett 2003, 90:67-70.
24. Peek L.J., Middaugh C.R., Berkland C. Nanotechnology in vaccine delivery. Adv Drug Delivery Rev 2008, 60:915-928.
25. Sakaue G., Hiroi T., Nakagawa Y., Someya K., Iwatani K., Sawa Y., et al. HIV mucosal vaccine: nasal immunization with gp160-encapsulated hemagglutinating virus of Japan-liposome induces antigen-specific CTLs and neutralizing antibody responses. J Immunol 2003, 170:495-502.
26. Zhang W., Wang L., Liu Y., Chen X., Li J., Yang T., et al. Comparison of PLA microparticles and alum as adjuvants for H5N1 influenza split vaccine: adjuvanticity evaluation and preliminary action mode analysis. Pharm Res 2014, 31:1015-1031.
27. Kreijtz J.H., Gilbert S.C., Sutter G. Poxvirus vectors. Vaccine 2013, 31:4217-4219.
28. + T-lymphocyte proliferative responses in healthy individuals immunized with an HIV-1 DNA vaccine and boosted with recombinant modified vaccinia virus ankara expressing HIV-1 genes. Clin Vaccine Immunol 2010, 17:1124-1131.
29. Brandler S., Lepelley A., Desdouits M., Guivel-Benhassine F., Ceccaldi P.E., Lévy Y., et al. Preclinical studies of a modified vaccinia virus Ankara-based HIV candidate vaccine: antigen presentation and antiviral effect. J Virol 2010, 84:5314-5328.
30. Nájera J.L., Gómez C.E., García-Arriaza J., Sorzano C.O., Esteban M. Insertion of vaccinia virus C7L host range gene into NYVAC-B genome potentiates immune responses against HIV-1 antigens. PLoS One 2010, 5:e11406.
31. García F., Bernaldo de Quirós J.C., Gómez C.E., Perdiguero B., Nájera J.L., Jiménez V., et al. Safety and immunogenicity of a modified pox vector-based HIV/AIDS vaccine candidate expressing Env, Gag, Pol and Nef proteins of HIV-1 subtype B (MVA-B) in healthy HIV-1-uninfected volunteers: a phase I clinical trial (RISVAC02). Vaccine 2011, 29:8309-8316.
32. Flynn B.J., Kastenmüller K., Wille-Reece U., Tomaras G.D., Alam M., Lindsay R.W., et al. Immunization with HIV Gag targeted to dendritic cells followed by recombinant New York vaccinia virus induces robust T-cell immunity in nonhuman primates. Proc Natl Acad Sci USA 2011, 108:7131-7136.
33. McMichael A.J., Borrow P., Tomaras G.D., Goonetilleke N., Haynes B.F. The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol 2010, 10:11-23.
34. Hanke T., Goonetilleke N., McMichael A.J., Dorrell L. 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 2007, 88:1-12.
35. Rodríguez-García M., Climent N., Oliva H., Casanova V., Franco R., Leon A., et al. Increased alpha-defensins 1-3 production by dendritic cells in HIV-infected individuals is associated with slower disease progression. PLoS One 2010, 5:e9436.
36. Liard C., Munier S., Arias M., Joulin-Giet A., Bonduelle O., Duffy D., et al. Targeting of HIV-p24 particle-based vaccine into differential skin layers induces distinct arms of the immune responses. Vaccine 2011, 29:6379-6391.
37. Ramirez J.C., Gherardi M.M., Esteban M. 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 2000, 74:923-933.
38. Gómez C.E., Nájera J.L., Jiménez E.P., Jiménez V., Wagner R., Graf M., et al. 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 2007, 25:2863-2885.
39. Drexler I., Antunes E., Schmitz M., Wölfel T., Huber C., Erfle V., et al. Modified vaccinia virus Ankara for delivery of human tyrosinase as melanoma-associated antigen: induction of tyrosinase- and melanoma-specific human leukocyte antigen A*0201-restricted cytotoxic T cells in vitro and in vivo. Cancer Res 1999, 59:4955-4963.
40. Kim G.G., Donnenberg V.S., Donnenberg A.D., Gooding W., Whiteside T.L. A novel multiparametric flow cytometry-based cytotoxicity assay simultaneously immunophenotypes effector cells: comparisons to a 4h 51Cr-release assay. J Immunol Methods 2007, 325:51-66.
41. Mahe B., Vogt A., Liard C., Duffy D., Abadie V., Bonduelle O., et al. Nanoparticle-based targeting of vaccine compounds to skin antigen-presenting cells by hair follicles and their transport in mice. J Invest Dermatol 2009, 129:1156-1164.
42. Combadiere B., Mahe B. Particle-based vaccines for transcutaneous vaccination. Comp Immunol Microbiol Infect Dis 2008, 31:293-315.
43. Weber C., Drogoz A., David L., Domard A., Charles M.H., Verrier B., et al. Polysaccharide-based vaccine delivery systems: macromolecular assembly, interactions with antigen presenting cells, and in vivo immunomonitoring. J Biomed Mater Res A 2010, 93:1322-1334.
44. Jonuleit H., Kühn U., Müller G., Steinbrink K., Paragnik L., Schmitt E., et al. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol 1997, 27:3135-3142.
45. Kim H.J., Kim H.O., Lee K., Baek E.J., Kim H.S. Two-step maturation of immature DCs with proinflammatory cytokine cocktail and poly(I:C) enhances migratory and T cell stimulatory capacity. Vaccine 2010, 28:2877-2886.
46. Rancan F., Amselgruber S., Hadam S., Munier S., Pavot V., Verrier B., et al. Particle-based transcutaneous administration of HIV-1 p24 protein to human skin explants and targeting of epidermal antigen presenting cells. J Controlled Release 2014, 176:115-122.
47. Casanova V., Naval-Macabuhay I., Massanella M., Rodríguez-García M., Blanco J., Gatell J.M., et al. Adenosine deaminase enhances the immunogenicity of human dendritic cells from healthy and HIV-infected individuals. PLoS One 2012, 7:e51287.
48. Hernández J.C., Stevenson M., Latz E., Urcuqui-Inchima S. HIV type 1 infection up-regulates TLR2 and TLR4 expression and function in vivo and in vitro. AIDS Res Hum Retroviruses 2012, 28:1313-1328.
49. Hashida S., Hashinaka K., Ishikawa S., Ishikawa E. More reliable diagnosis of infection with human immunodeficiency virus type 1 (HIV-1) by detection of antibody IgGs to pol and gag proteins of HIV-1 and p24 antigen of HIV-1 in urine, saliva, and/or serum with highly sensitive and specific enzyme immunoassay (immune complex transfer enzyme immunoassay): a review. J Clin Lab Anal 1997, 11:267-286.
50. Guilliams M., Bruhns P., Saeys Y., Hammad H., Lambrecht B.N. The function of Fcγ receptors in dendritic cells and macrophages. Nat Rev Immunol 2014, 14:94-108.
51. Reddy S.T., Swartz M.A., Hubbell J.A. Targeting dendritic cells with biomaterials: developing the next generation of vaccines. Trends Immunol 2006, 27:573-579.
52. Guerra S., Najera J.L., Gonzalez J.M., Lopez-Fernandez L.A., Climent N., Gatell J.M., et al. Distinct gene expression profiling after infection of immature human monocyte-derived dendritic cells by the attenuated poxvirus vectors MVA and NYVAC. J Virol 2007, 81:8707-8721.
53. Guerra S., Gonzalez J.M., Climent N., Reyburn H., Lopez-Fernandez L.A., Nájera J.L., et al. Selective induction of host genes by MVA-B, a candidate vaccine against HIV/AIDS. J Virol 2010, 84:8141-8152.
54. Vendrame D., Sourisseau M., Perrin V., Schwartz O., Mammano F. Partial inhibition of human immunodeficiency virus replication by type I interferons: impact of cell-to-cell viral transfer. J Virol 2009, 83:10527-10537.
55. Berger E.A., Murphy P.M., Farber J.M. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 1999, 17:657-700.
56. Promadej-Lanier N., Hanson D.L., Srinivasan P., Luo W., Adams D.R., Guenthner P.C., et al. 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 2010, 53:574-581.
57. Trucco M., Giannoukakis N. Immunoregulatory dendritic cells to prevent and reverse new-onset Type 1 diabetes mellitus. Expert Opin Biol Ther 2007, 7:951-963.
58. Messmer D., Jacqué J.M., Santisteban C., Bristow C., Han S.Y., Villamide-Herrera L., et al. Endogenously expressed nef uncouples cytokine and chemokine production from membrane phenotypic maturation in dendritic cells. J Immunol 2002, 169:4172-4182.
59. Sarkar R., Mitra D., Chakrabarti S. HIV-1 gp120 protein downregulates Nef induced IL-6 release in immature dentritic cells through interplay of DC-SIGN. PLoS One 2013, 8:e59073.
60. Mangino G., Percario Z.A., Fiorucci G., Vaccari G., Acconcia F., Chiarabelli C., et al. HIV-1 Nef induces proinflammatory state in macrophages through its acidic cluster domain: involvement of TNF alpha receptor associated factor 2. PLoS One 2011, 6:e22982.
61. Mothe B., Llano A., Ibarrondo J., Zamarreño J., Schiaulini M., Miranda C., et al. CTL responses of high functional avidity and broad variant cross-reactivity are associated with HIV control. PLoS One 2012, 7:e29717.
62. + T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 2007, 13:46-53.
63. + T cells: correlation with viral load. J Virol 2004, 78:3233-3243.
64. Zuñiga R., Lucchetti A., Galvan P., Sanchez S., Sanchez C., Hernandez A., et al. Relative dominance of Gag p24-specific cytotoxic T lymphocytes is associated with human immunodeficiency virus control. J Virol 2006, 80:3122-3125.
65. Lai L., Kwa S.F., Kozlowski P.A., Montefiori D.C., Nolen T.L., Hudgens M.G., et al. SIVmac239 MVA vaccine with and without a DNA prime, similar prevention of infection by a repeated dose SIVsmE660 challenge despite different immune responses. Vaccine 2012, 30:1737-1745.
66. Brown S.A., Surman S.L., Sealy R., Jones B.G., Slobod K.S., Branum K., et al. Heterologous prime-boost HIV-1 vaccination regimens in pre-clinical and clinical trials. Viruses 2010, 2:435-467.
67. Hansen S.G., Ford J.C., Lewis M.S., Ventura A.B., Hughes C.M., Coyne-Johnson L., et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 2011, 473:523-527.
68. Belisle S.E., Yin J., Shedlock D.J., Dai A., Yan J., Hirao L., et al. Long-term programming of antigen-specific immunity from gene expression signatures in the PBMC of rhesus macaques immunized with an SIV DNA vaccine. PLoS One 2011, 6:e19681.
69. Pillai V.K., Kannanganat S., Penaloza-Macmaster P., Chennareddi L., Robinson H.L., Blackwell J., et al. Different patterns of expansion, contraction and memory differentiation of HIV-1 Gag-specific CD8 T cells elicited by adenovirus type 5 and modified vaccinia Ankara vaccines. Vaccine 2011, 29:5399-5406.