Priming with a very low dose of DNA complexed with cationic block copolymers followed by protein boost elicits broad and long-lasting antigen-specific humoral and cellular responses in mice

Vaccine

Volumn 27, Issue 33, 2009, Pages 4498-4507

  Voltan, Rebecca ^a   Castaldello, Arianna ^a   Brocca Cofano, Egidio ^a   De Michele, Rita ^a   Triulzi, Chiara ^a   Altavilla, Giuseppe ^a   Tondelli, Luisa ^b   Laus, Michele ^c   Sparnacci, Katia ^c   Reali, Eva ^d   Gavioli, Riccardo ^d   Ensoli, Barbara ^e   Caputo, Antonella ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^d UNIVERSITY OF FERRARA   (Italy)

^e ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Cationic block copolymers; DNA vaccination; Prime boost

Indexed keywords

CATIONIC BLOCK COPOLYMER; COPOLYMER; DNA VACCINE; PCV TAT DNA VACCINE; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; ENZYME DEGRADATION; FEMALE; HUMORAL IMMUNITY; IMMUNIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; VACCINATION;

ADJUVANTS, IMMUNOLOGIC; AIDS VACCINES; ANIMALS; CATIONS; CELL PROLIFERATION; CYTOKINES; EPITOPE MAPPING; FEMALE; HIV ANTIBODIES; HIV ANTIGENS; IMMUNITY, CELLULAR; IMMUNOGLOBULIN G; INJECTIONS, INTRAMUSCULAR; MICE; MICE, INBRED BALB C; POLYMERS; SPLEEN; T-LYMPHOCYTES, CYTOTOXIC; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TH1 CELLS; VACCINES, DNA;

EID: 67649321235     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2009.05.031     Document Type: Article

References (68)

1. Garmory H.S., Perkins S.D., Phillpotts R.J., and Titball R.W. DNA vaccines for biodefence. Adv Drug Deliv Rev 57 9 (2005) 1343-1361
2. Donnelly J.J., Wahren B., and Liu M.A. DNA vaccines: progress and challenges. J Immunol 175 2 (2005) 633-639
3. Gurunathan S., Wu C.Y., Freidag B.L., and Seder R.A. DNA vaccines: a key for inducing long-term cellular immunity. Curr Opin Immunol 12 4 (2000) 442-447
4. Pachuk C.J., McCallus D.E., Weiner D.B., and Satishchandran C. DNA vaccines-challenges in delivery. Curr Opin Mol Ther 2 2 (2000) 188-198
5. O'Hagan D.T., Singh M., and Ulmer J.B. Microparticles for the delivery of DNA vaccines. Immunol Rev 199 (2004) 191-200
6. Wack A., and Rappuoli R. Vaccinology at the beginning of the 21st century. Curr Opin Immunol 17 4 (2005) 411-418
7. Dincer S., Turk M., and Piskin E. Intelligent polymers as nonviral vectors. Gene Ther 12 Suppl. 1 (2005) S139-S145
8. Lee M., and Kim S.W. Polyethylene glycol-conjugated copolymers for plasmid DNA delivery. Pharm Res 22 1 (2005) 1-10
9. Garnett M.C. Gene-delivery systems using cationic polymers. Crit Rev Ther Drug Carrier Syst 16 2 (1999) 147-207
10. Kushibiki T., and Tabata Y. A new gene delivery system based on controlled release technology. Curr Drug Deliv 1 2 (2004) 153-163
11. Prasmickaite L., Hogset A., Tjelle T.E., Olsen V.M., and Berg K. Role of endosomes in gene transfection mediated by photochemical internalisation (PCI). J Gene Med 2 6 (2000) 477-488
12. Laus M., Sparnacci K., Ensoli B., Butto S., Caputo A., Mantovani I., et al. Complex associates of plasmid DNA and a novel class of block copolymers with PEG and cationic segments as new vectors for gene delivery. J Biomater Sci Polym Ed 12 2 (2001) 209-228
13. Caputo A., Betti M., Altavilla G., Bonaccorsi A., Boarini C., Marchisio M., et al. Micellar-type complexes of tailor-made synthetic block copolymers containing the HIV-1 tat DNA for vaccine application. Vaccine 20 17-18 (2002) 2303-2317
14. Caputo A., Gavioli R., Altavilla G., Brocca-Cofano E., Boarini C., Betti M., et al. Immunization with low doses of HIV-1 tat DNA delivered by novel cationic block copolymers induces CTL responses against Tat. Vaccine 21 11-12 (2003) 1103-1111
15. Cafaro A., Titti F., Fracasso C., Maggiorella M.T., Baroncelli S., Caputo A., et al. Vaccination with DNA containing tat coding sequences and unmethylated CpG motifs protects cynomolgus monkeys upon infection with simian/human immunodeficiency virus (SHIV89.6P). Vaccine 19 20-22 (2001) 2862-2877
16. Caputo A., Brocca-Cofano E., Castaldello A., De Michele R., Altavilla G., Marchisio M., et al. Novel biocompatible anionic polymeric microspheres for the delivery of the HIV-1 Tat protein for vaccine application. Vaccine 22 21-22 (2004) 2910-2924
17. Caselli E., Betti M., Grossi M.P., Balboni P.G., Rossi C., Boarini C., et al. DNA immunization with HIV-1 tat mutated in the trans activation domain induces humoral and cellular immune responses against wild-type Tat. J Immunol 162 9 (1999) 5631-5638
18. Ramakrishna L., Anand K.K., Mohankumar K.M., and Ranga U. Codon optimization of the tat antigen of human immunodeficiency virus type 1 generates strong immune responses in mice following genetic immunization. J Virol 78 17 (2004) 9174-9189
19. Hinkula J., Lundholm P., and Wahren B. Nucleic acid vaccination with HIV regulatory genes: a combination of HIV-1 genes in separate plasmids induces strong immune responses. Vaccine 15 8 (1997) 874-878
20. Hinkula J., Svanholm C., Schwartz S., Lundholm P., Brytting M., Engstrom G., et al. Recognition of prominent viral epitopes induced by immunization with human immunodeficiency virus type 1 regulatory genes. J Virol 71 7 (1997) 5528-5539
21. Tahtinen M., Strengell M., Collings A., Pitkanen J., Kjerrstrom A., Hakkarainen K., et al. DNA vaccination in mice using HIV-1 nef, rev and tat genes in self-replicating pBN-vector. Vaccine 19 15-16 (2001) 2039-2047
22. Calarota S., Bratt G., Nordlund S., Hinkula J., Leandersson A.C., Sandstrom E., et al. Cellular cytotoxic response induced by DNA vaccination in HIV-1-infected patients. Lancet 351 9112 (1998) 1320-1325
23. Ensoli B., Fiorelli V., Ensoli F., Cafaro A., Titti F., Butto S., et al. Candidate HIV-1 Tat vaccine development: from basic science to clinical trials. AIDS 20 (2006) 2245-2261
24. Ensoli B., Fiorelli V., Ensoli F., Lazzarin A., Visintini R., Narciso P., et al. The therapeutic phase I trial of the recombinant native HIV-1 Tat protein. AIDS 22 16 (2008) 2207-2209
25. Gavioli R., Gallerani E., Fortini C., Fabris M., Bottoni A., Canella A., et al. HIV-1 tat protein modulates the generation of cytotoxic T cell epitopes by modifying proteasome composition and enzymatic activity. J Immunol 173 6 (2004) 3838-3843
26. Ensoli B. Introduction: rational vaccine strategies against AIDS. Microbes Infect 7 14 (2005) 1385
27. Ensoli B. Criteria for selection of HIV vaccine candidates-general principles. Microbes Infect 7 14 (2005) 1433-1435
28. Ensoli B. Rational vaccine strategies against AIDS: background and rationale. Microbes Infect 7 14 (2005) 1445-1452
29. Gavioli R., Cellini S., Castaldello A., Voltan R., Gallerani E., Gagliardoni F., et al. The Tat protein broadens T cell responses directed to the HIV-1 antigens Gag and Env: implications for the design of new vaccines against AIDS. Vaccine 26 (2007) 727-737
30. Caputo A., Brocca-Cofano E., Castaldello A., Voltan R., Gavioli R., Srivastava I.K., et al. Characterization of immune responses elicited in mice by intranasal co-immunization with HIV-1 Tat, gp140 DeltaV2Env and/or SIV Gag proteins and the nontoxicogenic heat-labile Escherichia coli enterotoxin. Vaccine 26 (2008) 1214-1227
31. Arya S.K., Guo C., Josephs S.F., and Wong-Staal F. Trans-activator gene of human T-lymphotropic virus type III (HTLV-III). Science 229 4708 (1985) 69-73
32. Chang H.C., Samaniego F., Nair B.C., Buonaguro L., and Ensoli B. HIV-1 Tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrix-associated heparan sulfate proteoglycans through its basic region. AIDS 11 12 (1997) 1421-1431
33. Ensoli B., Buonaguro L., Barillari G., Fiorelli V., Gendelman R., Morgan R.A., et al. Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J Virol 67 1 (1993) 277-287
34. Davis L., Dibner M., and Battey J. In: Davis L., Dibner, and MBattey J. (Eds). Basic methods in molecular biology (1986), Elsevier, New York
35. Fanales-Belasio E., Moretti S., Nappi F., Barillari G., Micheletti F., Cafaro A., et al. Native HIV-1 Tat protein targets monocyte-derived dendritic cells and enhances their maturation, function, and antigen-specific T cell responses. J Immunol 168 1 (2002) 197-206
36. Castaldello A., Brocca-Cofano E., Voltan R., Triulzi C., Altavilla G., Laus M., et al. DNA prime and protein boost immunization with innovative polymeric cationic core-shell nanoparticles elicits broad immune responses and strongly enhance cellular responses of HIV-1 tat DNA vaccination. Vaccine 24 (2006) 5655-5669
37. Sokak R., and Rohlf F. Estimation and hypothesys testing. In: Sokak, and RRohlf F. (Eds). Biometry: the principles and practice of statistics in biological research (1981), Freeman, San Francisco 128-135
38. Caputo A., Gavioli R., and Ensoli B. Recent advances in the development of HIV-1 Tat-based vaccines. Curr HIV Res 2 4 (2004) 357-376
39. Scriba T.J., zur Megede J., Glashoff R.H., Treurnicht F.K., Barnett S.W., and van Rensburg E.J. Functionally-inactive and immunogenic Tat, Rev and Nef DNA vaccines derived from sub-Saharan subtype C human immunodeficiency virus type 1 consensus sequences. Vaccine 23 9 (2005) 1158-1169
40. Ferrantelli F., Cafaro A., and Ensoli B. Nonstructural HIV proteins as targets for prophylactic or therapeutic vaccines. Curr Opin Biotechnol 15 6 (2004) 543-556
41. Ensoli B., and Cafaro A. Novel strategies toward the development of an effective vaccine to prevent human immunodeficiency virus infection or acquired immunodeficiency virus. AIDS Clin Rev (2000) 23-61
42. Rosenberg E.S., and Walker B.D. HIV type 1-specific helper T cells: a critical host defense. AIDS Res Hum Retroviruses 14 Suppl. 2 (1998) S143-S147
43. Rosenberg E.S., Billingsley J.M., Caliendo A.M., Boswell S.L., Sax P.E., Kalams S.A., et al. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278 5342 (1997) 1447-1450
44. Sun J.C., and Bevan M.J. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300 5617 (2003) 339-342
45. Sun J.C., Williams M.A., and Bevan M.J. CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol 5 9 (2004) 927-933
46. Altfeld M., and Rosenberg E.S. The role of CD4(+) T helper cells in the cytotoxic T lymphocyte response to HIV-1. Curr Opin Immunol 12 4 (2000) 375-380
47. Kalams S.A., and Walker B.D. The critical need for CD4 help in maintaining effective cytotoxic T lymphocyte responses. J Exp Med 188 12 (1998) 2199-2204
48. Shedlock D.J., and Shen H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300 5617 (2003) 337-339
49. Banchereau J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y.J., et al. Immunobiology of dendritic cells. Annu Rev Immunol 18 (2000) 767-811
50. Banchereau J., and Steinman R.M. Dendritic cells and the control of immunity. Nature 392 6673 (1998) 245-252
51. Hel Z., Tsai W.P., Tryniszewska E., Nacsa J., Markham P.D., Lewis M.G., et al. Improved vaccine protection from simian AIDS by the addition of nonstructural simian immunodeficiency virus genes. J Immunol 176 1 (2006) 85-96
52. van Baalen C.A., Pontesilli O., Huisman R.C., Geretti A.M., Klein M.R., de Wolf F., et al. Human immunodeficiency virus type 1 Rev- and Tat-specific cytotoxic T lymphocyte frequencies inversely correlate with rapid progression to AIDS. J Gen Virol 78 (1997) 1913-1918
53. Barillari G., and Ensoli B. Angiogenic effects of extracellular human immunodeficiency virus type 1 Tat protein and its role in the pathogenesis of AIDS-associated Kaposi's sarcoma. Clin Microbiol Rev 15 2 (2002) 310-326
54. Steinaa L., Sorensen A.M., Nielsen J.O., and Hansen J.E. Antibody to HIV-1 Tat protein inhibits the replication of virus in culture. Arch Virol 139 3-4 (1994) 263-271
55. Butto S., Fiorelli V., Tripiciano A., Ruiz-Alvarez M.J., Scoglio A., Ensoli F., et al. Sequence conservation and antibody cross-recognition of clade B human immunodeficiency virus (HIV) type 1 Tat protein in HIV-1-infected Italians, Ugandans, and South Africans. J Infect Dis 188 8 (2003) 1171-1180
56. Kittiworakarn J., Lecoq A., Moine G., Thai R., Lajeunesse E., Drevet P., et al. HIV-1 Tat raises an adjuvant-free humoral immune response controlled by its core region and its ability to form cysteine-mediated oligomers. J Biol Chem 281 6 (2006) 3105-3115
57. Schwarze S.R., Hruska K.A., and Dowdy S.F. Protein transduction: unrestricted delivery into all cells?. Trends Cell Biol 10 7 (2000) 290-295
58. Addo M.M., Altfeld M., Rosenberg E.S., Eldridge R.L., Philips M.N., Habeeb K., et al. The HIV-1 regulatory proteins Tat and Rev are frequently targeted by cytotoxic T lymphocytes derived from HIV-1-infected individuals. Proc Natl Acad Sci USA 98 4 (2001) 1781-1786
59. Krone W.J., Debouck C., Epstein L.G., Heutink P., Meloen R., and Goudsmit J. Natural antibodies to HIV-tat epitopes and expression of HIV-1 genes in vivo. J Med Virol 26 3 (1988) 261-270
60. Re M.C., Furlini G., Vignoli M., Ramazzotti E., Roderigo G., De Rosa V., et al. Effect of antibody to HIV-1 Tat protein on viral replication in vitro and progression of HIV-1 disease in vivo. J Acquir Immune Defic Syndr Hum Retrovirol 10 4 (1995) 408-416
61. Re M.C., Furlini G., Vignoli M., Ramazzotti E., Zauli G., and La Placa M. Antibody against human immunodeficiency virus type 1 (HIV-1) Tat protein may have influenced the progression of AIDS in HIV-1-infected hemophiliac patients. Clin Diagn Lab Immunol 3 2 (1996) 230-232
62. Re M.C., Vignoli M., Furlini G., Gibellini D., Colangeli V., Vitone F., et al. Antibodies against full-length Tat protein and some low-molecular-weight Tat-peptides correlate with low or undetectable viral load in HIV-1 seropositive patients. J Clin Virol 21 1 (2001) 81-89
63. Rezza G., Fiorelli V., Dorrucci M., Ciccozzi M., Tripiciano A., Scoglio A., et al. The presence of anti-Tat antibodies is predictive of long-term nonprogression to AIDS or severe immunodeficiency: findings in a cohort of HIV-1 seroconverters. J Infect Dis 191 8 (2005) 1321-1324
64. Rodman T.C., Pruslin F.H., To S.E., and Winston R. Human immunodeficiency virus (HIV) Tat-reactive antibodies present in normal HIV-negative sera and depleted in HIV-positive sera. Identification of the epitope. J Exp Med 175 5 (1992) 1247-1253
65. Ensoli B., and Cafaro A. Control of viral replication and disease onset in cynomolgus monkeys by HIV-1 TAT vaccine. J Biol Regul Homeost Agents 14 1 (2000) 22-26
66. Spearman P. HIV vaccine development: lessons from the past and promise for the future. Curr HIV Res 1 1 (2003) 101-120
67. McMichael A.J., and Hanke T. HIV vaccines 1983-2003. Nat Med 9 7 (2003) 874-880
68. Goulder P.J., Rowland-Jones S.L., McMichael A.J., and Walker B.D. Anti-HIV cellular immunity: recent advances towards vaccine design. AIDS 13 Suppl. A (1999) S121-S136