DOI: 10.1128/jvi.72.11.9400-9403.1998. Requirement for CD4+ T Cells in the Friend Murine Retrovirus Neutralizing Antibody Response: Evidence for Functional T Cells in Genetic Low-Recovery Mice

Requirement for CD4+ T Cells in the Friend Murine Retrovirus Neutralizing Antibody Response: Evidence for Functional T Cells in Genetic Low-Recovery Mice

10.1128/jvi.72.11.9400-9403.1998

Crossref journal-article

American Society for Microbiology

Journal of Virology (235)

Abstract

ABSTRACTRecovery from infection with the Friend murine leukemia retrovirus complex (FV) requires T-helper cells and cytotoxic T cells as well as neutralizing antibodies. Several host genes, including genes of the major histocompatibility complex (H-2) and anH-2-unlinked gene,Rfv-3, influence these FV-specific immune responses. (B10.A × A/Wy)F1mice, which have theH-2a/aRfv-3r/sgenotype, fail to mount a detectable FV-specific T-cell proliferative response but nevertheless produce FV-specific neutralizing immunoglobulin M (IgM) antibodies and can eliminate FV viremia. Thus, this IgM response, primarily influenced by theRfv-3gene, may be T-cell independent. To test this idea, mice were depleted of either CD4+or CD8+T-cell populations in vivo and were monitored for the effect on the neutralizing antibody response following FV infection. Surprisingly, mice in which CD4+cells were depleted showed undetectable FV-neutralizing antibody responses and high viremia levels compared to nondepleted or CD8-depleted animals. In addition to knocking out the FV antibody response, CD4+T-cell depletion reduced survival time significantly, further indicating the importance of CD4+T cells. These studies revealed the first evidence for a functional T-cell response following FV infection in these low-recovery mice and showed that CD4+T-helper cells are required for theRfv-3-controlled FV antibody response.

Bibliography

Super, H. J., Brooks, D., Hasenkrug, K., & Chesebro, B. (1998). Requirement for CD4+ T Cells in the Friend Murine Retrovirus Neutralizing Antibody Response: Evidence for Functional T Cells in Genetic Low-Recovery Mice. Journal of Virology, 72(11), 9400â9403. LOCKSS.

Authors 4

Heidi J. Super (first)
Diane Brooks (additional)
Kim Hasenkrug (additional)
Bruce Chesebro (additional)

References 29 Referenced 19

10.1016/S0167-5699(96)10066-9 / Immunol. Today / The influence of virus structure on antibody responses and virus serotype formation by Bachmann (1996)
10.1128/JVI.68.7.4700-4704.1994 / J. Virol. / Enhanced establishment of a virus carrier state in adult CD4+ T-cell-deficient mice by Battegay (1994)
10.1128/JVI.68.9.6103-6110.1994 / J. Virol. / Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection by Borrow (1994)
10.1084/jem.157.6.1736 / J. Exp. Med. / H-2D control of recovery from Friend virus leukemia: H-2D region influences the kinetics of the T lymphocyte response to Friend virus by Britt (1983)
10.4049/jimmunol.130.5.2363 / J. Immunol. / Use of monoclonal anti-gp70 antibodies to mimic the effects of the Rfv-3 gene in mice with Friend virus-induced leukemia by Britt (1983)
10.1084/jem.143.1.85 / J. Exp. Med. / Studies on the role of the host immune response in recovery from Friend virus leukemia. II. Cell-mediated immunity by Chesebro (1976)
10.1073/pnas.76.1.425 / Proc. Natl. Acad. Sci. USA / Identification of a non-H-2 gene (Rfv-3) influencing recovery from viremia and leukemia induced by Friend virus complex by Chesebro (1979)
10.1146/annurev.iy.08.040190.002401 / Annu. Rev. Immunol. / Host genetic control of spontaneous and induced immunity to Friend murine retrovirus infection by Chesebro (1990)
10.1038/312548a0 / Nature / Therapy with monoclonal antibodies by elimination of T-cell subsets in vivo by Cobbold (1984)
10.1056/NEJM198603133141105 / N. Engl. J. Med. / Infections with herpes simplex viruses by Corey (1986)
10.1126/science.3490689 / Science / T-lymphocyte priming and protection against Friend leukemia by vaccinia-retrovirus env gene recombinant by Earl (1986)
10.1073/pnas.92.23.10492 / Proc. Natl. Acad. Sci. USA / Passive immunotherapy for retroviral disease: influence of major histocompatibility complex type and T-cell responsiveness by Hasenkrug (1995)
10.1128/JVI.70.1.368-372.1996 / J. Virol. / Differing T-cell requirements for recombinant retrovirus vaccines by Hasenkrug (1996)
10.1128/JVI.69.4.2617-2620.1995 / J. Virol. / Chromosome mapping of Rfv3, a host resistance gene to Friend murine retrovirus by Hasenkrug (1995)
10.1073/pnas.94.15.7811 / Proc. Natl. Acad. Sci. USA / Immunity to retroviral infection: the Friend virus model by Hasenkrug (1997)
10.4049/jimmunol.146.11.3958 / J. Immunol. / Induction of protective immunity to Friend murine leukemia virus in genetic nonresponders to virus envelope protein by Ishihara (1991)
10.1006/viro.1997.8925 / Virology / Definition of an epitope on NS3 recognized by human CD4+ cytotoxic T lymphocyte clones cross-reactive for dengue virus types 2, 3, and 4 by Kurane (1998)
10.1128/JVI.68.12.8056-8063.1994 / J. Virol. / CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection by Matloubian (1994)
10.1084/jem.168.5.1587 / J. Exp. Med. / Genetic control of T cell responsiveness to the Friend murine leukemia virus envelope antigen. Identification of class II loci of the H-2 as immune response genes by Miyazawa (1988)
10.1038/329729a0 / Nature / Different H-2 subregions influence immunization against retrovirus and immunosuppression by Morrison (1987)
10.1084/jem.163.2.301 / J. Exp. Med. / Influence of the murine MHC (H-2) on Friend leukemia virus-induced immunosuppression by Morrison (1986)
{'key': 'B22_20200408120307', 'first-page': '1', 'article-title': 'The role of cytotoxic T lymphocytes in infectious disease: history, criteria, and state of the art', 'volume': '189', 'author': 'Oldstone', 'year': '1994', 'journal-title': 'Curr. Top. Microbiol. Immunol.'} / Curr. Top. Microbiol. Immunol. / The role of cytotoxic T lymphocytes in infectious disease: history, criteria, and state of the art by Oldstone (1994)
10.1128/JVI.68.8.4921-4926.1994 / J. Virol. / Contrasting effects from a single major histocompatibility complex class II molecule (H-2E) in recovery from Friend virus leukemia by Perry (1994)
10.1016/0161-5890(92)90118-H / Mol. Immunol. / Variable regions of antibodies to synthetic polypeptides. III. Antibodies arising in response to administration of anti-idiotope by Pincus (1992)
10.1073/pnas.94.13.6874 / Proc. Natl. Acad. Sci. USA / A critical role for neutralizing-antibody-producing B cells, CD4+ T cells and interferons in persistent and acute infections of mice with lymphocytic choriomeningitis virus: implications for adoptive immunotherapy of virus carriers by Planz (1997)
10.1128/JVI.66.6.3271-3277.1992 / J. Virol. / Role and specificity of T-cell subsets in spontaneous recovery from Friend virus-induced leukemia in mice by Robertson (1992)
10.1126/science.278.5342.1447 / Science / Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia by Rosenberg (1997)
10.1128/JVI.70.2.1072-1079.1996 / J. Virol. / CD4-deficient mice have reduced levels of memory cytotoxic T lymphocytes after immunization and show diminished resistance to subsequent virus challenge by von Herrath (1996)
{'key': 'B29_20200408120307', 'first-page': '271', 'article-title': 'Immune responses to viruses', 'volume-title': 'Clinical virology.', 'author': 'Yewdell', 'year': '1997'} / Clinical virology. / Immune responses to viruses by Yewdell (1997)

Dates

Type	When
Created	5 years, 7 months ago (Dec. 31, 2019, 1:04 p.m.)
Deposited	1 year, 11 months ago (Sept. 24, 2023, 11:03 a.m.)
Indexed	4 months, 3 weeks ago (March 30, 2025, 2:47 a.m.)
Issued	26 years, 9 months ago (Nov. 1, 1998)
Published	26 years, 9 months ago (Nov. 1, 1998)
Published Print	26 years, 9 months ago (Nov. 1, 1998)

Funders 0

None

BibTeX

@article{Super_1998, title={Requirement for CD4+ T Cells in the Friend Murine Retrovirus Neutralizing Antibody Response: Evidence for Functional T Cells in Genetic Low-Recovery Mice}, volume={72}, ISSN={0022-538X}, url={http://dx.doi.org/10.1128/jvi.72.11.9400-9403.1998}, DOI={10.1128/jvi.72.11.9400-9403.1998}, number={11}, journal={Journal of Virology}, publisher={American Society for Microbiology}, author={Super, Heidi J. and Brooks, Diane and Hasenkrug, Kim and Chesebro, Bruce}, year={1998}, month=nov, pages={9400–9403} }

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      "author": "Chesebro",
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