Live simian immunodeficiency virus vaccine correlate of protection: Local antibody production and concentration on the path of virus entry

Qingsheng Li; Ming Zeng; Lijie Duan; James E. Voss; Anthony J. Smith; Stefan Pambuccian; Liang Shang; Stephen Wietgrefe; Peter J. Southern; Cavan S. Reilly; Pamela J. Skinner; Mary L. Zupancic; John V. Carlis; Michael Piatak; Diane Waterman; R. Keith Reeves; Katherine Masek-Hammerman; Cynthia A. Derdeyn; Michael D. Alpert; David T. Evans; Heinz Kohler; Sybille Müller; James Robinson; Jeffrey D. Lifson; Dennis R. Burton; R. Paul Johnson; Ashley T. Haase

doi:10.4049/jimmunol.1400820

Live simian immunodeficiency virus vaccine correlate of protection: Local antibody production and concentration on the path of virus entry

Qingsheng Li, Ming Zeng, Lijie Duan, James E. Voss, Anthony J. Smith, Stefan Pambuccian, Liang Shang, Stephen Wietgrefe, Peter J. Southern, Cavan S. Reilly, Pamela J. Skinner, Mary L. Zupancic, John V. Carlis, Michael Piatak, Diane Waterman, R. Keith Reeves, Katherine Masek-Hammerman, Cynthia A. Derdeyn, Michael D. Alpert, David T. EvansHeinz Kohler, Sybille Müller, James Robinson, Jeffrey D. Lifson, Dennis R. Burton, R. Paul Johnson, Ashley T. Haase

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Abstract

We sought design principles for a vaccine to prevent HIV transmission to women by identifying correlates of protection conferred by a highly effective live attenuated SIV vaccine in the rhesus macaque animal model. We show that SIVmac239Δnef vaccination recruits plasma cells and induces ectopic lymphoid follicle formation beneath the mucosal epithelium in the rhesus macaque female reproductive tract. The plasma cells and ectopic follicles produce IgG Abs reactive with viral envelope glycoprotein gp41 trimers, and these Abs are concentrated on the path of virus entry by the neonatal FcR in cervical reserve epithelium and in vaginal epithelium. This local Ab production and delivery system correlated spatially and temporally with the maturation of local protection against high-dose pathogenic SIV vaginal challenge. Thus, designing vaccines to elicit production and concentration of Abs at mucosal frontlines could aid in the development of an effective vaccine to protect women against HIV-1.

Original language	English (US)
Pages (from-to)	3113-3125
Number of pages	13
Journal	Journal of Immunology
Volume	193
Issue number	6
DOIs	https://doi.org/10.4049/jimmunol.1400820
State	Published - Sep 15 2014

Bibliographical note

Funding Information:
This work was supported by a grant from the International AIDS Vaccine Initiative (to A.T.H.); National Institutes of Health Grants AI 086922 (to A.T.H.), AI 071306 and RR00168 (to R.P.J.), AI095985 (to R.P.J. and A.T.H.), and AI 055332 and 1UM1AI100663 (to D.R.B.); a Center for HIV/AIDS Vaccine Immunology/HIV Vaccine Trials Network Early Stage Investigator award and Grant U19 AI 067854 (to R.K.R.); a Ragon Fellowship (to J.E.V.); and by federal funds from the National Cancer Institute, National Institutes of Health under Contract HHSN261200800001E and the National Institutes of Health/National Institute of Allergy and Infectious Diseases Reagent Resource Support Program for AIDS Vaccine Development, Quality Biological, Inc., Gaithersburg, MD (National Institute of Allergy and Infectious Diseases Division of AIDS Contract HHSN272201100023C).

Publisher Copyright:
Copyright © 2014 by The American Association of Immunologists, Inc.

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Li, Q., Zeng, M., Duan, L., Voss, J. E., Smith, A. J., Pambuccian, S., Shang, L., Wietgrefe, S., Southern, P. J., Reilly, C. S., Skinner, P. J., Zupancic, M. L., Carlis, J. V., Piatak, M., Waterman, D., Reeves, R. K., Masek-Hammerman, K., Derdeyn, C. A., Alpert, M. D., ... Haase, A. T. (2014). Live simian immunodeficiency virus vaccine correlate of protection: Local antibody production and concentration on the path of virus entry. Journal of Immunology, 193(6), 3113-3125. https://doi.org/10.4049/jimmunol.1400820

Li, Q, Zeng, M, Duan, L, Voss, JE, Smith, AJ, Pambuccian, S, Shang, L, Wietgrefe, S, Southern, PJ , Reilly, CS , Skinner, PJ, Zupancic, ML, Carlis, JV, Piatak, M, Waterman, D, Reeves, RK, Masek-Hammerman, K, Derdeyn, CA, Alpert, MD, Evans, DT, Kohler, H, Müller, S, Robinson, J, Lifson, JD, Burton, DR, Johnson, RP & Haase, AT 2014, 'Live simian immunodeficiency virus vaccine correlate of protection: Local antibody production and concentration on the path of virus entry', Journal of Immunology, vol. 193, no. 6, pp. 3113-3125. https://doi.org/10.4049/jimmunol.1400820

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title = "Live simian immunodeficiency virus vaccine correlate of protection: Local antibody production and concentration on the path of virus entry",

abstract = "We sought design principles for a vaccine to prevent HIV transmission to women by identifying correlates of protection conferred by a highly effective live attenuated SIV vaccine in the rhesus macaque animal model. We show that SIVmac239Δnef vaccination recruits plasma cells and induces ectopic lymphoid follicle formation beneath the mucosal epithelium in the rhesus macaque female reproductive tract. The plasma cells and ectopic follicles produce IgG Abs reactive with viral envelope glycoprotein gp41 trimers, and these Abs are concentrated on the path of virus entry by the neonatal FcR in cervical reserve epithelium and in vaginal epithelium. This local Ab production and delivery system correlated spatially and temporally with the maturation of local protection against high-dose pathogenic SIV vaginal challenge. Thus, designing vaccines to elicit production and concentration of Abs at mucosal frontlines could aid in the development of an effective vaccine to protect women against HIV-1.",

author = "Qingsheng Li and Ming Zeng and Lijie Duan and Voss, {James E.} and Smith, {Anthony J.} and Stefan Pambuccian and Liang Shang and Stephen Wietgrefe and Southern, {Peter J.} and Reilly, {Cavan S.} and Skinner, {Pamela J.} and Zupancic, {Mary L.} and Carlis, {John V.} and Michael Piatak and Diane Waterman and Reeves, {R. Keith} and Katherine Masek-Hammerman and Derdeyn, {Cynthia A.} and Alpert, {Michael D.} and Evans, {David T.} and Heinz Kohler and Sybille M{\"u}ller and James Robinson and Lifson, {Jeffrey D.} and Burton, {Dennis R.} and Johnson, {R. Paul} and Haase, {Ashley T.}",

note = "Funding Information: This work was supported by a grant from the International AIDS Vaccine Initiative (to A.T.H.); National Institutes of Health Grants AI 086922 (to A.T.H.), AI 071306 and RR00168 (to R.P.J.), AI095985 (to R.P.J. and A.T.H.), and AI 055332 and 1UM1AI100663 (to D.R.B.); a Center for HIV/AIDS Vaccine Immunology/HIV Vaccine Trials Network Early Stage Investigator award and Grant U19 AI 067854 (to R.K.R.); a Ragon Fellowship (to J.E.V.); and by federal funds from the National Cancer Institute, National Institutes of Health under Contract HHSN261200800001E and the National Institutes of Health/National Institute of Allergy and Infectious Diseases Reagent Resource Support Program for AIDS Vaccine Development, Quality Biological, Inc., Gaithersburg, MD (National Institute of Allergy and Infectious Diseases Division of AIDS Contract HHSN272201100023C). Publisher Copyright: Copyright {\textcopyright} 2014 by The American Association of Immunologists, Inc.",

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AU - Li, Qingsheng

AU - Zeng, Ming

AU - Duan, Lijie

AU - Voss, James E.

AU - Smith, Anthony J.

AU - Pambuccian, Stefan

AU - Shang, Liang

AU - Wietgrefe, Stephen

AU - Southern, Peter J.

AU - Reilly, Cavan S.

AU - Skinner, Pamela J.

AU - Zupancic, Mary L.

AU - Carlis, John V.

AU - Piatak, Michael

AU - Waterman, Diane

AU - Reeves, R. Keith

AU - Masek-Hammerman, Katherine

AU - Derdeyn, Cynthia A.

AU - Alpert, Michael D.

AU - Evans, David T.

AU - Kohler, Heinz

AU - Müller, Sybille

AU - Robinson, James

AU - Lifson, Jeffrey D.

AU - Burton, Dennis R.

AU - Johnson, R. Paul

AU - Haase, Ashley T.

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N2 - We sought design principles for a vaccine to prevent HIV transmission to women by identifying correlates of protection conferred by a highly effective live attenuated SIV vaccine in the rhesus macaque animal model. We show that SIVmac239Δnef vaccination recruits plasma cells and induces ectopic lymphoid follicle formation beneath the mucosal epithelium in the rhesus macaque female reproductive tract. The plasma cells and ectopic follicles produce IgG Abs reactive with viral envelope glycoprotein gp41 trimers, and these Abs are concentrated on the path of virus entry by the neonatal FcR in cervical reserve epithelium and in vaginal epithelium. This local Ab production and delivery system correlated spatially and temporally with the maturation of local protection against high-dose pathogenic SIV vaginal challenge. Thus, designing vaccines to elicit production and concentration of Abs at mucosal frontlines could aid in the development of an effective vaccine to protect women against HIV-1.

AB - We sought design principles for a vaccine to prevent HIV transmission to women by identifying correlates of protection conferred by a highly effective live attenuated SIV vaccine in the rhesus macaque animal model. We show that SIVmac239Δnef vaccination recruits plasma cells and induces ectopic lymphoid follicle formation beneath the mucosal epithelium in the rhesus macaque female reproductive tract. The plasma cells and ectopic follicles produce IgG Abs reactive with viral envelope glycoprotein gp41 trimers, and these Abs are concentrated on the path of virus entry by the neonatal FcR in cervical reserve epithelium and in vaginal epithelium. This local Ab production and delivery system correlated spatially and temporally with the maturation of local protection against high-dose pathogenic SIV vaginal challenge. Thus, designing vaccines to elicit production and concentration of Abs at mucosal frontlines could aid in the development of an effective vaccine to protect women against HIV-1.

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Live simian immunodeficiency virus vaccine correlate of protection: Local antibody production and concentration on the path of virus entry

Abstract

Bibliographical note

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