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Anti-HIV IgA isotypes: differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission

Although passive immunization with anti-HIV-1 Env IgG1 neutralizing monoclonal antibodies (nmAbs) prevented simian-human immunodeficiency virus (SHIV) infection in rhesus monkeys, IgA nmAbs have not been tested. Here, we sought to determine whether human anti-HIV-1 dimeric (d)IgA1, dIgA2, and IgG1 d... Full description

Journal Title: AIDS (London) 2013, Vol.27 (9), p.F13-F20
Main Author: WATKINS, Jennifer D
Other Authors: SHOLUKH, Anton M , VILLINGER, Francois , CORTI, Davide , RUPRECHT, Ruth M , MUKHTAR, Muhammad M , SIDDAPPA, Nagadenahalli B , LAKHASHE, Samir K , KIM, Mikyung , REINHERZ, Ellis L , GUPTA, Sandeep , FORTHAL, Donald N , SATTENTAU, Quentin J
Format: Electronic Article Electronic Article
Language: English
Subjects:
Publisher: Hagerstown, MD: Lippincott Williams & Wilkins
ID: ISSN: 0269-9370
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recordid: cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4084966
title: Anti-HIV IgA isotypes: differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission
format: Article
creator:
  • WATKINS, Jennifer D
  • SHOLUKH, Anton M
  • VILLINGER, Francois
  • CORTI, Davide
  • RUPRECHT, Ruth M
  • MUKHTAR, Muhammad M
  • SIDDAPPA, Nagadenahalli B
  • LAKHASHE, Samir K
  • KIM, Mikyung
  • REINHERZ, Ellis L
  • GUPTA, Sandeep
  • FORTHAL, Donald N
  • SATTENTAU, Quentin J
subjects:
  • Administration, Rectal
  • AIDS Vaccines - administration & dosage
  • AIDS Vaccines - immunology
  • Animals
  • Antibodies, Monoclonal - immunology
  • Antibodies, Neutralizing - immunology
  • Antiviral agents
  • Article
  • Biological and medical sciences
  • HIV Antibodies - immunology
  • HIV neutralization
  • HIV-1 - genetics
  • HIV-1 - immunology
  • Human immunodeficiency virus
  • Human viral diseases
  • Humans
  • Immunity, Mucosal - immunology
  • Immunization, Passive
  • Immunodeficiencies
  • Immunodeficiencies. Immunoglobulinopathies
  • Immunoglobulin A - immunology
  • immunoglobulin A isotypes
  • Immunopathology
  • Infectious diseases
  • Intestinal Mucosa - virology
  • Macaca mulatta
  • Medical sciences
  • mucosal transmission
  • Neutralization Tests
  • R5 SHIV
  • RNA, Viral - blood
  • Simian Acquired Immunodeficiency Syndrome - prevention & control
  • Simian Acquired Immunodeficiency Syndrome - transmission
  • Simian Immunodeficiency Virus - immunology
  • transcytosis
  • Transcytosis - drug effects
  • Transcytosis - physiology
  • Viral diseases
  • Viral diseases of the lymphoid tissue and the blood. Aids
  • Viral Load
  • Virion - immunology
  • virion capture
ispartof: AIDS (London), 2013, Vol.27 (9), p.F13-F20
description: Although passive immunization with anti-HIV-1 Env IgG1 neutralizing monoclonal antibodies (nmAbs) prevented simian-human immunodeficiency virus (SHIV) infection in rhesus monkeys, IgA nmAbs have not been tested. Here, we sought to determine whether human anti-HIV-1 dimeric (d)IgA1, dIgA2, and IgG1 differ in their ability to prevent mucosal R5 SHIV acquisition in rhesus monkeys. DIgA1, dIgA2, and IgG1 versions of nmAb HGN194 were applied intrarectally in three rhesus monkey groups 30 min before intrarectal SHIV challenge. After a control pharmacokinetic study confirmed that nmAb concentrations in rectal fluids over time were similar for all HGN194 isotypes, control and nmAb-treated animals were challenged intrarectally with an R5 SHIV, and viral loads were monitored. Unexpectedly, dIgA1 provided the best protection in vivo--although all nmAbs showed similar neutralizing activity in vitro. Five out of the six dIgA1-treated rhesus monkeys remained virus-free compared to only one out of six animals given dIgA2 (P=0.045 by log-rank test) and two out of six rhesus monkeys treated with IgG1 forms of the nmAb (P=0.12). Protection correlated significantly with virion capture activity by a given nmAb form, as well as inhibition of transcytosis of cell-free virus across an epithelial cell layer in vitro. Our data imply that dIgA1-mediated capturing of virions in mucosal secretions and inhibition of transcytosis can provide significant prevention of lentiviral acquisition--over and above direct virus neutralization. Vaccine strategies that induce mucosal IgA, especially IgA1, should be developed as a first line of defense against HIV-1, a virus predominantly transmitted mucosally.
language: eng
source:
identifier: ISSN: 0269-9370
fulltext: no_fulltext
issn:
  • 0269-9370
  • 1473-5571
url: Link


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titleAnti-HIV IgA isotypes: differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission
creatorWATKINS, Jennifer D ; SHOLUKH, Anton M ; VILLINGER, Francois ; CORTI, Davide ; RUPRECHT, Ruth M ; MUKHTAR, Muhammad M ; SIDDAPPA, Nagadenahalli B ; LAKHASHE, Samir K ; KIM, Mikyung ; REINHERZ, Ellis L ; GUPTA, Sandeep ; FORTHAL, Donald N ; SATTENTAU, Quentin J
creatorcontribWATKINS, Jennifer D ; SHOLUKH, Anton M ; VILLINGER, Francois ; CORTI, Davide ; RUPRECHT, Ruth M ; MUKHTAR, Muhammad M ; SIDDAPPA, Nagadenahalli B ; LAKHASHE, Samir K ; KIM, Mikyung ; REINHERZ, Ellis L ; GUPTA, Sandeep ; FORTHAL, Donald N ; SATTENTAU, Quentin J ; CAVD Project Group
descriptionAlthough passive immunization with anti-HIV-1 Env IgG1 neutralizing monoclonal antibodies (nmAbs) prevented simian-human immunodeficiency virus (SHIV) infection in rhesus monkeys, IgA nmAbs have not been tested. Here, we sought to determine whether human anti-HIV-1 dimeric (d)IgA1, dIgA2, and IgG1 differ in their ability to prevent mucosal R5 SHIV acquisition in rhesus monkeys. DIgA1, dIgA2, and IgG1 versions of nmAb HGN194 were applied intrarectally in three rhesus monkey groups 30 min before intrarectal SHIV challenge. After a control pharmacokinetic study confirmed that nmAb concentrations in rectal fluids over time were similar for all HGN194 isotypes, control and nmAb-treated animals were challenged intrarectally with an R5 SHIV, and viral loads were monitored. Unexpectedly, dIgA1 provided the best protection in vivo--although all nmAbs showed similar neutralizing activity in vitro. Five out of the six dIgA1-treated rhesus monkeys remained virus-free compared to only one out of six animals given dIgA2 (P=0.045 by log-rank test) and two out of six rhesus monkeys treated with IgG1 forms of the nmAb (P=0.12). Protection correlated significantly with virion capture activity by a given nmAb form, as well as inhibition of transcytosis of cell-free virus across an epithelial cell layer in vitro. Our data imply that dIgA1-mediated capturing of virions in mucosal secretions and inhibition of transcytosis can provide significant prevention of lentiviral acquisition--over and above direct virus neutralization. Vaccine strategies that induce mucosal IgA, especially IgA1, should be developed as a first line of defense against HIV-1, a virus predominantly transmitted mucosally.
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1EISSN: 1473-5571
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languageeng
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subjectAdministration, Rectal ; AIDS Vaccines - administration & dosage ; AIDS Vaccines - immunology ; Animals ; Antibodies, Monoclonal - immunology ; Antibodies, Neutralizing - immunology ; Antiviral agents ; Article ; Biological and medical sciences ; HIV Antibodies - immunology ; HIV neutralization ; HIV-1 - genetics ; HIV-1 - immunology ; Human immunodeficiency virus ; Human viral diseases ; Humans ; Immunity, Mucosal - immunology ; Immunization, Passive ; Immunodeficiencies ; Immunodeficiencies. Immunoglobulinopathies ; Immunoglobulin A - immunology ; immunoglobulin A isotypes ; Immunopathology ; Infectious diseases ; Intestinal Mucosa - virology ; Macaca mulatta ; Medical sciences ; mucosal transmission ; Neutralization Tests ; R5 SHIV ; RNA, Viral - blood ; Simian Acquired Immunodeficiency Syndrome - prevention & control ; Simian Acquired Immunodeficiency Syndrome - transmission ; Simian Immunodeficiency Virus - immunology ; transcytosis ; Transcytosis - drug effects ; Transcytosis - physiology ; Viral diseases ; Viral diseases of the lymphoid tissue and the blood. Aids ; Viral Load ; Virion - immunology ; virion capture
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0WATKINS, Jennifer D
1SHOLUKH, Anton M
2VILLINGER, Francois
3CORTI, Davide
4RUPRECHT, Ruth M
5MUKHTAR, Muhammad M
6SIDDAPPA, Nagadenahalli B
7LAKHASHE, Samir K
8KIM, Mikyung
9REINHERZ, Ellis L
10GUPTA, Sandeep
11FORTHAL, Donald N
12SATTENTAU, Quentin J
13CAVD Project Group
title
0Anti-HIV IgA isotypes: differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission
1AIDS (London)
addtitleAIDS
descriptionAlthough passive immunization with anti-HIV-1 Env IgG1 neutralizing monoclonal antibodies (nmAbs) prevented simian-human immunodeficiency virus (SHIV) infection in rhesus monkeys, IgA nmAbs have not been tested. Here, we sought to determine whether human anti-HIV-1 dimeric (d)IgA1, dIgA2, and IgG1 differ in their ability to prevent mucosal R5 SHIV acquisition in rhesus monkeys. DIgA1, dIgA2, and IgG1 versions of nmAb HGN194 were applied intrarectally in three rhesus monkey groups 30 min before intrarectal SHIV challenge. After a control pharmacokinetic study confirmed that nmAb concentrations in rectal fluids over time were similar for all HGN194 isotypes, control and nmAb-treated animals were challenged intrarectally with an R5 SHIV, and viral loads were monitored. Unexpectedly, dIgA1 provided the best protection in vivo--although all nmAbs showed similar neutralizing activity in vitro. Five out of the six dIgA1-treated rhesus monkeys remained virus-free compared to only one out of six animals given dIgA2 (P=0.045 by log-rank test) and two out of six rhesus monkeys treated with IgG1 forms of the nmAb (P=0.12). Protection correlated significantly with virion capture activity by a given nmAb form, as well as inhibition of transcytosis of cell-free virus across an epithelial cell layer in vitro. Our data imply that dIgA1-mediated capturing of virions in mucosal secretions and inhibition of transcytosis can provide significant prevention of lentiviral acquisition--over and above direct virus neutralization. Vaccine strategies that induce mucosal IgA, especially IgA1, should be developed as a first line of defense against HIV-1, a virus predominantly transmitted mucosally.
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0Administration, Rectal
1AIDS Vaccines - administration & dosage
2AIDS Vaccines - immunology
3Animals
4Antibodies, Monoclonal - immunology
5Antibodies, Neutralizing - immunology
6Antiviral agents
7Article
8Biological and medical sciences
9HIV Antibodies - immunology
10HIV neutralization
11HIV-1 - genetics
12HIV-1 - immunology
13Human immunodeficiency virus
14Human viral diseases
15Humans
16Immunity, Mucosal - immunology
17Immunization, Passive
18Immunodeficiencies
19Immunodeficiencies. Immunoglobulinopathies
20Immunoglobulin A - immunology
21immunoglobulin A isotypes
22Immunopathology
23Infectious diseases
24Intestinal Mucosa - virology
25Macaca mulatta
26Medical sciences
27mucosal transmission
28Neutralization Tests
29R5 SHIV
30RNA, Viral - blood
31Simian Acquired Immunodeficiency Syndrome - prevention & control
32Simian Acquired Immunodeficiency Syndrome - transmission
33Simian Immunodeficiency Virus - immunology
34transcytosis
35Transcytosis - drug effects
36Transcytosis - physiology
37Viral diseases
38Viral diseases of the lymphoid tissue and the blood. Aids
39Viral Load
40Virion - immunology
41virion capture
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1SHOLUKH, Anton M
2VILLINGER, Francois
3CORTI, Davide
4RUPRECHT, Ruth M
5MUKHTAR, Muhammad M
6SIDDAPPA, Nagadenahalli B
7LAKHASHE, Samir K
8KIM, Mikyung
9REINHERZ, Ellis L
10GUPTA, Sandeep
11FORTHAL, Donald N
12SATTENTAU, Quentin J
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titleAnti-HIV IgA isotypes: differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission
authorWATKINS, Jennifer D ; SHOLUKH, Anton M ; VILLINGER, Francois ; CORTI, Davide ; RUPRECHT, Ruth M ; MUKHTAR, Muhammad M ; SIDDAPPA, Nagadenahalli B ; LAKHASHE, Samir K ; KIM, Mikyung ; REINHERZ, Ellis L ; GUPTA, Sandeep ; FORTHAL, Donald N ; SATTENTAU, Quentin J
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0Administration, Rectal
1AIDS Vaccines - administration & dosage
2AIDS Vaccines - immunology
3Animals
4Antibodies, Monoclonal - immunology
5Antibodies, Neutralizing - immunology
6Antiviral agents
7Article
8Biological and medical sciences
9HIV Antibodies - immunology
10HIV neutralization
11HIV-1 - genetics
12HIV-1 - immunology
13Human immunodeficiency virus
14Human viral diseases
15Humans
16Immunity, Mucosal - immunology
17Immunization, Passive
18Immunodeficiencies
19Immunodeficiencies. Immunoglobulinopathies
20Immunoglobulin A - immunology
21immunoglobulin A isotypes
22Immunopathology
23Infectious diseases
24Intestinal Mucosa - virology
25Macaca mulatta
26Medical sciences
27mucosal transmission
28Neutralization Tests
29R5 SHIV
30RNA, Viral - blood
31Simian Acquired Immunodeficiency Syndrome - prevention & control
32Simian Acquired Immunodeficiency Syndrome - transmission
33Simian Immunodeficiency Virus - immunology
34transcytosis
35Transcytosis - drug effects
36Transcytosis - physiology
37Viral diseases
38Viral diseases of the lymphoid tissue and the blood. Aids
39Viral Load
40Virion - immunology
41virion capture
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0WATKINS, Jennifer D
1SHOLUKH, Anton M
2VILLINGER, Francois
3CORTI, Davide
4RUPRECHT, Ruth M
5MUKHTAR, Muhammad M
6SIDDAPPA, Nagadenahalli B
7LAKHASHE, Samir K
8KIM, Mikyung
9REINHERZ, Ellis L
10GUPTA, Sandeep
11FORTHAL, Donald N
12SATTENTAU, Quentin J
13CAVD Project Group
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0WATKINS, Jennifer D
1SHOLUKH, Anton M
2VILLINGER, Francois
3CORTI, Davide
4RUPRECHT, Ruth M
5MUKHTAR, Muhammad M
6SIDDAPPA, Nagadenahalli B
7LAKHASHE, Samir K
8KIM, Mikyung
9REINHERZ, Ellis L
10GUPTA, Sandeep
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atitleAnti-HIV IgA isotypes: differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission
jtitleAIDS (London)
addtitleAIDS
date2013
risdate2013
volume27
issue9
spageF13
epageF20
pagesF13-F20
issn0269-9370
eissn1473-5571
notes
0CAVD Project Group: Girish HEMASHETTARa, Vivekanandan SHANMUGANATHANa, Sandra LEEa, Barbara C. BACHLERa,h, Dieter KLEINh, Kenneth ROGERSe, Katie KINSEYe, Gloria AGATICg, Shiu-Lok HUi, Jonathan L. HEENEYj, Robin A. WEISSk, Antonio LANZAVECCHIAl.
1Current address: Department of Pathology and Laboratory Medicine, Emory University, Atlanta, GA 30329, USA.
abstractAlthough passive immunization with anti-HIV-1 Env IgG1 neutralizing monoclonal antibodies (nmAbs) prevented simian-human immunodeficiency virus (SHIV) infection in rhesus monkeys, IgA nmAbs have not been tested. Here, we sought to determine whether human anti-HIV-1 dimeric (d)IgA1, dIgA2, and IgG1 differ in their ability to prevent mucosal R5 SHIV acquisition in rhesus monkeys. DIgA1, dIgA2, and IgG1 versions of nmAb HGN194 were applied intrarectally in three rhesus monkey groups 30 min before intrarectal SHIV challenge. After a control pharmacokinetic study confirmed that nmAb concentrations in rectal fluids over time were similar for all HGN194 isotypes, control and nmAb-treated animals were challenged intrarectally with an R5 SHIV, and viral loads were monitored. Unexpectedly, dIgA1 provided the best protection in vivo--although all nmAbs showed similar neutralizing activity in vitro. Five out of the six dIgA1-treated rhesus monkeys remained virus-free compared to only one out of six animals given dIgA2 (P=0.045 by log-rank test) and two out of six rhesus monkeys treated with IgG1 forms of the nmAb (P=0.12). Protection correlated significantly with virion capture activity by a given nmAb form, as well as inhibition of transcytosis of cell-free virus across an epithelial cell layer in vitro. Our data imply that dIgA1-mediated capturing of virions in mucosal secretions and inhibition of transcytosis can provide significant prevention of lentiviral acquisition--over and above direct virus neutralization. Vaccine strategies that induce mucosal IgA, especially IgA1, should be developed as a first line of defense against HIV-1, a virus predominantly transmitted mucosally.
copHagerstown, MD
pubLippincott Williams & Wilkins
pmid23775002
doi10.1097/QAD.0b013e328360eac6
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