B cell responses associated with vaccine-induced delayed SIVmac251 acquisition in female rhesus macaques

Journal of Immunology

Volumn 197, Issue 6, 2016, Pages 2316-2324

  Mohanram, Venkatramanan ^a   Demberg, Thorsten ^a   Musich, Thomas ^a   Tuero, Iskra ^a   Vargas Inchaustegui, Diego A ^a   Miller Novak, Leia ^a   Venzon, David ^a   Robert Guroff, Marjorie ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; MESSENGER RNA; IMMUNOGLOBULIN G; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CD4 LYMPHOCYTE COUNT; CELL POPULATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; HUMORAL IMMUNITY; IMMUNOREGULATION; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MALE; MEMORY CELL; MOLECULAR DYNAMICS; NONHUMAN; PLASMABLAST; PRIORITY JOURNAL; RHESUS MONKEY; SEX DIFFERENCE; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; ANIMAL; ANTIBODY AFFINITY; BLOOD; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PHAGOCYTOSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIREMIA;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; B-LYMPHOCYTES; FEMALE; IMMUNOGLOBULIN G; IMMUNOLOGIC MEMORY; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MACACA MULATTA; PHAGOCYTOSIS; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; VIREMIA;

EID: 84988980960     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600544     Document Type: Article

References (40)

1. Rerks-Ngarm, S., P. Pitisuttithum, S. Nitayaphan, J. Kaewkungwal, J. Chiu, R. Paris, N. Premsri, C. Namwat, M. de Souza, E. Adams, et al. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361: 2209-2220.
2. Porakishvili, N., R. Mageed, C. Jamin, J. O. Pers, N. Kulikova, Y. Renaudineau, P. M. Lydyard, and P. Youinou. 2001. Recent progress in the understanding of B-cell functions in autoimmunity. Scand. J. Immunol. 54: 30-38.
3. Silverman, G. J., and D. A. Carson. 2003. Roles of B cells in rheumatoid arthritis. Arthritis Res. Ther. 5(Suppl. 4): S1-S6.
4. Anderton, S. M., and S. Fillatreau. 2008. Activated B cells in autoimmune diseases: the case for a regulatory role. Nat. Clin. Pract. Rheumatol. 4: 657-666.
5. Kessel, A., T. Haj, R. Peri, A. Snir, D. Melamed, E. Sabo, and E. Toubi. 2012. Human CD19+CD25high B regulatory cells suppress proliferation of CD4+ T cells and enhance Foxp3 and CTLA-4 expression in T-regulatory cells. Autoimmun. Rev. 11: 670-677.
6. de Andrés, C., M. Tejera-Alhambra, B. Alonso, L. Valor, R. Teijeiro, R. Ramos-Medina, D. Mateos, F. Faure, and S. Sánchez-Ramón. 2014. New regulatory CD19+CD25+ B-cell subset in clinically isolated syndrome and multiple sclerosis relapse: changes after glucocorticoids. J. Neuroimmunol. 270: 37-44.
7. Siewe, B., J. Wallace, S. Rygielski, J. T. Stapleton, J. Martin, S. G. Deeks, and A. Landay. 2014. Regulatory B cells inhibit cytotoxic T lymphocyte (CTL) activity and elimination of infected CD4 T cells after in vitro reactivation of HIV latent reservoirs. PLoS One 9: e92934.
8. Das, A., G. Ellis, C. Pallant, A. R. Lopes, P. Khanna, D. Peppa, A. Chen, P. Blair, G. Dusheiko, U. Gill, et al. 2012. IL-10-producing regulatory B cells in the pathogenesis of chronic hepatitis B virus infection. J. Immunol. 189: 3925-3935.
9. Moir, S., and A. S. Fauci. 2013. Insights into B cells and HIV-specific B-cell responses in HIV-infected individuals. Immunol. Rev. 254: 207-224.
10. Kuhrt, D., S. A. Faith, A. Leone, M. Rohankedkar, D. L. Sodora, L. J. Picker, and K. S. Cole. 2010. Evidence of early B-cell dysregulation in simian immunodeficiency virus infection: rapid depletion of naïve and memory B-cell subsets with delayed reconstitution of the naive B-cell population. J. Virol. 84: 2466-2476.
11. D'Orsogna, L. J., R. G. Krueger, E. J. McKinnon, and M. A. French. 2007. Circulating memory B-cell subpopulations are affected differently by HIV infection and antiretroviral therapy. AIDS 21: 1747-1752.
12. Regidor, D. L., R. Detels, E. C. Breen, D. P. Widney, L. P. Jacobson, F. Palella, C. R. Rinaldo, J. H. Bream, and O. Martínez-Maza. 2011. Effect of highly active antiretroviral therapy on biomarkers of B-lymphocyte activation and inflammation. AIDS 25: 303-314.
13. Demberg, T., E. Brocca-Cofano, P. Xiao, D. Venzon, D. Vargas-Inchaustegui, E. M. Lee, I. Kalisz, V. S. Kalyanaraman, J. Dipasquale, K. McKinnon, and M. Robert-Guroff. 2012. Dynamics of memory B-cell populations in blood, lymph nodes, and bone marrow during antiretroviral therapy and envelope boosting in simian immunodeficiency virus SIVmac251-infected rhesus macaques. J. Virol. 86: 12591-12604.
14. Morgan, C., M. Marthas, C. Miller, A. Duerr, C. Cheng-Mayer, R. Desrosiers, J. Flores, N. Haigwood, S. L. Hu, R. P. Johnson, et al. 2008. The use of nonhuman primate models in HIV vaccine development. PLoS Med. 5: e173.
15. Fennessey, C. M., and B. F. Keele. 2013. Using nonhuman primates to model HIV transmission. Curr. Opin. HIV AIDS 8: 280-287.
16. Addo, M. M., and M. Altfeld. 2014. Sex-based differences in HIV type 1 pathogenesis. J. Infect. Dis. 209(Suppl 3): S86-S92.
17. Tuero, I., V. Mohanram, T. Musich, L. Miller, D. A. Vargas-Inchaustegui, T. Demberg, D. Venzon, I. Kalisz, V. S. Kalyanaraman, R. Pal, et al. 2015. Mucosal B cells are associated with delayed SIV acquisition in vaccinated female but not male rhesus macaques following SIVmac251 rectal challenge. PLoS Pathog. 11: e1005101.
18. Afshan, G., N. Afzal, and S. Qureshi. 2012. CD4+CD25hi regulatory T cells in healthy males and females mediate gender difference in the prevalence of autoimmune diseases. Clin. Lab. 58: 567-571.
19. Lee, E. M., H. K. Chung, J. Livesay, J. Suschak, L. Finke, L. Hudacik, L. Galmin, B. Bowen, P. Markham, A. Cristillo, and R. Pal. 2010. Molecular methods for evaluation of virological status of nonhuman primates challenged with simian immunodeficiency or simian-human immunodeficiency viruses. J. Virol. Methods 163: 287-294.
20. Mohanram, V., T. Demberg, I. Tuero, D. Vargas-Inchaustegui, G. N. Pavlakis, B. K. Felber, and M. Robert-Guroff. 2014. Improved flow-based method for HIV/SIV envelope-specific memory B-cell evaluation in rhesus macaques. J. Immunol. Methods 412: 78-84.
21. Demberg, T., V. Mohanram, D. Venzon, and M. Robert-Guroff. 2014. Phenotypes and distribution of mucosal memory B-cell populations in the SIV/SHIV rhesus macaque model. Clin. Immunol. 153: 264-276.
22. Demberg, T., A. C. Ettinger, S. Aladi, K. McKinnon, T. Kuddo, D. Venzon, L. J. Patterson, T. M. Phillips, and M. Robert-Guroff. 2011. Strong viremia control in vaccinated macaques does not prevent gradual Th17 cell loss from central memory. Vaccine 29: 6017-6028.
23. Demberg, T., E. Brocca-Cofano, S. Kuate, S. Aladi, D. A. Vargas-Inchaustegui, D. Venzon, I. Kalisz, V. S. Kalyanaraman, E. M. Lee, R. Pal, et al. 2013. Impact of antibody quality and anamnestic response on viremia control post-challenge in a combined Tat/Env vaccine regimen in rhesus macaques. Virology 440: 210-221.
24. Zhao, J., L. Lai, R. R. Amara, D. C. Montefiori, F. Villinger, L. Chennareddi, L. S. Wyatt, B. Moss, and H. L. Robinson. 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.
25. Xiao, P., J. Zhao, L. J. Patterson, E. Brocca-Cofano, D. Venzon, P. A. Kozlowski, R. Hidajat, T. Demberg, and M. Robert-Guroff. 2010. Multiple vaccine-elicited nonneutralizing antienvelope antibody activities contribute to protective efficacy by reducing both acute and chronic viremia following simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J. Virol. 84: 7161-7173.
26. Gómez-Román, V. R., R. H. Florese, L. J. Patterson, B. Peng, D. Venzon, K. Aldrich, and M. Robert-Guroff. 2006. A simplified method for the rapid fluorometric assessment of antibody-dependent cell-mediated cytotoxicity. J. Immunol. Methods 308: 53-67.
27. Ackerman, M. E., B. Moldt, R. T. Wyatt, A. S. Dugast, E. McAndrew, S. Tsoukas, S. Jost, C. T. Berger, G. Sciaranghella, Q. Liu, et al. 2011. A robust, high-throughput assay to determine the phagocytic activity of clinical antibody samples. J. Immunol. Methods 366: 8-19.
28. Schur, P. H. 1988. IgG subclasses: a historical perspective. Monogr. Allergy 23: 1-11.
29. Ferrante, A., L. J. Beard, and R. G. Feldman. 1990. IgG subclass distribution of antibodies to bacterial and viral antigens. Pediatr. Infect. Dis. J. 9(Suppl.): S16-S24.
30. Bindon, C. I., G. Hale, M. Brüggemann, and H. Waldmann. 1988. Human monoclonal IgG isotypes differ in complement activating function at the level of C4 as well as C1q. J. Exp. Med. 168: 127-142.
31. Yates, N. L., H. X. Liao, Y. Fong, A. deCamp, N. A. Vandergrift,W. T. Williams, S. M. Alam, G. Ferrari, Z. Y. Yang, K. E. Seaton, et al. 2014. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci. Transl. Med. 6: 228ra39.
32. Agematsu, K. 2000. Memory B cells and CD27. Histol. Histopathol. 15: 573-576.
33. Brisslert, M., M. Bokarewa, P. Larsson, K. Wing, L. V. Collins, and A. Tarkowski. 2006. Phenotypic and functional characterization of human CD25+ B cells. Immunology 117: 548-557.
34. Amu, S., A. Tarkowski, T. Dörner, M. Bokarewa, and M. Brisslert. 2007. The human immunomodulatory CD25+ B cell population belongs to the memory B cell pool. Scand. J. Immunol. 66: 77-86.
35. Liu, J., W. Zhan, C. J. Kim, K. Clayton, H. Zhao, E. Lee, J. C. Cao, B. Ziegler, A. Gregor, F. Y. Yue, et al. 2014. IL-10-producing B cells are induced early in HIV-1 infection and suppress HIV-1-specific T cell responses. PLoS One 9: e89236.
36. Ravetch, J. V., and S. Bolland. 2001. IgG Fc receptors. Annu. Rev. Immunol. 19: 275-290.
37. Mauri, C., and A. Bosma. 2012. Immune regulatory function of B cells. Annu. Rev. Immunol. 30: 221-241.
38. Shen, P., and S. Fillatreau. 2015. Suppressive functions of B cells in infectious diseases. Int. Immunol. 27: 513-519.
39. Fettke, F., A. Schumacher, S. D. Costa, and A. C. Zenclussen. 2014. B cells: the old new players in reproductive immunology. Front. Immunol. 5: 285.
40. Muzzio, D., M. Zygmunt, and F. Jensen. 2014. The role of pregnancy-associated hormones in the development and function of regulatory B cells. Front. Endocrinol. (Lausanne) 5: 39.