Single epitope mucosal vaccine delivered via immuno-stimulating complexes induces low level of immunity against simian-HIV

Vaccine

Volumn 24, Issue 47-48, 2006, Pages 6839-6849

  Pahar, Bapi ^a   Cantu, Mayra A ^a   Zhao, Wei ^a   Kuroda, Marcelo J ^a   Veazey, Ronald S ^a   Montefiori, David C ^b   Clements, John D ^c   Aye, Pyone P ^a   Lackner, Andrew A ^a   Lovgren Bengtsson, Karin ^d   Sestak, Karol ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Uppsala Innovation Center   (Sweden)

Author keywords

HIV; Mucosal route; Peptide vaccine; Rhesus macaque; SIV

Indexed keywords

ISCOM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOSTIMULATION; NONHUMAN; PREDICTION; PRIORITY JOURNAL; RHESUS MONKEY; RNA ANALYSIS; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODY FORMATION; ANTIGENS, CD95; CD4-POSITIVE T-LYMPHOCYTES; EPITOPES; GENE PRODUCTS, GAG; IMMUNITY, CELLULAR; IMMUNITY, MUCOSAL; IMMUNIZATION; INTERFERON TYPE II; KI-67 ANTIGEN; MACACA MULATTA; NEUTRALIZATION TESTS; PHENOTYPE; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 33846254613     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2006.06.050     Document Type: Article

References (67)

1. Ahlers J.D., Pendleton C.D., Dunlop N., Minassian A., Nara P.L., and Berzofsky J.A. Construction of an HIV-1 peptide vaccine containing a multideterminant helper peptide linked to a V3 loop peptide 18 inducing strong neutralizing antibody responses in mice of multiple MHC haplotypes after two immunizations. J Immunol 150 12 (1993) 5647-5665
2. Allen T.M., Mothe B.R., Sidney J., Jing P., Dzuris J.L., Liebl M.E., et al. CD8(+) lymphocytes from simian immunodeficiency virus-infected rhesus macaques recognize 14 different epitopes bound by the major histocompatibility complex class I molecule Mamu-A*01: implications for vaccine design and testing. J Virol 75 2 (2001) 738-749
3. Barouch D.H., Powers J., Truitt D.M., Kishko M.G., Arthur J.C., Peyerl F.W., et al. Dynamic immune responses maintain cytotoxic T lymphocyte epitope mutations in transmitted simian immunodeficiency virus variants. Nat Immunol 6 3 (2005) 247-252
4. Belyakov I.M., Hel Z., Kelsall B., Kuznetsov V.A., Ahlers J.D., Nacsa J., et al. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat Med 7 12 (2001) 1320-1326
5. Fouts T., Godfrey K., Bobb K., Montefiori D., Hanson C.V., Kalyanaraman V.S., et al. Crosslinked HIV-1 envelope-CD4 receptor complexes elicit broadly cross-reactive neutralizing antibodies in rhesus macaques. Proc Natl Acad Sci USA 99 18 (2002) 11842-11847
6. Gomez-Roman V.R., Patterson L.J., Venzon D., Liewehr D., Aldrich K., Florese R., et al. Vaccine-elicited antibodies mediate antibody-dependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J Immunol 174 4 (2005) 2185-2189
7. Greenier J.L., Van Rompay K.K., Montefiori D., Earl P., Moss B., and Marthas M.L. Simian immunodeficiency virus (SIV) envelope quasispecies transmission and evolution in infant rhesus macaques after oral challenge with uncloned SIVmac251: increased diversity is associated with neutralizing antibodies and improved survival in previously immunized animals. Virol J 2 1 (2005) 11
8. Johnson R.P. HIV pathogenesis and vaccine development. Top HIV Med 13 1 (2005) 9-15
9. Mooij P., Nieuwenhuis I.G., Knoop C.J., Doms R.W., Bogers W.M., Ten Haaft P.J., et al. Qualitative T-helper responses to multiple viral antigens correlate with vaccine-induced immunity to simian/human immunodeficiency virus infection. J Virol 78 7 (2004) 3333-3342
10. Morris C.B., Cheng E., Thanawastien A., Cardenas-Freytag L., and Clements J.D. Effectiveness of intranasal immunization with HIV-gp160 and an HIV-1 env CTL epitope peptide (E7) in combination with the mucosal adjuvant LT(R192G). Vaccine 18 18 (2000) 1944-1951
11. Nacsa J., Edghill-Smith Y., Tsai W.P., Venzon D., Tryniszewska E., Hryniewicz A., et al. Contrasting effects of low-dose IL-2 on vaccine-boosted simian immunodeficiency virus (SIV)-specific CD4+ and CD8+ T cells in macaques chronically infected with SIVmac251. J Immunol 174 4 (2005) 1913-1921
12. Parren P.W., Marx P.A., Hessell A.J., Luckay A., Harouse J., Cheng-Mayer C., et al. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J Virol 75 17 (2001) 8340-8347
13. Quinnan Jr. G.V., Yu X.F., Lewis M.G., Zhang P.F., Sutter G., Silvera P., et al. Protection of rhesus monkeys against infection with minimally pathogenic simian-human immunodeficiency virus: correlations with neutralizing antibodies and cytotoxic T cells. J Virol 79 6 (2005) 3358-3369
14. Schmitz J.E., Johnson R.P., McClure H.M., Manson K.H., Wyand M.S., Kuroda M.J., et al. Effect of CD8+ lymphocyte depletion on virus containment after simian immunodeficiency virus SIVmac251 challenge of live attenuated SIVmac239delta3-vaccinated rhesus macaques. J Virol 79 13 (2005) 8131-8141
15. Seaman M.S., Santra S., Newberg M.H., Philippon V., Manson K., Xu L., et al. Vaccine-elicited memory cytotoxic T lymphocytes contribute to Mamu-A*01-associated control of simian/human immunodeficiency virus 89.6P replication in rhesus monkeys. J Virol 79 8 (2005) 4580-4588
16. Ho D.D., Neumann A.U., Perelson A.S., Chen W., Leonard J.M., and Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373 6510 (1995) 123-126
17. Lifson J.D., and Martin M.A. One step forwards, one step back. Nature 415 6869 (2002) 272-273
18. Louwagie J., Janssens W., Mascola J., Heyndrickx L., Hegerich P., van der Groen G., et al. Genetic diversity of the envelope glycoprotein from human immunodeficiency virus type 1 isolates of African origin. J Virol 69 1 (1995) 263-271
19. Zolla-Pazner S. Identifying epitopes of HIV-1 that induce protective antibodies. Nat Rev Immunol 4 3 (2004) 199-210
20. Berzofsky J.A. Design of engineered vaccines for systemic and mucosal immunity to HIV. Pathol Biol (Paris) 49 6 (2001) 466-467
21. Sarkar S., Kalia V., Murphey-Corb M., and Montelaro R.C. Detailed analysis of CD4+ Th responses to envelope and Gag proteins of simian immunodeficiency virus reveals an exclusion of broadly reactive Th epitopes from the glycosylated regions of envelope. J Immunol 168 8 (2002) 4001-4011
22. Morris C.B., Thanawastien A., Sullivan D.E., and Clements J.D. Identification of a peptide capable of inducing an HIV-1 Tat-specific CTL response. Vaccine 20 1-2 (2002) 12-15
23. Veazey R.S., DeMaria M., Chalifoux L.V., Shvetz D.E., Pauley D.R., Knight H.L., et al. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280 5362 (1998) 427-431
24. Veazey R.S., Marx P.A., and Lackner A.A. The mucosal immune system: primary target for HIV infection and AIDS. Trends Immunol 22 11 (2001) 626-633
25. Yasutomi Y., Palker T.J., Gardner M.B., Haynes B.F., and Letvin N.L. Synthetic peptide in mineral oil adjuvant elicits simian immunodeficiency virus-specific CD8 cytotoxic T lymphocytes in Rhesus monkeys. J Immunol 151 (1993) 5096-5105
26. Feinberg M.B., and Moore J.P. AIDS vaccine models: challenging challenge viruses. Nat Med 8 3 (2002) 207-210
27. Harouse J.M., Gettie A., Tan R.C., Blanchard J., and Cheng-Mayer C. Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs. Science 284 5415 (1999) 816-819
28. Lycke N. From toxin to adjuvant: the rational design of a vaccine adjuvant vector, CTA1-DD/ISCOM. Cell Microbiol 6 1 (2004) 23-32
29. Morein B., Villacres Eriksson M., Akerblom L., Ronnberg B., Lovgren K., and Sjolander A. Mechanisms behind the immune response induced by immunostimulating complexes. AIDS Res Hum Retroviruses 10 Suppl 2 (1994) S109-S114
30. Andersson C., Wikman M., Lovgren-Bengtsson K., Lunden A., and Stahl S. In vivo and in vitro lipidation of recombinant immunogens for direct iscom incorporation. J Immunol Methods 255 1-2 (2001) 135-148
31. Blomqvist G.A., Lovgren-Bengtsson K., and Morein B. Influence of maternal immunity on antibody and T-cell response in mice. Vaccine 21 17-18 (2003) 2022-2031
32. Harouse J., Tan R.C., Gettie A., Dailey P., Marx P.A., Luciw P.A., et al. In vitro infection of primate PBMC with simian/human immunodeficiency virus, SHIV(SF33A): correlation to in vivo outcome. J Med Primatol 27 2-3 (1998) 81-86
33. Joag S.V., Li Z., Foresman L., Stephens E.B., Zhao L.J., Adany I., et al. Chimeric simian/human immunodeficiency virus that causes progressive loss of CD4+ T cells and AIDS in pig-tailed macaques. J Virol 70 5 (1996) 3189-3197
34. Sestak K., McNeal M.M., Choi A., Cole M.J., Ramesh G., Alvarez X., et al. Defining T-cell-mediated immune responses in rotavirus-infected juvenile rhesus macaques. J Virol 78 19 (2004) 10258-10264
35. Kuroda M.J., Schmitz J.E., Barouch D.H., Craiu A., Allen T.M., Sette A., et al. Analysis of Gag-specific cytotoxic T lymphocytes in simian immunodeficiency virus-infected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J Exp Med 9 187 (1998) 1373-1381
36. Montefiori D. Evaluating neutralizing antibodies against HIV, SIV and SHIV in luciferase reporter gene assays. In: Coligan J., Kruisbeek A., Margulies D., Shevach E., Strober W., and Coico R. (Eds). Current protocols in immunology (2004), John Wiley & Sons, New York, NY pp. 12.11.1-12.11.15
37. Bures R., Gaitan A., Zhu T., Graziosi C., McGrath K.M., Tartaglia J., et al. Immunization with recombinant canarypox vectors expressing membrane-anchored glycoprotein 120 followed by glycoprotein 160 boosting fails to generate antibodies that neutralize R5 primary isolates of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 16 18 (2000) 2019-2035
38. Li M., Gao F., Mascola J., Stamatatos L., Polonis V.R., Koutsoukos M., et al. Human immunodeficiency virus type 1 env clones from acute and early Subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J Virol 79 16 (2005) 10108-10125
39. Veazey R.S., Klasse P.J., Ketas T.J., Reeves J.D., Piatak Jr. M., Kunstman K., et al. Use of a small molecule CCR5 inhibitor in macaques to treat simian immunodeficiency virus infection or prevent simian-human immunodeficiency virus infection. J Exp Med 198 10 (2003) 1551-1562
40. Pahar B., Li J., Rourke T., Miller C.J., and McChesney M.B. Detection of antigen-specific T cell interferon gamma expression by ELISPOT and cytokine flow cytometry assays in rhesus macaques. J Immunol Meth 282 1-2 (2003) 103-115
41. Pitcher C.J., Hagen S.I., Walker J.M., Lum R., Mitchell B.L., Maino V.C., et al. Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168 1 (2002) 29-43
42. Cline A.N., Bess J.W., Piatak Jr. M., and Lifson J.D. Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J Med Primatol 34 5-6 (2005) 303-312
43. Suryanarayana K., Wiltrout T.A., Vasquez G.M., Hirsch V.M., and Lifson J.D. Plasma SIV RNA viral load determination by real-time quantification of product generation in reverse transcriptase-polymerase chain reaction. AIDS Res Hum Retroviruses 14 2 (1998) 183-189
44. Robbins J.B., Schneerson R., and Szu S.C. Perspective: hypothesis: serum IgG antibody is sufficient to confer protection against infectious diseases by inactivating the inoculum. J Infect Dis 171 (1995) 1387-1396
45. Johnson R.P., and Kaur A. HIV: viral blitzkrieg. Nature 434 (2005) 1080-1081
46. Veazey R.S., and Lackner A.A. HIV swiftly guts the immune system. Nat Med 11 5 (2005) 469-470
47. Amara R.R., Villinger F., Altman J.D., Lydy S.L., O'Neil S.P., Staprans S.I., et al. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292 (2001) 69-74
48. Ambrose Z., Larsen K., Thompson J., Stevens Y., Finn E., Hu S.L., et al. Evidence for early local viral replication and local production of antiviral immunity upon mucosal simian-human immunodeficiency virus SHIV (89.6) infection in Macaca nemestrina. J Virol 75 (2001) 8589-8596
49. Girard M., Habel A., and Chanel C. New prospects for the development of a vaccine against human immunodeficiency virus type 1. C R Acad Sci III 322 (1999) 989-1066
50. Hiroi T., Goto H., Someya K., Yanagita M., Honda M., Yamanaka N., et al. HIV mucosal vaccine: nasal immunization with RBCG-V3J1 induces a long term V3J1 peptide-specific neutralizing immunity in Th1- and Th2-deficient conditions. Immunology 167 (2001) 5862-5867
51. Kato H., Bukawa H., Hagiwara E., Xin K.Q., Hamajima K., Kawamoto S., et al. Rectal and vaginal immunization with a macromolecular multicomponent peptide vaccine candidate for HIV-1 infection induces HIV-specific protective immune responses. Vaccine 18 (2000) 1151-1160
52. Lehner T., Bergmeier L., Wang Y., Tao L., and Mitchell E. A rational basis for mucosal vaccination against HIV infection. Immunol Rev 170 (1999) 197-222
53. Goulder P.J., and Watkins D.I. HIV and SIV CTL escape: implications for vaccine design. Nat Rev Immunol 4 8 (2004) 630-640
54. Letvin N.L. Progress in the development of an HIV-1 vaccine. Science 280 (1998) 1875-1880
55. Walker B.D., and Korber B.T. Immune control of HIV: the obstacles of HLA and viral diversity. Nat Immunol 2 (2001) 473-475
56. Donahoe S.M., Moretto W.J., Samuel R.V., Metzner K.J., Marx P.A., Hanke T., et al. Direct measurement of CD8+ T cell responses in macaques infected with simian immunodeficiency virus. Virol 272 (2000) 347-356
57. Berzofsky J.A., Ahlers J.D., Derby M.A., Pendleton C.D., Arichi T., and Belyakov I.M. Approaches to improve engineered vaccines for human immunodeficiency virus (HIV) and other viruses that cause chronic infections. Immunol Rev 170 (1999) 151-172
58. Takahashi M., Nakagawa Y., Berzofsky J.A., and Takahashi H. Counter-regulation of cytolytic activity and cytokine production in HIV-1-specific murine CD8+ cytotoxic T lymphocytes by free antigenic peptide. Int Immunol 13 (2001) 43-51
59. Letvin N.L., Huang Y., Chakrabarti B.K., Xu L., Seaman M.S., Beaudry K., et al. Heterologous envelope immunogens contribute to AIDS vaccine protection in rhesus monkeys. J Virol 78 14 (2004) 7490-7497
60. Zhan X., Martin L.N., Slobod K.S., Coleclough C., Lockey T.D., Brown S.A., et al. Multi-envelope HIV-1 vaccine devoid of SIV components controls disease in macaques challenged with heterologous pathogenic SHIV. Vaccine 23 46-47 (2005) 5306-5320
61. Seaman M.S., Xu L., Beaudry K., Martin K.L., Beddall M.H., Miura A., et al. Multiclade human immunodeficiency virus type 1 envelope immunogens elicit broad cellular and humoral immunity in rhesus monkeys. J Virol 79 5 (2005) 2956-2963
62. Vogel T.U., Beer B.E., zur Megede J., Ihlenfeldt H.G., Jung G., Holzammer S., et al. Induction of anti-simian immunodeficiency virus cellular and humoral immune responses in rhesus macaques by peptide immunogens: correlation of CTL activity and reduction of cell-associated but not plasma virus load following challenge. J Gen Virol 83 Pt 1 (2002) 81-91
63. Yasutomi Y., Koenig S., Woods R.M., Madsen J., Wassef N.M., Alving C.R., et al. A vaccine-elicited, single viral epitope-specific cytotoxic T lymphocyte response does not protect against intravenous, cell-free simian immunodeficiency virus challenge. J Virol 69 4 (1995) 2279-2284
64. Kaur A., Hale C.L., Ramanujan S., Jain R.K., and Johnson R.P. Differential dynamics of CD4(+) and CD8(+) T-lymphocyte proliferation and activation in acute simian immunodeficiency virus infection. J Virol 74 18 (2000) 8413-8424
65. Monceaux V., Ho Tsong Fang R., Cumont M.C., Hurtrel B., and Estaquier J. Distinct cycling CD4(+)- and CD8(+)-T-cell profiles during the asymptomatic phase of simian immunodeficiency virus SIVmac251 infection in rhesus macaques. J Virol 77 18 (2003) 10047-10059
66. Newberg M.H., McEvers K.J., Gorgone D.A., Lifton M.A., Baumeister S.H., Veazey R.S., et al. Immunodomination in the evolution of dominant epitope-specific CD8+ T lymphocyte responses in simian immunodeficiency virus-infected rhesus monkeys. J Immunol 176 1 (2006) 319-328
67. Peters B., Bui H.H., Sidney J., Weng Z., Loffredo J.T., Watkins D.I., et al. A computational resource for the prediction of peptide binding to Indian rhesus macaque MHC class I molecules. Vaccine 23 45 (2005) 5212-5224