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Journal of Virology, January 2002, p. 292-302, Vol. 76, No. 1
0022-538X/01/$04.00+0     DOI: 10.1128/JVI.76.1.292-302.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

ALVAC-SIV-gag-pol-env-Based Vaccination and Macaque Major Histocompatibility Complex Class I (A*01) Delay Simian Immunodeficiency Virus SIVmac-Induced Immunodeficiency

R. Pal,1 D. Venzon,2 N. L. Letvin,3 S. Santra,3 D. C. Montefiori,4 N. R. Miller,5 E. Tryniszewska,6,7 M. G. Lewis,8 T. C. VanCott,9 V. Hirsch,10 R. Woodward,1 A. Gibson,1 M. Grace,1 E. Dobratz,1 P. D. Markham,1 Z. Hel,6 J. Nacsa,6 M. Klein,11 J. Tartaglia,12 and G. Franchini6*

Advanced BioScience Laboratories, Inc., Kensington, Maryland 20895,1 Biostatistics and Data Management Section,2 Beth Israel Deaconess Medical Center, Boston, Massachusetts 02215,3 Department of Surgery, Center for AIDS Research, Duke University Medical Center, Durham, North Carolina 27710,4 National Cancer Institute, and National Institute of Allergy and Infectious Diseases Bethesda, Maryland 20892,5 Basic Research Laboratory,6 3rd Department of Pediatrics, Medical Academy of Bialystok, Bialystok, Poland,7 Southern Research Institute, Frederick, Maryland 21701,8 Walter Reed Army Institute of Research and Henry M. Jackson Foundation,9 National Institute of Allergy and Infectious Diseases, Rockville, Maryland 20852,10 Aventis-Pasteur, Ltd., Marcy l’Etoile, France 69280,11 Aventis-Pasteur, Ltd., Toronto, Ontario M2R 3T4, Canada,12

Received 29 May 2001/ Accepted 3 October 2001

T-cell-mediated immune effector mechanisms play an important role in the containment of human immunodeficiency virus/simian immunodeficiency virus (HIV/SIV) replication after infection. Both vaccination- and infection-induced T-cell responses are dependent on the host major histocompatibility complex classes I and II (MHC-I and MHC-II) antigens. Here we report that both inherent, host-dependent immune responses to SIVmac251 infection and vaccination-induced immune responses to viral antigens were able to reduce virus replication and/or CD4+ T-cell loss. Both the presence of the MHC-I Mamu-A*01 genotype and vaccination of rhesus macaques with ALVAC-SIV-gag-pol-env (ALVAC-SIV-gpe) contributed to the restriction of SIVmac251 replication during primary infection, preservation of CD4+ T cells, and delayed disease progression following intrarectal challenge exposure of the animals to SIVmac251 (561). ALVAC-SIV-gpe immunization induced cytotoxic T-lymphocyte (CTL) responses cumulatively in 67% of the immunized animals. Following viral challenge, a significant secondary virus-specific CD8+ T-cell response was observed in the vaccinated macaques. In the same immunized macaques, a decrease in virus load during primary infection (P = 0.0078) and protection from CD4 loss during both acute and chronic phases of infection (P = 0.0099 and P = 0.03, respectively) were observed. A trend for enhanced survival of the vaccinated macaques was also observed. Neither boosting the ALVAC-SIV-gpe with gp120 immunizations nor administering the vaccine by the combination of mucosal and systemic immunization routes increased significantly the protective effect of the ALVAC-SIV-gpe vaccine. While assessing the role of MHC-I Mamu-A*01 alone in the restriction of viremia following challenge of nonvaccinated animals with other SIV isolates, we observed that the virus load was not significantly lower in Mamu-A*01-positive macaques following intravenous challenge with either SIVmac251 (561) or SIVSME660. However, a significant delay in CD4+ T-cell loss was observed in Mamu-A*01-positive macaques in each group. Of interest, in the case of intravenous or intrarectal challenge with the chimeric SIV/HIV strains SHIV89.6P or SHIVKU2, respectively, MHC-I Mamu-A*01-positive macaques did not significantly restrict primary viremia. The finding of the protective effect of the Mamu-A*01 molecule parallels the protective effect of the B*5701 HLA allele in HIV-1-infected humans and needs to be accounted for in the evaluation of vaccine efficacy against SIV challenge models.

* Corresponding author. Mailing address: National Cancer Institute, Basic Research Laboratory, 41/D804. Bethesda, MD 20892. Phone: (301) 496-2386. Fax: (301) 402-0055. E-mail: franchig{at}mail.nih.gov.

Journal of Virology, January 2002, p. 292-302, Vol. 76, No. 1
0022-538X/01/$04.00+0     DOI: 10.1128/JVI.76.1.292-302.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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