Immunization of neonatal mice with LAMP/p55 HIV gag DNA elicits robust immune responses that last to adulthood

Virology

Volumn 406, Issue 1, 2010, Pages 37-47

  Rigato, Paula Ordonhez ^a   Maciel, Milton ^b   Goldoni, Adriana Letícia ^a   Piubelli, Orlando ^a   de Brito, Cyro Alves ^a   Fusaro, Ana Elisa ^a   Eurico de Alencar, Liciana Xavier ^d   August, Thomas ^c   Azevedo Marques, Ernesto Torres ^d,e   da Silva Duarte, Alberto José ^a   Sato, Maria Notomi ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF MARYLAND   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d INSTITUTO OSWALDO CRUZ   (Brazil)

^e Center for Vaccine Research   (United States)

Author keywords

DNA vaccine; HIV 1; Immunological memory; Mice; Neonatal

Indexed keywords

ANTIBODY; CD4 ANTIGEN; CYTOKINE; DNA VACCINE; GAG PROTEIN; GAMMA INTERFERON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PROTEIN P55; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; P55 GAG PRECURSOR PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN PRECURSOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; DNA IMMUNIZATION; DRUG DOSE INCREASE; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOGENICITY; IMMUNOLOGICAL MEMORY; LOW DRUG DOSE; MALE; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VIRUS IMMUNITY; ANIMAL; BAGG ALBINO MOUSE; GENETICS; HIV INFECTIONS; IMMUNIZATION; IMMUNOLOGY; T LYMPHOCYTE SUBPOPULATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; MUS;

AIDS VACCINES; ANIMALS; ANIMALS, NEWBORN; FEMALE; HIV INFECTIONS; HIV-1; IMMUNIZATION; IMMUNIZATION, SECONDARY; IMMUNOLOGIC MEMORY; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MALE; MICE; MICE, INBRED BALB C; PROTEIN PRECURSORS; T-LYMPHOCYTE SUBSETS; VACCINES, DNA;

EID: 77956177205     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.06.050     Document Type: Article

References (45)

1. Adkins B. Peripheral CD4+ lymphocytes derived from fetal versus adult thymic precursors differ phenotypically and functionally. J. Immunol. 2003, 171(10):5157-5164.
2. Adkins B., Leclerc C., Marshall-Clarke S. Neonatal adaptive immunity comes of age. Nat. Rev. Immunol. 2004, 4(7):553-564.
3. Amanna I.J., Slifka M.K., Crotty S. Immunity and immunological memory following smallpox vaccination. Immunol. Rev. 2006, 211:320-337.
4. Arruda L.B., Sim D., Chikhlikar P.R., et al. Dendritic cell-lysosomal-associated membrane protein (LAMP) and LAMP-1-HIV-1 gag chimeras have distinct cellular trafficking pathways and prime T and B cell responses to a diverse repertoire of epitopes. J. Immunol. 2006, 177(4):2265-2275.
5. Bennett S.R., Carbone F.R., Karamalis F., Miller J.F., Heath W.R. Induction of a CD8+ cytotoxic T lymphocyte response by cross-priming requires cognate CD4+ T cell help. J. Exp. Med. 1997, 186(1):65-70.
6. Blanche S., Newell M.L., Mayaux M.J., et al. Morbidity and mortality in European children vertically infected by HIV-1. The French Pediatric HIV Infection Study Group and European Collaborative Study. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 1997, 14(5):442-450.
7. Brito C.A., Goldoni A.L., Sato M.N. Immune adjuvants in early life: targeting the innate immune system to overcome impaired adaptive response. Immunotherapy 2009, 1:883-895.
8. Buseyne F., Le Chenadec J., Corre B., Porrot F., Burgard M., et al. Inverse correlation between memory Gag-specific cytotoxic T lymphocytes and viral replication in human immunodeficiency virus-infected children. J. Infect. Dis. 2002, 186:1589-1596.
9. Calarota S.A., Weiner D.B. Approaches for the design and evaluation of HIV-1 DNA vaccines. Expert Rev. Vaccin. 2004, 3(4 Suppl):S135-S149.
10. Capozzo A.V., Ramirez K., Polo J.M., et al. Neonatal immunization with a Sindbis virus-DNA measles vaccine induces adult-like neutralizing antibodies and cell-mediated immunity in the presence of maternal antibodies. J. Immunol. 2006, 176(9):5671-5681.
11. Cassese G., Arce S., Hauser A.E., et al. Plasma cell survival is mediated by synergistic effects of cytokines and adhesion-dependent signals. J. Immunol. 2003, 171(4):1684-1690.
12. Chan K., Lee D.J., Schubert A., et al. The roles of MHC class II, CD40, and B7 costimulation in CTL induction by plasmid DNA. J. Immunol. 2001, 166(5):3061-3066.
13. Cheng W.F., Hung C.F., Chai C.Y., et al. Tumor-specific immunity and antiangiogenesis generated by a DNA vaccine encoding calreticulin linked to a tumor antigen. J. Clin. Invest. 2001, 108(5):669-678.
14. Chikhlikar P., Barros de Arruda L., Agrawal S., et al. Inverted terminal repeat sequences of adeno-associated virus enhance the antibody and CD8(+) responses to a HIV-1 p55Gag/LAMP DNA vaccine chimera. Virology 2004, 323(2):220-232.
15. Chikhlikar P., de Arruda L.B., Maciel M., et al. DNA encoding an HIV-1 Gag/human lysosome-associated membrane protein-1 chimera elicits a broad cellular and humoral immune response in Rhesus macaques. PLoS ONE 2006, 1:e135.
16. Coelho-Castelo A.A., Trombone A.P., Rosada R.S., Santos R.R., Bonato V.L., Sartori A., Silva C.L. Tissue distribution of a plasmid DNA encoding Hsp65 gene is dependent on the dose administered through intramuscular delivery. Genet. Vaccines Ther. 2006, 4:1.
17. de Arruda L.B., Chikhlikar P.R., August J.T., Marques E.T. DNA vaccine encoding human immunodeficiency virus-1 Gag, targeted to the major histocompatibility complex II compartment by lysosomal-associated membrane protein, elicits enhanced long-term memory response. Immunology 2004, 112(1):126-133.
18. Dorner T., Radbruch A. Antibodies and B cell memory in viral immunity. Immunity 2007, 27(3):384-392.
19. Forsthuber T., Yip H.C., Lehmann P.V. Induction of TH1 and TH2 immunity in neonatal mice. Science 1996, 271(5256):1728-1730.
20. Gold M.C., Robinson T.L., Cook M.S., et al. Human neonatal dendritic cells are competent in MHC class I antigen processing and presentation. PLoS ONE 2007, 2(9):e957.
21. Kessler P.D., Podsakoff G.M., Chen X., et al. Gene delivery to skeletal muscle results in sustained expression and systemic delivery of a therapeutic protein. Proc. Natl Acad. Sci. USA 1996, 93(24):14082-14087.
22. Lichterfeld M., Yu X.G., Waring M.T., et al. HIV-1-specific cytotoxicity is preferentially mediated by a subset of CD8(+) T cells producing both interferon-gamma and tumor necrosis factor-alpha. Blood 2004, 104(2):487-494.
23. Lu S., Wang S., Grimes-Serrano J.M. Current progress of DNA vaccine studies in humans. Expert Rev. Vaccin. 2008, 7(2):175-191.
24. Maecker H.T., Umetsu D.T., DeKruyff R.H., Levy S. Cytotoxic T cell responses to DNA vaccination: dependence on antigen presentation via class II MHC. J. Immunol. 1998, 161(12):6532-6536.
25. Marques E.T., Chikhlikar P., de Arruda L.B., et al. HIV-1 p55Gag encoded in the lysosome-associated membrane protein-1 as a DNA plasmid vaccine chimera is highly expressed, traffics to the major histocompatibility class II compartment, and elicits enhanced immune responses. J. Biol. Chem. 2003, 278(39):37926-37936.
26. Martinez X., Brandt C., Saddallah F., et al. DNA immunization circumvents deficient induction of T helper type 1 and cytotoxic T lymphocyte responses in neonates and during early life. Proc. Natl Acad. Sci. USA 1997, 94(16):8726-8731.
27. Mayaux M.J., Burgard M., Teglas J.P., et al. Neonatal characteristics in rapidly progressive perinatally acquired HIV-1 disease. The French Pediatric HIV Infection Study Group. Jama 1996, 275(8):606-610.
28. Min B., Legge K.L., Bell J.J., et al. Neonatal exposure to antigen induces a defective CD40 ligand expression that undermines both IL-12 production by APC and IL-2 receptor up-regulation on splenic T cells and perpetuates IFN-gamma-dependent T cell anergy. J. Immunol. 2001, 166(9):5594-5603.
29. Muthukkumar S., Goldstein J., Stein K.E. The ability of B cells and dendritic cells to present antigen increases during ontogeny. J. Immunol. 2000, 165(9):4803-4813.
30. Pihlgren M., Schallert N., Tougne C., et al. Delayed and deficient establishment of the long-term bone marrow plasma cell pool during early life. Eur. J. Immunol. 2001, 31(3):939-946.
31. Rigato P.O., Fusaro A.E., Victor J.R., Sato M.N. Maternal immunization to modulate the development of allergic response and pathogen infections. Immunotherapy 2009, 1:141-156.
32. Rose S., Lichtenheld M., Foote M.R., Adkins B. Murine neonatal CD4+ cells are poised for rapid Th2 effector-like function. J. Immunol. 2007, 178(5):2667-2678.
33. Sacha J.B., Chung C., Rakasz E.G., et al. Gag-specific CD8+ T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J. Immunol. 2007, 178(5):2746-2754.
34. Sarzotti M., Robbins D.S., Hoffman P.M. Induction of protective CTL responses in newborn mice by a murine retrovirus. Science 1996, 271(5256):1726-1728.
35. Sedegah M., Belmonte M., Epstein J.E., et al. Successful induction of CD8 T cell-dependent protection against malaria by sequential immunization with DNA and recombinant poxvirus of neonatal mice born to immune mothers. J. Immunol. 2003, 171(6):3148-3153.
36. Siegrist C.A. Neonatal and early life vaccinology. Vaccine 2001, 19(25-26):3331-3346.
37. Siegrist C.A. The challenges of vaccine responses in early life: selected examples. J. Comp. Pathol. 2007, 137(Suppl 1):S4-S9.
38. Simon G.G., Hu Y., Khan A.M., Zhou J., et al. Dendritic cell mediated delivery of plasmid DNA encoding LAMP/HIV-1 Gag fusion immunogen enhances T cell epitope responses in HLA DR4 transgenic mice. PLoS ONE 2010, 5(1):e8574.
39. Simpson C.C., Woods G.M., Muller H.K. Impaired CD40-signalling in Langerhans' cells from murine neonatal draining lymph nodes: implications for neonatally induced cutaneous tolerance. Clin. Exp. Immunol. 2003, 132(2):201-208.
40. Stevenson F.K. DNA vaccines and adjuvants. Immunol. Rev. 2004, 199:5-8.
41. AIDS Epidemic Update 2008, UNAIDS.
42. Valentin A., Chikhlikar P., Patel V., et al. Comparison of DNA vaccines producing HIV-1 Gag and LAMP/Gag chimera in rhesus macaques reveals antigen-specific T-cell responses with distinct phenotypes. Vaccine 2009, 27(35):4840-4849.
43. Xin K.Q., Sasaki S., Kojima Y., et al. Detection of progeny immune responses after intravenous administration of DNA vaccine to pregnant mice. Biol. Proced. Online 2002, 3:91-101.
44. Xin K.Q., Ooki T., Jounai N., et al. A DNA vaccine containing inverted terminal repeats from adeno-associated virus increases immunity to HIV. J. Gene Med. 2003, 5(5):438-445.
45. Zhang J., Silvestri N., Whitton J.L., Hassett D.E. Neonates mount robust and protective adult-like CD8(+)-T-cell responses to DNA vaccines. J. Virol. 2002, 76(23):11911-11919.