This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Cole, K. S.
Right arrow Articles by Montelaro, R. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Cole, K. S.
Right arrow Articles by Montelaro, R. C.

 Previous Article  |  Next Article 

J. Virol., 07 1997, 5069-5079, Vol 71, No. 7
Copyright © 1997, American Society for Microbiology

Evolution of envelope-specific antibody responses in monkeys experimentally infected or immunized with simian immunodeficiency virus and its association with the development of protective immunity

KS Cole, JL Rowles, BA Jagerski, M Murphey-Corb, T Unangst, JE Clements, J Robinson, MS Wyand, RC Desrosiers and RC Montelaro
Department of Molecular Genetics and Biochemistry, University of Pittsburgh School of Medicine, Pennsylvania 15261, USA.

Previous studies of attenuated simian immunodeficiency virus (SIV) vaccines in rhesus macaques have demonstrated the development of broad protection against experimental challenge, indicating the potential for the production of highly effective immune responses to SIV antigens. However, the development of this protective immune status was found to be critically dependent on the length of time postvaccination with the attenuated virus strain, suggesting a necessary maturation of immune responses. In this study, the evolution of SIV envelope-specific antibodies in monkeys experimentally infected with various attenuated strains of SIV was characterized by using a comprehensive panel of serological assays to assess the progression of antibodies in longitudinal serum samples that indicate the development of protective immunity. In parallel studies, we also used the same panel of antibody assays to characterize the properties of SIV envelope-specific antibodies elicited by inactivated whole-virus and envelope subunit vaccines previously reported to be ineffective in producing protective immunity. The results of these studies demonstrate that the evolution of protective immunity in monkeys inoculated with attenuated strains of SIV is associated with a complex and lengthy maturation of antibody responses over the first 6 to 8 months postinoculation, as reflected in progressive changes in antibody conformational dependence and avidity properties. The establishment of long-term protective immunity at this time in general parallels the absence of further detectable changes in antibody responses and a maintenance of relatively constant antibody titer, avidity, conformational dependence, and the presence of neutralizing antibody for at least 2 years postinoculation. In contrast to the mature antibody responses elicited by the attenuated SIV vaccines, the whole-virus and envelope subunit vaccines in general elicited only immature antibody responses characterized by poor reactivity with native envelope proteins, low avidity, low conformational dependence, and the absence of neutralization activity against the challenge strain. Thus, these studies establish for the first time an association between the effectiveness of experimental vaccines and the capacity of the vaccine to produce a mature antibody response to SIV envelope proteins and further indicate that a combination of several antibody parameters (including titer, avidity, conformational dependence, and virus neutralization) are superior to any single antibody parameter as prognostic indicators to evaluate candidate AIDS vaccines.


This article has been cited by other articles:

  • Zhao, J., Lai, L., Amara, R. R., Montefiori, D. C., Villinger, F., Chennareddi, L., Wyatt, L. S., Moss, B., Robinson, H. L. (2009). Preclinical Studies of Human Immunodeficiency Virus/AIDS Vaccines: Inverse Correlation between Avidity of Anti-Env Antibodies and Peak Postchallenge Viremia. J. Virol. 83: 4102-4111 [Abstract] [Full Text]  
  • Mahalanabis, M., Jayaraman, P., Miura, T., Pereyra, F., Chester, E. M., Richardson, B., Walker, B., Haigwood, N. L. (2009). Continuous Viral Escape and Selection by Autologous Neutralizing Antibodies in Drug-Naive Human Immunodeficiency Virus Controllers. J. Virol. 83: 662-672 [Abstract] [Full Text]  
  • Tagmyer, T. L., Craigo, J. K., Cook, S. J., Even, D. L., Issel, C. J., Montelaro, R. C. (2008). Envelope Determinants of Equine Infectious Anemia Virus Vaccine Protection and the Effects of Sequence Variation on Immune Recognition. J. Virol. 82: 4052-4063 [Abstract] [Full Text]  
  • Milush, J. M., Stefano-Cole, K., Schmidt, K., Durudas, A., Pandrea, I., Sodora, D. L. (2007). Mucosal Innate Immune Response Associated with a Timely Humoral Immune Response and Slower Disease Progression after Oral Transmission of Simian Immunodeficiency Virus to Rhesus Macaques. J. Virol. 81: 6175-6186 [Abstract] [Full Text]  
  • Tagmyer, T. L., Craigo, J. K., Cook, S. J., Issel, C. J., Montelaro, R. C. (2007). Envelope-specific T-helper and cytotoxic T-lymphocyte responses associated with protective immunity to equine infectious anemia virus. J. Gen. Virol. 88: 1324-1336 [Abstract] [Full Text]  
  • Gupta, S., Leutenegger, C. M., Dean, G. A., Steckbeck, J. D., Cole, K. S., Sparger, E. E. (2007). Vaccination of Cats with Attenuated Feline Immunodeficiency Virus Proviral DNA Vaccine Expressing Gamma Interferon. J. Virol. 81: 465-473 [Abstract] [Full Text]  
  • Margolin, D. H., Saunders, E. H., Bronfin, B., de Rosa, N., Axthelm, M. K., Goloubeva, O. G., Eapen, S., Gelman, R. S., Letvin, N. L. (2006). Germinal Center Function in the Spleen during Simian HIV Infection in Rhesus Monkeys. J. Immunol. 177: 1108-1119 [Abstract] [Full Text]  
  • Steckbeck, J. D., Orlov, I., Chow, A., Grieser, H., Miller, K., Bruno, J., Robinson, J. E., Montelaro, R. C., Cole, K. S. (2005). Kinetic Rates of Antibody Binding Correlate with Neutralization Sensitivity of Variant Simian Immunodeficiency Virus Strains. J. Virol. 79: 12311-12320 [Abstract] [Full Text]  
  • Hodara, V. L., Velasquillo, M. C., Parodi, L. M., Giavedoni, L. D. (2005). Expression of CD154 by a Simian Immunodeficiency Virus Vector Induces Only Transitory Changes in Rhesus Macaques. J. Virol. 79: 4679-4690 [Abstract] [Full Text]  
  • Craigo, J. K., Li, F., Steckbeck, J. D., Durkin, S., Howe, L., Cook, S. J., Issel, C., Montelaro, R. C. (2005). Discerning an Effective Balance between Equine Infectious Anemia Virus Attenuation and Vaccine Efficacy. J. Virol. 79: 2666-2677 [Abstract] [Full Text]  
  • Haigwood, N. L., Montefiori, D. C., Sutton, W. F., McClure, J., Watson, A. J., Voss, G., Hirsch, V. M., Richardson, B. A., Letvin, N. L., Hu, S.-L., Johnson, P. R. (2004). Passive Immunotherapy in Simian Immunodeficiency Virus-Infected Macaques Accelerates the Development of Neutralizing Antibodies. J. Virol. 78: 5983-5995 [Abstract] [Full Text]  
  • Bower, J. F., Yang, X., Sodroski, J., Ross, T. M. (2004). Elicitation of Neutralizing Antibodies with DNA Vaccines Expressing Soluble Stabilized Human Immunodeficiency Virus Type 1 Envelope Glycoprotein Trimers Conjugated to C3d. J. Virol. 78: 4710-4719 [Abstract] [Full Text]  
  • Cole, K. S., Steckbeck, J. D., Rowles, J. L., Desrosiers, R. C., Montelaro, R. C. (2004). Removal of N-Linked Glycosylation Sites in the V1 Region of Simian Immunodeficiency Virus gp120 Results in Redirection of B-Cell Responses to V3. J. Virol. 78: 1525-1539 [Abstract] [Full Text]  
  • Dreja, H., Gros, L., Villard, S., Bachrach, E., Oates, A., Granier, C., Chardes, T., Mani, J.-C., Piechaczyk, M., Pelegrin, M. (2003). Monoclonal Antibody 667 Recognizes the Variable Region A Motif of the Ecotropic Retrovirus CasBrE Envelope Glycoprotein and Inhibits Env Binding to the Viral Receptor. J. Virol. 77: 10984-10993 [Abstract] [Full Text]  
  • Li, F., Craigo, J. K., Howe, L., Steckbeck, J. D., Cook, S., Issel, C., Montelaro, R. C. (2003). A Live Attenuated Equine Infectious Anemia Virus Proviral Vaccine with a Modified S2 Gene Provides Protection from Detectable Infection by Intravenous Virulent Virus Challenge of Experimentally Inoculated Horses. J. Virol. 77: 7244-7253 [Abstract] [Full Text]  
  • Abel, K., Compton, L., Rourke, T., Montefiori, D., Lu, D., Rothaeusler, K., Fritts, L., Bost, K., Miller, C. J. (2003). Simian-Human Immunodeficiency Virus SHIV89.6-Induced Protection against Intravaginal Challenge with Pathogenic SIVmac239 Is Independent of the Route of Immunization and Is Associated with a Combination of Cytotoxic T-Lymphocyte and Alpha Interferon Responses. J. Virol. 77: 3099-3118 [Abstract] [Full Text]  
  • Green, T. D., Montefiori, D. C., Ross, T. M. (2003). Enhancement of Antibodies to the Human Immunodeficiency Virus Type 1 Envelope by Using the Molecular Adjuvant C3d. J. Virol. 77: 2046-2055 [Abstract] [Full Text]  
  • Van Rompay, K. K. A., Greenier, J. L., Cole, K. S., Earl, P., Moss, B., Steckbeck, J. D., Pahar, B., Rourke, T., Montelaro, R. C., Canfield, D. R., Tarara, R. P., Miller, C., McChesney, M. B., Marthas, M. L. (2002). Immunization of Newborn Rhesus Macaques with Simian Immunodeficiency Virus (SIV) Vaccines Prolongs Survival after Oral Challenge with Virulent SIVmac251. J. Virol. 77: 179-190 [Abstract] [Full Text]  
  • Shacklett, B. L., Shaw, K. E. S., Adamson, L. A., Wilkens, D. T., Cox, C. A., Montefiori, D. C., Gardner, M. B., Sonigo, P., Luciw, P. A. (2002). Live, Attenuated Simian Immunodeficiency Virus SIVmac-M4, with Point Mutations in the Env Transmembrane Protein Intracytoplasmic Domain, Provides Partial Protection from Mucosal Challenge with Pathogenic SIVmac251. J. Virol. 76: 11365-11378 [Abstract] [Full Text]  
  • Sarkar, S., Kalia, V., Murphey-Corb, M., Montelaro, R. C. (2002). 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: 4001-4011 [Abstract] [Full Text]  
  • Johnson, W. E., Morgan, J., Reitter, J., Puffer, B. A., Czajak, S., Doms, R. W., Desrosiers, R. C. (2002). A Replication-Competent, Neutralization-Sensitive Variant of Simian Immunodeficiency Virus Lacking 100 Amino Acids of Envelope. J. Virol. 76: 2075-2086 [Abstract] [Full Text]  
  • Puffer, B. A., Pohlmann, S., Edinger, A. L., Carlin, D., Sanchez, M. D., Reitter, J., Watry, D. D., Fox, H. S., Desrosiers, R. C., Doms, R. W. (2002). CD4 Independence of Simian Immunodeficiency Virus Envs Is Associated with Macrophage Tropism, Neutralization Sensitivity, and Attenuated Pathogenicity. J. Virol. 76: 2595-2605 [Abstract] [Full Text]  
  • Srivastava, I. K., Stamatatos, L., Legg, H., Kan, E., Fong, A., Coates, S. R., Leung, L., Wininger, M., Donnelly, J. J., Ulmer, J. B., Barnett, S. W. (2002). Purification and Characterization of Oligomeric Envelope Glycoprotein from a Primary R5 Subtype B Human Immunodeficiency Virus. J. Virol. 76: 2835-2847 [Abstract] [Full Text]  
  • Malenbaum, S. E., Yang, D., Cheng-Mayer, C. (2001). Evidence for Similar Recognition of the Conserved Neutralization Epitopes of Human Immunodeficiency Virus Type 1 Envelope gp120 in Humans and Macaques. J. Virol. 75: 9287-9296 [Abstract] [Full Text]  
  • ENSHELL-SEIJFFERS, D., SMELYANSKI, L., VARDINON, N., YUST, I., GERSHONI, J. M. (2001). Dissection of the humoral immune response toward an immunodominant epitope of HIV: a model for the analysis of antibody diversity in HIV+ individuals. FASEB J. 15: 2112-2120 [Abstract] [Full Text]  
  • Ly, A., Stamatatos, L. (2000). V2 Loop Glycosylation of the Human Immunodeficiency Virus Type 1 SF162 Envelope Facilitates Interaction of This Protein with CD4 and CCR5 Receptors and Protects the Virus from Neutralization by Anti-V3 Loop and Anti-CD4 Binding Site Antibodies. J. Virol. 74: 6769-6776 [Abstract] [Full Text]  
  • Shacklett, B. L., Weber, C. J., Shaw, K. E. S., Keddie, E. M., Gardner, M. B., Sonigo, P., Luciw, P. A. (2000). The Intracytoplasmic Domain of the Env Transmembrane Protein Is a Locus for Attenuation of Simian Immunodeficiency Virus SIVmac in Rhesus Macaques. J. Virol. 74: 5836-5844 [Abstract] [Full Text]  
  • Hammond, S. A., Li, F., McKeon, B. M. Sr., Cook, S. J., Issel, C. J., Montelaro, R. C. (2000). Immune Responses and Viral Replication in Long-Term Inapparent Carrier Ponies Inoculated with Equine Infectious Anemia Virus. J. Virol. 74: 5968-5981 [Abstract] [Full Text]  
  • Carpenter, S., Vaughn, E. M., Yang, J., Baccam, P., Roth, J. A., Wannemuehler, Y. (2000). Antigenic and genetic stability of bovine immunodeficiency virus during long-term persistence in cattle experimentally infected with the BIVR29 isolate. J. Gen. Virol. 81: 1463-1472 [Abstract] [Full Text]  
  • Giavedoni, L. D., Velasquillo, M. C., Parodi, L. M., Hubbard, G. B., Hodara, V. L. (2000). Cytokine Expression, Natural Killer Cell Activation, and Phenotypic Changes in Lymphoid Cells from Rhesus Macaques during Acute Infection with Pathogenic Simian Immunodeficiency Virus. J. Virol. 74: 1648-1657 [Abstract] [Full Text]  
  • Buge, S. L., Murty, L., Arora, K., Kalyanaraman, V. S., Markham, P. D., Richardson, E. S., Aldrich, K., Patterson, L. J., Miller, C. J., Cheng, S.-M., Robert-Guroff, M. (1999). Factors Associated with Slow Disease Progression in Macaques Immunized with an Adenovirus-Simian Immunodeficiency Virus (SIV) Envelope Priming-gp120 Boosting Regimen and Challenged Vaginally with SIVmac251. J. Virol. 73: 7430-7440 [Abstract] [Full Text]  
  • Johnson, R. P., Lifson, J. D., Czajak, S. C., Cole, K. S., Manson, K. H., Glickman, R., Yang, J., Montefiori, D. C., Montelaro, R., Wyand, M. S., Desrosiers, R. C. (1999). Highly Attenuated Vaccine Strains of Simian Immunodeficiency Virus Protect against Vaginal Challenge: Inverse Relationship of Degree of Protection with Level of Attenuation. J. Virol. 73: 4952-4961 [Abstract] [Full Text]  
  • Mazzetti, P., Giannecchini, S., Del Mauro, D., Matteucci, D., Portincasa, P., Merico, A., Chezzi, C., Bendinelli, M. (1999). AIDS Vaccination Studies Using an Ex Vivo Feline Immunodeficiency Virus Model: Detailed Analysis of the Humoral Immune Response to a Protective Vaccine. J. Virol. 73: 1-10 [Abstract] [Full Text]  
  • Kent, S. J., Zhao, A., Best, S. J., Chandler, J. D., Boyle, D. B., Ramshaw, I. A. (1998). Enhanced T-Cell Immunogenicity and Protective Efficacy of a Human Immunodeficiency Virus Type 1 Vaccine Regimen Consisting of Consecutive Priming with DNA and Boosting with Recombinant Fowlpox Virus. J. Virol. 72: 10180-10188 [Abstract] [Full Text]  
  • Richmond, J. F. L., Lu, S., Santoro, J. C., Weng, J., Hu, S.-L., Montefiori, D. C., Robinson, H. L. (1998). Studies of the Neutralizing Activity and Avidity of Anti-Human Immunodeficiency Virus Type 1 Env Antibody Elicited by DNA Priming and Protein Boosting. J. Virol. 72: 9092-9100 [Abstract] [Full Text]  
  • Gundlach, B. R., Reiprich, S., Sopper, S., Means, R. E., Dittmer, U., Matz-Rensing, K., Stahl-Hennig, C., Uberla, K. (1998). Env-Independent Protection Induced by Live, Attenuated Simian Immunodeficiency Virus Vaccines. J. Virol. 72: 7846-7851 [Abstract] [Full Text]  
  • Cole, K. S., Murphey-Corb, M., Narayan, O., Joag, S. V., Shaw, G. M., Montelaro, R. C. (1998). Common Themes of Antibody Maturation to Simian Immunodeficiency Virus, Simian-Human Immunodeficiency Virus, and Human Immunodeficiency Virus Type 1 Infections. J. Virol. 72: 7852-7859 [Abstract] [Full Text]  
  • Etemad-Moghadam, B., Karlsson, G. B., Halloran, M., Sun, Y., Schenten, D., Fernandes, M., Letvin, N. L., Sodroski, J. (1998). Characterization of Simian-Human Immunodeficiency Virus Envelope Glycoprotein Epitopes Recognized by Neutralizing Antibodies from Infected Monkeys. J. Virol. 72: 8437-8445 [Abstract] [Full Text]  
  • Harmache, A., Vitu, C., Guiguen, F., Russo, P., Bertoni, G., Pepin, M., Vigne, R., Suzan, M. (1998). Priming with tat-Deleted Caprine Arthritis Encephalitis Virus (CAEV) Proviral DNA or Live Virus Protects Goats from Challenge with Pathogenic CAEV. J. Virol. 72: 6796-6804 [Abstract] [Full Text]  
  • Langlois, A. J., Desrosiers, R. C., Lewis, M. G., KewalRamani, V. N., Littman, D. R., Zhou, J. Y., Manson, K., Wyand, M. S., Bolognesi, D. P., Montefiori, D. C. (1998). Neutralizing Antibodies in Sera from Macaques Immunized with Attenuated Simian Immunodeficiency Virus. J. Virol. 72: 6950-6955 [Abstract] [Full Text]