A Period of Transient Viremia and Occult Infection Precedes Persistent Viremia and Antiviral Immune Responses During Multiple Low-dose Intravaginal Simian Immunodeficiency Virus Inoculations

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 2004 Nov 27

PMID 15564513

Citations 29

Authors

Zhong-Min Ma

Kristina Abel

Tracy Rourke

Yichuan Wang

Christopher J Miller

Affiliations

Soon will be listed here.

Abstract

In rhesus macaques, classic systemic infection, characterized by persistent viremia and seroconversion, occurred after multiple low-dose (10(3) 50% tissue culture infective doses) intravaginal (IVAG) inoculations with simian immunodeficiency virus (SIV) strain SIVmac251. Monkeys developed classic SIV infections after a variable number of low-dose IVAG exposures to SIVmac251. Once established, the systemic infection was identical to SIV infection following high-dose IVAG SIV inoculation. However, occult systemic infection characterized by transient cell-associated or cell-free viremia consistently occurred early in the series of multiple vaginal SIV exposures. Further, antiviral cellular immune responses were present prior to the establishment of a classic systemic infection in the low-dose vaginal SIV transmission model.

Citing Articles

Antiretroviral therapy reveals triphasic decay of intact SIV genomes and persistence of ancestral variants.

Fray E, Wu F, Simonetti F, Zitzmann C, Sambaturu N, Molina-Paris C Cell Host Microbe. 2023; 31(3):356-372.e5.

PMID: 36809762 PMC: 10583177. DOI: 10.1016/j.chom.2023.01.016.

Recombinant Herpesvirus Vectors: Durable Immune Responses and Durable Protection against Simian Immunodeficiency Virus SIVmac239 Acquisition.

Castro I, Ricciardi M, Gonzalez-Nieto L, Rakasz E, Lifson J, Desrosiers R J Virol. 2021; 95(14):e0033021.

PMID: 33910957 PMC: 8223948. DOI: 10.1128/JVI.00330-21.

Lymphatic Dissemination of Simian Immunodeficiency Virus after Penile Inoculation.

Ma Z, Dutra J, Fritts L, Miller C J Virol. 2016; 90(8):4093-4104.

PMID: 26865706 PMC: 4810538. DOI: 10.1128/JVI.02947-15.

A Shot in the Arm for HIV Prevention? Recent Successes and Critical Thresholds.

Hope T, Marrazzo J AIDS Res Hum Retroviruses. 2015; 31(11):1055-9.

PMID: 26486613 PMC: 4651048. DOI: 10.1089/aid.2015.0310.

Parsimonious Determination of the Optimal Infectious Dose of a Pathogen for Nonhuman Primate Models.

Roederer M PLoS Pathog. 2015; 11(8):e1005100.

PMID: 26285041 PMC: 4540461. DOI: 10.1371/journal.ppat.1005100.

References

Beyrer C, Artenstein A, Rugpao S, Stephens H, Vancott T, Robb M . Epidemiologic and biologic characterization of a cohort of human immunodeficiency virus type 1 highly exposed, persistently seronegative female sex workers in northern Thailand. Chiang Mai HEPS Working Group. J Infect Dis. 1998; 179(1):59-67. DOI: 10.1086/314556. View

McChesney M, Collins J, Lu D, Lu X, Torten J, Ashley R . Occult systemic infection and persistent simian immunodeficiency virus (SIV)-specific CD4(+)-T-cell proliferative responses in rhesus macaques that were transiently viremic after intravaginal inoculation of SIV. J Virol. 1998; 72(12):10029-35. PMC: 110525. DOI: 10.1128/JVI.72.12.10029-10035.1998. View

Lu X, Kiyono H, Lu D, Kawabata S, Torten J, Srinivasan S . Targeted lymph-node immunization with whole inactivated simian immunodeficiency virus (SIV) or envelope and core subunit antigen vaccines does not reliably protect rhesus macaques from vaginal challenge with SIVmac251. AIDS. 1998; 12(1):1-10. PMC: 3401021. DOI: 10.1097/00002030-199801000-00001. View

Miller C, McChesney M, Lu X, Dailey P, Chutkowski C, Lu D . Rhesus macaques previously infected with simian/human immunodeficiency virus are protected from vaginal challenge with pathogenic SIVmac239. J Virol. 1997; 71(3):1911-21. PMC: 191267. DOI: 10.1128/JVI.71.3.1911-1921.1997. View

Miller C, Marthas M, Torten J, Alexander N, Moore J, Doncel G . Intravaginal inoculation of rhesus macaques with cell-free simian immunodeficiency virus results in persistent or transient viremia. J Virol. 1994; 68(10):6391-400. PMC: 237059. DOI: 10.1128/JVI.68.10.6391-6400.1994. View

Lohman B, Higgins J, Marthas M, Marx P, Pedersen N . Development of simian immunodeficiency virus isolation, titration, and neutralization assays which use whole blood from rhesus monkeys and an antigen capture enzyme-linked immunosorbent assay. J Clin Microbiol. 1991; 29(10):2187-92. PMC: 270295. DOI: 10.1128/jcm.29.10.2187-2192.1991. View

Miller C, Alexander N, Sutjipto S, Lackner A, Gettie A, Hendrickx A . Genital mucosal transmission of simian immunodeficiency virus: animal model for heterosexual transmission of human immunodeficiency virus. J Virol. 1989; 63(10):4277-84. PMC: 251042. DOI: 10.1128/JVI.63.10.4277-4284.1989. View

Zhu T, Corey L, Hwangbo Y, Lee J, Learn G, Mullins J . Persistence of extraordinarily low levels of genetically homogeneous human immunodeficiency virus type 1 in exposed seronegative individuals. J Virol. 2003; 77(11):6108-16. PMC: 154986. DOI: 10.1128/jvi.77.11.6108-6116.2003. View

Promadej N, Costello C, Wernett M, Kulkarni P, Robison V, Nelson K . Broad human immunodeficiency virus (HIV)-specific T cell responses to conserved HIV proteins in HIV-seronegative women highly exposed to a single HIV-infected partner. J Infect Dis. 2003; 187(7):1053-63. DOI: 10.1086/368127. View

10.

Coombs R, Reichelderfer P, Landay A . Recent observations on HIV type-1 infection in the genital tract of men and women. AIDS. 2003; 17(4):455-80. DOI: 10.1097/00002030-200303070-00001. View

11.

Abel K, Compton L, Rourke T, Montefiori D, Lu D, Rothaeusler K . 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.... J Virol. 2003; 77(5):3099-118. PMC: 149756. DOI: 10.1128/jvi.77.5.3099-3118.2003. View

12.

Van Rompay K, Greenier J, Cole K, Earl P, Moss B, Steckbeck J . Immunization of newborn rhesus macaques with simian immunodeficiency virus (SIV) vaccines prolongs survival after oral challenge with virulent SIVmac251. J Virol. 2002; 77(1):179-90. PMC: 140621. DOI: 10.1128/jvi.77.1.179-190.2003. View

13.

Okamoto M, Byrn R, Eyre R, Mullen T, Church P, Kiessling A . Seminal plasma induces programmed cell death in cultured peripheral blood mononuclear cells. AIDS Res Hum Retroviruses. 2002; 18(11):797-803. DOI: 10.1089/08892220260139549. View

14.

Williams S, Flanigan T, Cu-Uvin S, Mayer K, Williams P, Ettore C . Human immunodeficiency virus (HIV)-specific antibody in cervicovaginal lavage specimens obtained from women infected with HIV type 1. Clin Infect Dis. 2002; 35(5):611-7. DOI: 10.1086/342201. View

15.

Marthas M, Lu D, Penedo M, Hendrickx A, Miller C . Titration of an SIVmac251 stock by vaginal inoculation of Indian and Chinese origin rhesus macaques: transmission efficiency, viral loads, and antibody responses. AIDS Res Hum Retroviruses. 2001; 17(15):1455-66. PMC: 3401017. DOI: 10.1089/088922201753197123. View

16.

Schmechel S, Russell N, HLADIK F, LANG J, Wilson A, Ha R . Immune defence against HIV-1 infection in HIV-1-exposed seronegative persons. Immunol Lett. 2001; 79(1-2):21-7. DOI: 10.1016/s0165-2478(01)00262-0. View

17.

Kaul R, Rowland-Jones S, Kimani J, Fowke K, Dong T, Kiama P . New insights into HIV-1 specific cytotoxic T-lymphocyte responses in exposed, persistently seronegative Kenyan sex workers. Immunol Lett. 2001; 79(1-2):3-13. DOI: 10.1016/s0165-2478(01)00260-7. View