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Science 6 April 2001:
Vol. 292. no. 5514, pp. 69 - 74
DOI:

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Research Articles

Control of a Mucosal Challenge and Prevention of AIDS by a Multiprotein DNA/MVA Vaccine

Rama Rao Amara,13 Francois Villinger,2 John D. Altman,3 Shari L. Lydy,13 Shawn P. O'Neil,13 Silvija I. Staprans,6 David C. Montefiori,4 Yan Xu,1 James G. Herndon,1 Linda S. Wyatt,5 Maria Angelito Candido,1* Natalia L. Kozyr,6 Patricia L. Earl,5 James M. Smith,13 Hak-Ling Ma,17dagger Bennett D. Grimm,2 Michael L. Hulsey,3 Joseph Miller,3 Harold M. McClure,1 Janet M. McNicholl,7 Bernard Moss,5 Harriet L. Robinson13ddagger

Heterologous prime/boost regimens have the potential for raising high levels of immune responses. Here we report that DNA priming followed by a recombinant modified vaccinia Ankara (rMVA) booster controlled a highly pathogenic immunodeficiency virus challenge in a rhesus macaque model. Both the DNA and rMVA components of the vaccine expressed multiple immunodeficiency virus proteins. Two DNA inoculations at 0 and 8 weeks and a single rMVA booster at 24 weeks effectively controlled an intrarectal challenge administered 7 months after the booster. These findings provide hope that a relatively simple multiprotein DNA/MVA vaccine can help to control the acquired immune deficiency syndrome epidemic.

1 Vaccine Research Center and Yerkes Regional Primate Research Center, Emory University, Atlanta, GA 30329, USA.
2 Vaccine Research Center and Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Atlanta, GA 30322, USA.
3 Vaccine Research Center and Department of Microbiology and Immunology of Emory University School of Medicine, Atlanta, GA 30322, USA.
4 Department of Surgery, Duke University Medical Center, Durham, NC 27710, USA.
5 Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
6 Vaccine Research Center and Department of Medicine, Division of Infectious Diseases of Emory University School of Medicine, Atlanta, GA 30322, USA.
7 Division of AIDS, STD and TB Laboratory Research, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30330, USA.
*   Present address: Department of Microbiology, University of Toronto, Toronto, Ontario, Canada M5G 1X5.

dagger    Present address: MIT Center for Cancer Research, Cambridge, MA 02139, USA.

ddagger    To whom correspondence should be addressed. E-mail: hrobins{at}rmy.emory.edu

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Vaccination of Rhesus Macaques with Recombinant Mycobacterium bovis Bacillus Calmette-Guerin Env V3 Elicits Neutralizing Antibody-Mediated Protection against Simian-Human Immunodeficiency Virus with a Homologous but Not a Heterologous V3 Motif.
K. Someya, D. Cecilia, Y. Ami, T. Nakasone, K. Matsuo, S. Burda, H. Yamamoto, N. Yoshino, M. Kaizu, S. Ando, et al. (2005)
J. Virol. 79, 1452-1462
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Analysis of Pigtail Macaque Major Histocompatibility Complex Class I Molecules Presenting Immunodominant Simian Immunodeficiency Virus Epitopes.
M. Z. Smith, C. J. Dale, R. De Rose, I. Stratov, C. S. Fernandez, A. G. Brooks, J. Weinfurter, K. Krebs, C. Riek, D. I. Watkins, et al. (2005)
J. Virol. 79, 684-695
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Neutralizing Antibodies Elicited by Immunization of Monkeys with DNA Plasmids and Recombinant Adenoviral Vectors Expressing Human Immunodeficiency Virus Type 1 Proteins.
J. R. Mascola, A. Sambor, K. Beaudry, S. Santra, B. Welcher, M. K. Louder, T. C. VanCott, Y. Huang, B. K. Chakrabarti, W.-P. Kong, et al. (2005)
J. Virol. 79, 771-779
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Novel Adeno-Associated Virus Vector Vaccine Restricts Replication of Simian Immunodeficiency Virus in Macaques.
P. R. Johnson, B. C. Schnepp, M. J. Connell, D. Rohne, S. Robinson, G. R. Krivulka, C. I. Lord, R. Zinn, D. C. Montefiori, N. L. Letvin, et al. (2005)
J. Virol. 79, 955-965
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CD8+ T-Cell-Mediated Cross-Clade Protection in the Genital Tract following Intranasal Immunization with Inactivated Human Immunodeficiency Virus Antigen Plus CpG Oligodeoxynucleotides.
J. Q. Jiang, A. Patrick, R. B. Moss, and K. L. Rosenthal (2005)
J. Virol. 79, 393-400
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Immunogenicity Study of Glycoprotein-Deficient Rabies Virus Expressing Simian/Human Immunodeficiency Virus SHIV89.6P Envelope in a Rhesus Macaque.
P. M. McKenna, P. P. Aye, B. Dietzschold, D. C. Montefiori, L. N. Martin, P. A. Marx, R. J. Pomerantz, A. Lackner, and M. J. Schnell (2004)
J. Virol. 78, 13455-13459
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Efficacy of DNA and Fowlpox Virus Priming/Boosting Vaccines for Simian/Human Immunodeficiency Virus.
C. J. Dale, R. De Rose, I. Stratov, S. Chea, D. C. Montefiori, S. Thomson, I. A. Ramshaw, B. E. H. Coupar, D. B. Boyle, M. Law, et al. (2004)
J. Virol. 78, 13819-13828
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A Novel Adjuvant for Mucosal Immunity to HIV-1 gp120 in Nonhuman Primates.
N. Yoshino, F. X.-S. Lu, K. Fujihashi, Y. Hagiwara, K. Kataoka, D. Lu, L. Hirst, M. Honda, F. W. van Ginkel, Y. Takeda, et al. (2004)
J. Immunol. 173, 6850-6857
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Gene Expression Profiling of Host Response in Models of Acute HIV Infection.
S. E. Bosinger, K. A. Hosiawa, M. J. Cameron, D. Persad, L. Ran, L. Xu, M. R. Boulassel, M. Parenteau, J. Fournier, E. W. Rud, et al. (2004)
J. Immunol. 173, 6858-6863
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Intranasal HIV-1-gp160-DNA/gp41 Peptide Prime-Boost Immunization Regimen in Mice Results in Long-Term HIV-1 Neutralizing Humoral Mucosal and Systemic Immunity.
C. Devito, B. Zuber, U. Schroder, R. Benthin, K. Okuda, K. Broliden, B. Wahren, and J. Hinkula (2004)
J. Immunol. 173, 7078-7089
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Combined Vaccine Regimen Based on Parenteral Priming with a DNA Vaccine and Administration of an Oral Booster Consisting of a Recombinant Salmonella enterica Serovar Typhimurium Vaccine Strain for Immunization against Infection with Human-Derived Enterotoxigenic Escherichia coli Strains.
M. O. Lasaro, W. B. Luiz, M. E. Sbrogio-Almeida, L. S. Nishimura, B. E. C. Guth, and L. C. S. Ferreira (2004)
Infect. Immun. 72, 6480-6491
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Predicting the Impact of a Nonsterilizing Vaccine against Human Immunodeficiency Virus.
M. P. Davenport, R. M. Ribeiro, D. L. Chao, and A. S. Perelson (2004)
J. Virol. 78, 11340-11351
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Modulation by Morphine of Viral Set Point in Rhesus Macaques Infected with Simian Immunodeficiency Virus and Simian-Human Immunodeficiency Virus.
R. Kumar, C. Torres, Y. Yamamura, I. Rodriguez, M. Martinez, S. Staprans, R. M. Donahoe, E. Kraiselburd, E. B. Stephens, and A. Kumar (2004)
J. Virol. 78, 11425-11428
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Vaccine protection from CD4+ T-cell loss caused by simian immunodeficiency virus (SIV) mac251 is afforded by sequential immunization with three unrelated vaccine vectors encoding multiple SIV antigens.
G. Koopman, D. Mortier, S. Hofman, H. Niphuis, Z. Fagrouch, S. Norley, G. Sutter, P. Liljestrom, and J. L. Heeney (2004)
J. Gen. Virol. 85, 2915-2924
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Repertoire and Immunofocusing of CD8 T Cell Responses Generated by HIV-1 gag-pol and Expression Library Immunization Vaccines.
R. A. K. Singh and M. A. Barry (2004)
J. Immunol. 173, 4387-4393
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Novel and Promiscuous CTL Epitopes in Conserved Regions of Gag Targeted by Individuals with Early Subtype C HIV Type 1 Infection from Southern Africa.
A. M. Masemola, T. N. Mashishi, G. Khoury, H. Bredell, M. Paximadis, T. Mathebula, D. Barkhan, A. Puren, E. Vardas, M. Colvin, et al. (2004)
J. Immunol. 173, 4607-4617
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A Consecutive Priming-Boosting Vaccination of Mice with Simian Immunodeficiency Virus (SIV) gag/pol DNA and Recombinant Vaccinia Virus Strain DIs Elicits Effective Anti-SIV Immunity.
K. Someya, K.-Q. Xin, K. Matsuo, K. Okuda, N. Yamamoto, and M. Honda (2004)
J. Virol. 78, 9842-9853
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Kinetics of Virus-Specific CD8+ T Cells and the Control of Human Immunodeficiency Virus Infection.
M. P. Davenport, R. M. Ribeiro, and A. S. Perelson (2004)
J. Virol. 78, 10096-10103
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Adjuvant Activities of Novel Cytokines, Interleukin-23 (IL-23) and IL-27, for Induction of Hepatitis C Virus-Specific Cytotoxic T Lymphocytes in HLA-A*0201 Transgenic Mice.
M. Matsui, O. Moriya, M. L. Belladonna, S. Kamiya, F. A. Lemonnier, T. Yoshimoto, and T. Akatsuka (2004)
J. Virol. 78, 9093-9104
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Codon Optimization of the Tat Antigen of Human Immunodeficiency Virus Type 1 Generates Strong Immune Responses in Mice following Genetic Immunization.
L. Ramakrishna, K. K. Anand, K. M. Mohankumar, and U. Ranga (2004)
J. Virol. 78, 9174-9189
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Induction of Cellular Immune Responses to Simian Immunodeficiency Virus Gag by Two Recombinant Negative-Strand RNA Virus Vectors.
Y. Nakaya, T. Nakaya, M.-S. Park, J. Cros, J. Imanishi, P. Palese, and A. Garcia-Sastre (2004)
J. Virol. 78, 9366-9375
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Enhanced SIV replication and accelerated progression to AIDS in macaques primed to mount a CD4 T cell response to the SIV envelope protein.
S. I. Staprans, A. P. Barry, G. Silvestri, J. T. Safrit, N. Kozyr, B. Sumpter, H. Nguyen, H. McClure, D. Montefiori, J. I. Cohen, et al. (2004)
PNAS 101, 13026-13031
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Highly pathogenic SHIVs and SIVs target different CD4+ T cell subsets in rhesus monkeys, explaining their divergent clinical courses.
Y. Nishimura, T. Igarashi, O. K. Donau, A. Buckler-White, C. Buckler, B. A. P. Lafont, R. M. Goeken, S. Goldstein, V. M. Hirsch, and M. A. Martin (2004)
PNAS 101, 12324-12329
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Enhanced cellular immunity and systemic control of SHIV infection by combined parenteral and mucosal administration of a DNA prime MVA boost vaccine regimen.
B. Makitalo, P. Lundholm, J. Hinkula, C. Nilsson, K. Karlen, A. Morner, G. Sutter, V. Erfle, J. L. Heeney, B. Wahren, et al. (2004)
J. Gen. Virol. 85, 2407-2419
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Attenuated poxviruses generate clinically relevant frequencies of CMV-specific T cells.
Z. Wang, C. La Rosa, S. Mekhoubad, S. F. Lacey, M. C. Villacres, S. Markel, J. Longmate, J. D. I. Ellenhorn, R. F. Siliciano, C. Buck, et al. (2004)
Blood 104, 847-856
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Recombinant poxvirus boosting of DNA-primed rhesus monkeys augments peak but not memory T lymphocyte responses.
S. Santra, D. H. Barouch, B. Korioth-Schmitz, C. I. Lord, G. R. Krivulka, F. Yu, M. H. Beddall, D. A. Gorgone, M. A. Lifton, A. Miura, et al. (2004)
PNAS 101, 11088-11093
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Human Immunodeficiency Virus Type 1-Specific Immune Responses in Primates upon Sequential Immunization with Adenoviral Vaccine Carriers of Human and Simian Serotypes.
A. Reyes-Sandoval, J. C. Fitzgerald, R. Grant, S. Roy, Z. Q. Xiang, Y. Li, G. P. Gao, J. M. Wilson, and H. C. J. Ertl (2004)
J. Virol. 78, 7392-7399
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Heterologous Envelope Immunogens Contribute to AIDS Vaccine Protection in Rhesus Monkeys.
N. L. Letvin, Y. Huang, B. K. Chakrabarti, L. Xu, M. S. Seaman, K. Beaudry, B. Korioth-Schmitz, F. Yu, D. Rohne, K. L. Martin, et al. (2004)
J. Virol. 78, 7490-7497
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Loss of virus-specific CD4+ T cells with increases in viral loads in the chronic phase after vaccine-based partial control of primary simian immunodeficiency virus replication in macaques.
W.-H. Lun, A. Takeda, H. Nakamura, M. Kano, K. Mori, T. Sata, Y. Nagai, and T. Matano (2004)
J. Gen. Virol. 85, 1955-1963
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Induction of Disease by a Molecularly Cloned Highly Pathogenic Simian Immunodeficiency Virus/Human Immunodeficiency Virus Chimera Is Multigenic.
R. Sadjadpour, T. S. Theodore, T. Igarashi, O. K. Donau, R. J. Plishka, A. Buckler-White, and M. A. Martin (2004)
J. Virol. 78, 5513-5519
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Induction of HIV Immunity in the Genital Tract After Intranasal Delivery of a MVA Vector: Enhanced Immunogenicity After DNA Prime-Modified Vaccinia Virus Ankara Boost Immunization Schedule.
M. M. Gherardi, E. Perez-Jimenez, J. L. Najera, and M. Esteban (2004)
J. Immunol. 172, 6209-6220
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Roles of Target Cells and Virus-Specific Cellular Immunity in Primary Simian Immunodeficiency Virus Infection.
R. R. Regoes, R. Antia, D. A. Garber, G. Silvestri, M. B. Feinberg, and S. I. Staprans (2004)
J. Virol. 78, 4866-4875
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Protective efficacy of a multicomponent vector vaccine in cynomolgus monkeys after intrarectal simian immunodeficiency virus challenge.
D. R. M. Negri, S. Baroncelli, S. Catone, A. Comini, Z. Michelini, M. T. Maggiorella, L. Sernicola, F. Crostarosa, R. Belli, M. G. Mancini, et al. (2004)
J. Gen. Virol. 85, 1191-1201
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Induction in Humans of CD8+ and CD4+ T Cell and Antibody Responses by Sequential Immunization with Malaria DNA and Recombinant Protein.
R. Wang, J. Epstein, Y. Charoenvit, F. M. Baraceros, N. Rahardjo, T. Gay, J.-G. Banania, R. Chattopadhyay, P. de la Vega, T. L. Richie, et al. (2004)
J. Immunol. 172, 5561-5569
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Long-Lived Poxvirus Immunity, Robust CD4 Help, and Better Persistence of CD4 than CD8 T Cells.
R. R. Amara, P. Nigam, S. Sharma, J. Liu, and V. Bostik (2004)
J. Virol. 78, 3811-3816
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Highly Effective Control of an AIDS Virus Challenge in Macaques by Using Vesicular Stomatitis Virus and Modified Vaccinia Virus Ankara Vaccine Vectors in a Single-Boost Protocol.
E. Ramsburg, N. F. Rose, P. A. Marx, M. Mefford, D. F. Nixon, W. J. Moretto, D. Montefiori, P. Earl, B. Moss, and J. K. Rose (2004)
J. Virol. 78, 3930-3940
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Recombinant Modified Vaccinia Virus Ankara Expressing a Soluble Form of Glycoprotein B Causes Durable Immunity and Neutralizing Antibodies against Multiple Strains of Human Cytomegalovirus.
Z. Wang, C. La Rosa, R. Maas, H. Ly, J. Brewer, S. Mekhoubad, P. Daftarian, J. Longmate, W. J. Britt, and D. J. Diamond (2004)
J. Virol. 78, 3965-3976
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Unexpectedly, induction of cytotoxic T lymphocytes enhances the humoral response after DNA immunization.
C. M. Dyer, Y. Zhan, J. L. Brady, F. R. Carbone, M. J. Smyth, and A. M. Lew (2004)
Blood 103, 3073-3075
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DNA Vaccines against Human Immunodeficiency Virus Type 1 in the Past Decade.
M. Giri, K. E. Ugen, and D. B. Weiner (2004)
Clin. Microbiol. Rev. 17, 370-389
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Hierarchical Targeting of Subtype C Human Immunodeficiency Virus Type 1 Proteins by CD8+ T Cells: Correlation with Viral Load.
A. Masemola, T. Mashishi, G. Khoury, P. Mohube, P. Mokgotho, E. Vardas, M. Colvin, L. Zijenah, D. Katzenstein, R. Musonda, et al. (2004)
J. Virol. 78, 3233-3243
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Qualitative T-Helper Responses to Multiple Viral Antigens Correlate with Vaccine-Induced Immunity to Simian/Human Immunodeficiency Virus Infection.
P. Mooij, I. G. Nieuwenhuis, C. J. Knoop, R. W. Doms, W. M. J. M. Bogers, P. J. F. ten Haaft, H. Niphuis, W. Koornstra, K. Bieler, J. Kostler, et al. (2004)
J. Virol. 78, 3333-3342
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