Interleukin-7 Facilitates HIV-1 Transmission to Cervico-Vaginal Tissue ex vivo

The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen is more than a mere carrier of HIV-1, since it contains many biological factors, in particular cytokines, that may affect HIV-1 transmission....

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Published inPLoS pathogens Vol. 9; no. 2; p. e1003148
Main Authors Introini, Andrea, Vanpouille, Christophe, Lisco, Andrea, Grivel, Jean-Charles, Margolis, Leonid
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.02.2013
Public Library of Science (PLoS)
Subjects
Acquired immune deficiency syndrome
AIDS
Apoptosis
Apoptosis Regulatory Proteins - metabolism
Biology
CD4-Positive T-Lymphocytes - cytology
CD4-Positive T-Lymphocytes - metabolism
CD4-Positive T-Lymphocytes - virology
Cell Proliferation
Cervix Uteri - virology
Colleges & universities
Disease transmission
Experiments
Female
Gene Expression Regulation, Viral
Health aspects
HIV
HIV infection
HIV Infections - transmission
HIV Infections - virology
HIV-1 - physiology
Human immunodeficiency virus
Humans
Interleukin-7 - metabolism
Interleukins
Ki-67 Antigen - metabolism
Lymphocytes
Lymphoid Tissue - virology
Lymphoma
Male
Medicine
Molecular Sequence Data
Palatine Tonsil - virology
Physiological aspects
Plasma
Proteins
Proto-Oncogene Proteins c-bcl-2 - metabolism
Recombinant Proteins
Sexual intercourse
Statistical analysis
Tissues
Vagina - virology
Virus Replication
Italy
HIV Infections
HIV-1
Cell Proliferation
Humans
Molecular Sequence Data
Vagina
Male
Recombinant Proteins
Cervix Uteri
Interleukin-7
Lymphoid Tissue
Palatine Tonsil
Apoptosis Regulatory Proteins
Virus Replication
Gene Expression Regulation, Viral
Ki-67 Antigen
Female
CD4-Positive T-Lymphocytes
Proto-Oncogene Proteins c-bcl-2
Apoptosis
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Abstract The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen is more than a mere carrier of HIV-1, since it contains many biological factors, in particular cytokines, that may affect HIV-1 transmission. The concentration of interleukin (IL)-7, one of the most prominent cytokines in semen of healthy individuals, is further increased in semen of HIV-1-infected men. Here, we investigated the potential role of IL-7 in HIV-1 vaginal transmission in an ex vivo system of human cervico-vaginal tissue. We simulated an in vivo situation by depositing HIV-1 on cervico-vaginal tissue in combination with IL-7 at concentrations comparable with those measured in semen of HIV-1-infected individuals. We found that IL-7 significantly enhanced virus replication in ex vivo infected cervico-vaginal tissue. Similarly, we observed an enhancement of HIV-1 replication in lymphoid tissue explants. Analysis of T cells isolated from infected tissues showed that IL-7 reduced CD4⁺ T cell depletion preventing apoptosis, as shown by the decrease in the number of cells expressing the apoptotic marker APO2.7 and the increase in the expression of the anti-apoptotic protein B-cell lymphoma (Bcl)-2. Also, IL-7 increased the fraction of cycling CD4⁺ T cells, as evidenced by staining for the nuclear factor Ki-67. High levels of seminal IL-7 in vivo may be relevant to the survival of the founder pool of HIV-1-infected cells in the cervico-vaginal mucosa at the initial stage of infection, promoting local expansion and dissemination of HIV infection.
AbstractList The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen is more than a mere carrier of HIV-1, since it contains many biological factors, in particular cytokines, that may affect HIV-1 transmission. The concentration of interleukin (IL)-7, one of the most prominent cytokines in semen of healthy individuals, is further increased in semen of HIV-1-infected men. Here, we investigated the potential role of IL-7 in HIV-1 vaginal transmission in an ex vivo system of human cervico-vaginal tissue. We simulated an in vivo situation by depositing HIV-1 on cervico-vaginal tissue in combination with IL-7 at concentrations comparable with those measured in semen of HIV-1-infected individuals. We found that IL-7 significantly enhanced virus replication in ex vivo infected cervico-vaginal tissue. Similarly, we observed an enhancement of HIV-1 replication in lymphoid tissue explants. Analysis of T cells isolated from infected tissues showed that IL-7 reduced CD4+ T cell depletion preventing apoptosis, as shown by the decrease in the number of cells expressing the apoptotic marker APO2.7 and the increase in the expression of the anti-apoptotic protein B-cell lymphoma (Bcl)-2. Also, IL-7 increased the fraction of cycling CD4+ T cells, as evidenced by staining for the nuclear factor Ki-67. High levels of seminal IL-7 in vivo may be relevant to the survival of the founder pool of HIV-1-infected cells in the cervico-vaginal mucosa at the initial stage of infection, promoting local expansion and dissemination of HIV infection.
The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen is more than a mere carrier of HIV-1, since it contains many biological factors, in particular cytokines, that may affect HIV-1 transmission. The concentration of interleukin (IL)-7, one of the most prominent cytokines in semen of healthy individuals, is further increased in semen of HIV-1-infected men. Here, we investigated the potential role of IL-7 in HIV-1 vaginal transmission in an ex vivo system of human cervico-vaginal tissue. We simulated an in vivo situation by depositing HIV-1 on cervico-vaginal tissue in combination with IL-7 at concentrations comparable with those measured in semen of HIV-1-infected individuals. We found that IL-7 significantly enhanced virus replication in ex vivo infected cervico-vaginal tissue. Similarly, we observed an enhancement of HIV-1 replication in lymphoid tissue explants. Analysis of T cells isolated from infected tissues showed that IL-7 reduced CD4⁺ T cell depletion preventing apoptosis, as shown by the decrease in the number of cells expressing the apoptotic marker APO2.7 and the increase in the expression of the anti-apoptotic protein B-cell lymphoma (Bcl)-2. Also, IL-7 increased the fraction of cycling CD4⁺ T cells, as evidenced by staining for the nuclear factor Ki-67. High levels of seminal IL-7 in vivo may be relevant to the survival of the founder pool of HIV-1-infected cells in the cervico-vaginal mucosa at the initial stage of infection, promoting local expansion and dissemination of HIV infection.
The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen is more than a mere carrier of HIV-1, since it contains many biological factors, in particular cytokines, that may affect HIV-1 transmission. The concentration of interleukin (IL)-7, one of the most prominent cytokines in semen of healthy individuals, is further increased in semen of HIV-1-infected men. Here, we investigated the potential role of IL-7 in HIV-1 vaginal transmission in an ex vivo system of human cervico-vaginal tissue. We simulated an in vivo situation by depositing HIV-1 on cervico-vaginal tissue in combination with IL-7 at concentrations comparable with those measured in semen of HIV-1-infected individuals. We found that IL-7 significantly enhanced virus replication in ex vivo infected cervico-vaginal tissue. Similarly, we observed an enhancement of HIV-1 replication in lymphoid tissue explants. Analysis of T cells isolated from infected tissues showed that IL-7 reduced [CD4.sup.+] T cell depletion preventing apoptosis, as shown by the decrease in the number of cells expressing the apoptotic marker APO2.7 and the increase in the expression of the anti-apoptotic protein B-cell lymphoma (Bcl)-2. Also, IL-7 increased the fraction of cycling [CD4.sup.+] T cells, as evidenced by staining for the nuclear factor Ki-67. High levels of seminal IL-7 in vivo may be relevant to the survival of the founder pool of HIV-1-infected cells in the cervico-vaginal mucosa at the initial stage of infection, promoting local expansion and dissemination of HIV infection.
  The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen is more than a mere carrier of HIV-1, since it contains many biological factors, in particular cytokines, that may affect HIV-1 transmission. The concentration of interleukin (IL)-7, one of the most prominent cytokines in semen of healthy individuals, is further increased in semen of HIV-1-infected men. Here, we investigated the potential role of IL-7 in HIV-1 vaginal transmission in an ex vivo system of human cervico-vaginal tissue. We simulated an in vivo situation by depositing HIV-1 on cervico-vaginal tissue in combination with IL-7 at concentrations comparable with those measured in semen of HIV-1-infected individuals. We found that IL-7 significantly enhanced virus replication in ex vivo infected cervico-vaginal tissue. Similarly, we observed an enhancement of HIV-1 replication in lymphoid tissue explants. Analysis of T cells isolated from infected tissues showed that IL-7 reduced CD4+ T cell depletion preventing apoptosis, as shown by the decrease in the number of cells expressing the apoptotic marker APO2.7 and the increase in the expression of the anti-apoptotic protein B-cell lymphoma (Bcl)-2. Also, IL-7 increased the fraction of cycling CD4+ T cells, as evidenced by staining for the nuclear factor Ki-67. High levels of seminal IL-7 in vivo may be relevant to the survival of the founder pool of HIV-1-infected cells in the cervico-vaginal mucosa at the initial stage of infection, promoting local expansion and dissemination of HIV infection.
The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen is more than a mere carrier of HIV-1, since it contains many biological factors, in particular cytokines, that may affect HIV-1 transmission. The concentration of interleukin (IL)-7, one of the most prominent cytokines in semen of healthy individuals, is further increased in semen of HIV-1-infected men. Here, we investigated the potential role of IL-7 in HIV-1 vaginal transmission in an ex vivo system of human cervico-vaginal tissue. We simulated an in vivo situation by depositing HIV-1 on cervico-vaginal tissue in combination with IL-7 at concentrations comparable with those measured in semen of HIV-1-infected individuals. We found that IL-7 significantly enhanced virus replication in ex vivo infected cervico-vaginal tissue. Similarly, we observed an enhancement of HIV-1 replication in lymphoid tissue explants. Analysis of T cells isolated from infected tissues showed that IL-7 reduced CD4⁺ T cell depletion preventing apoptosis, as shown by the decrease in the number of cells expressing the apoptotic marker APO2.7 and the increase in the expression of the anti-apoptotic protein B-cell lymphoma (Bcl)-2. Also, IL-7 increased the fraction of cycling CD4⁺ T cells, as evidenced by staining for the nuclear factor Ki-67. High levels of seminal IL-7 in vivo may be relevant to the survival of the founder pool of HIV-1-infected cells in the cervico-vaginal mucosa at the initial stage of infection, promoting local expansion and dissemination of HIV infection.The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen is more than a mere carrier of HIV-1, since it contains many biological factors, in particular cytokines, that may affect HIV-1 transmission. The concentration of interleukin (IL)-7, one of the most prominent cytokines in semen of healthy individuals, is further increased in semen of HIV-1-infected men. Here, we investigated the potential role of IL-7 in HIV-1 vaginal transmission in an ex vivo system of human cervico-vaginal tissue. We simulated an in vivo situation by depositing HIV-1 on cervico-vaginal tissue in combination with IL-7 at concentrations comparable with those measured in semen of HIV-1-infected individuals. We found that IL-7 significantly enhanced virus replication in ex vivo infected cervico-vaginal tissue. Similarly, we observed an enhancement of HIV-1 replication in lymphoid tissue explants. Analysis of T cells isolated from infected tissues showed that IL-7 reduced CD4⁺ T cell depletion preventing apoptosis, as shown by the decrease in the number of cells expressing the apoptotic marker APO2.7 and the increase in the expression of the anti-apoptotic protein B-cell lymphoma (Bcl)-2. Also, IL-7 increased the fraction of cycling CD4⁺ T cells, as evidenced by staining for the nuclear factor Ki-67. High levels of seminal IL-7 in vivo may be relevant to the survival of the founder pool of HIV-1-infected cells in the cervico-vaginal mucosa at the initial stage of infection, promoting local expansion and dissemination of HIV infection.
The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen is more than a mere carrier of HIV-1, since it contains many biological factors, in particular cytokines, that may affect HIV-1 transmission. The concentration of interleukin (IL)-7, one of the most prominent cytokines in semen of healthy individuals, is further increased in semen of HIV-1-infected men. Here, we investigated the potential role of IL-7 in HIV-1 vaginal transmission in an ex vivo system of human cervico-vaginal tissue. We simulated an in vivo situation by depositing HIV-1 on cervico-vaginal tissue in combination with IL-7 at concentrations comparable with those measured in semen of HIV-1-infected individuals. We found that IL-7 significantly enhanced virus replication in ex vivo infected cervico-vaginal tissue. Similarly, we observed an enhancement of HIV-1 replication in lymphoid tissue explants. Analysis of T cells isolated from infected tissues showed that IL-7 reduced CD4 + T cell depletion preventing apoptosis, as shown by the decrease in the number of cells expressing the apoptotic marker APO2.7 and the increase in the expression of the anti-apoptotic protein B-cell lymphoma (Bcl)-2. Also, IL-7 increased the fraction of cycling CD4 + T cells, as evidenced by staining for the nuclear factor Ki-67. High levels of seminal IL-7 in vivo may be relevant to the survival of the founder pool of HIV-1-infected cells in the cervico-vaginal mucosa at the initial stage of infection, promoting local expansion and dissemination of HIV infection. Male-to-female HIV-1 transmission occurs predominantly through vaginal intercourse when the virus is transmitted with seminal fluid. The identification of the determinants of HIV-1 transmission to the female lower genital tract is of pivotal importance for understanding the basic mechanisms of HIV-1 infection. This understanding is necessary for the development of new strategies to prevent or contain this infection. Semen of HIV-1-infected individuals is highly enriched with IL-7, a crucial cytokine for the life cycle of CD4 + T cells, the primary target of HIV-1. Here, we utilized a system of human cervico-vaginal and lymphoid tissues ex vivo to study the effect of IL-7 on HIV-1 transmission and dissemination. Our results show that IL-7 at concentrations comparable to those found in semen of HIV-1-infected individuals enhanced HIV-1 replication by preventing the death and by stimulating the proliferation of CD4 + T cells. This allows sustained viral production by infected cells and provides new cellular targets for propagation of infection. The concentration of IL-7 in semen of HIV-1-infected men may be a key determinant of the efficiency of HIV-1 transmission to an uninfected female partner through vaginal intercourse.
Audience Academic
Author Vanpouille, Christophe
Lisco, Andrea
Grivel, Jean-Charles
Margolis, Leonid
Introini, Andrea
AuthorAffiliation 2 Department of Biomedical Sciences and Technology, University of Milan, Milan, Italy
1 Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, United States of America
University of Pennsylvania School of Medicine, United States of America
AuthorAffiliation_xml – name: 1 Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, United States of America
– name: University of Pennsylvania School of Medicine, United States of America
– name: 2 Department of Biomedical Sciences and Technology, University of Milan, Milan, Italy
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/23408885$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
2013 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Citation: Introini A, Vanpouille C, Lisco A, Grivel J-C, Margolis L (2013) Interleukin-7 Facilitates HIV-1 Transmission to Cervico-Vaginal Tissue ex vivo. PLoS Pathog 9(2): e1003148. doi:10.1371/journal.ppat.1003148
2013
2013 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Citation: Introini A, Vanpouille C, Lisco A, Grivel J-C, Margolis L (2013) Interleukin-7 Facilitates HIV-1 Transmission to Cervico-Vaginal Tissue ex vivo. PLoS Pathog 9(2): e1003148. doi:10.1371/journal.ppat.1003148
Copyright_xml – notice: COPYRIGHT 2013 Public Library of Science
– notice: 2013 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Citation: Introini A, Vanpouille C, Lisco A, Grivel J-C, Margolis L (2013) Interleukin-7 Facilitates HIV-1 Transmission to Cervico-Vaginal Tissue ex vivo. PLoS Pathog 9(2): e1003148. doi:10.1371/journal.ppat.1003148
– notice: 2013
– notice: 2013 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Citation: Introini A, Vanpouille C, Lisco A, Grivel J-C, Margolis L (2013) Interleukin-7 Facilitates HIV-1 Transmission to Cervico-Vaginal Tissue ex vivo. PLoS Pathog 9(2): e1003148. doi:10.1371/journal.ppat.1003148
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DocumentTitleAlternate IL-7 Increases HIV-1 Transmission ex vivo
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Issue 2
Keywords HIV Infections
HIV-1
Cell Proliferation
Humans
Molecular Sequence Data
Vagina
Male
Recombinant Proteins
Cervix Uteri
Interleukin-7
Lymphoid Tissue
Palatine Tonsil
Apoptosis Regulatory Proteins
Virus Replication
Gene Expression Regulation, Viral
Ki-67 Antigen
Female
CD4-Positive T-Lymphocytes
Proto-Oncogene Proteins c-bcl-2
Apoptosis
Language English
License This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
Creative Commons Attribution License
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Notes ObjectType-Article-1
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content type line 14
content type line 23
Current address: University Hospitals, Case Western Reserve University, Cleveland, Ohio, United States of America.
Conceived and designed the experiments: AI CV AL JCG LM. Performed the experiments: AI CV. Analyzed the data: AI CV JCG LM. Wrote the paper: AI CV AL JCG LM.
The authors have declared that no competing interests exist.
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Snippet The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa. Semen...
  The majority of HIV-1 infections in women occur through vaginal intercourse, in which virus-containing semen is deposited on the cervico-vaginal mucosa....
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StartPage e1003148
SubjectTerms Acquired immune deficiency syndrome
AIDS
Apoptosis
Apoptosis Regulatory Proteins - metabolism
Biology
CD4-Positive T-Lymphocytes - cytology
CD4-Positive T-Lymphocytes - metabolism
CD4-Positive T-Lymphocytes - virology
Cell Proliferation
Cervix Uteri - virology
Colleges & universities
Disease transmission
Experiments
Female
Gene Expression Regulation, Viral
Health aspects
HIV
HIV infection
HIV Infections - transmission
HIV Infections - virology
HIV-1 - physiology
Human immunodeficiency virus
Humans
Interleukin-7 - metabolism
Interleukins
Ki-67 Antigen - metabolism
Lymphocytes
Lymphoid Tissue - virology
Lymphoma
Male
Medicine
Molecular Sequence Data
Palatine Tonsil - virology
Physiological aspects
Plasma
Proteins
Proto-Oncogene Proteins c-bcl-2 - metabolism
Recombinant Proteins
Sexual intercourse
Statistical analysis
Tissues
Vagina - virology
Virus Replication
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Title Interleukin-7 Facilitates HIV-1 Transmission to Cervico-Vaginal Tissue ex vivo
URI https://www.ncbi.nlm.nih.gov/pubmed/23408885
https://www.proquest.com/docview/1314344726
https://www.proquest.com/docview/1288312579
https://pubmed.ncbi.nlm.nih.gov/PMC3567179
https://doaj.org/article/34146f7e4a164209981dd24b345a2acb
http://dx.doi.org/10.1371/journal.ppat.1003148
Volume 9
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