Complex sex-biased antibody responses: estrogen receptors bind estrogen response elements centered within immunoglobulin heavy chain gene enhancers

Nuclear hormones influence antibody production quantitatively and qualitatively Abstract Nuclear hormone receptors including the estrogen receptor (ERα) and the retinoic acid receptor regulate a plethora of biological functions including reproduction, circulation and immunity. To understand how estr...

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Published inInternational immunology Vol. 31; no. 3; pp. 141 - 156
Main Authors Jones, Bart G, Sealy, Robert E, Penkert, Rhiannon R, Surman, Sherri L, Maul, Robert W, Neale, Geoff, Xu, Beisi, Gearhart, Patricia J, Hurwitz, Julia L
Format Journal Article
LanguageEnglish
Published UK Oxford University Press 05.03.2019
Subjects
Animals
Antibody Formation - genetics
Antibody Formation - immunology
Binding Sites
Enhancer Elements, Genetic
Immunoglobulin Heavy Chains - genetics
Immunoglobulin Heavy Chains - immunology
Mice
Mice, Inbred BALB C
Mice, Inbred C3H
Mice, Inbred C57BL
Original Research
Receptors, Estrogen - metabolism
Response Elements - genetics
Response Elements - immunology
Sex Characteristics
vaccine
female
ligand
male
nuclear hormone receptor
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Abstract Nuclear hormones influence antibody production quantitatively and qualitatively Abstract Nuclear hormone receptors including the estrogen receptor (ERα) and the retinoic acid receptor regulate a plethora of biological functions including reproduction, circulation and immunity. To understand how estrogen and other nuclear hormones influence antibody production, we characterized total serum antibody isotypes in female and male mice of C57BL/6J, BALB/cJ and C3H/HeJ mouse strains. Antibody levels were higher in females compared to males in all strains and there was a female preference for IgG2b production. Sex-biased patterns were influenced by vitamin levels, and by antigen specificity toward influenza virus or pneumococcus antigens. To help explain sex biases, we examined the direct effects of estrogen on immunoglobulin heavy chain sterile transcript production among purified, lipopolysaccharide-stimulated B cells. Supplemental estrogen in B-cell cultures significantly increased immunoglobulin heavy chain sterile transcripts. Chromatin immunoprecipitation analyses of activated B cells identified significant ERα binding to estrogen response elements (EREs) centered within enhancer elements of the immunoglobulin heavy chain locus, including the Eµ enhancer and hypersensitive site 1,2 (HS1,2) in the 3′ regulatory region. The ERE in HS1,2 was conserved across animal species, and in humans marked a site of polymorphism associated with the estrogen-augmented autoimmune disease, lupus. Taken together, the results highlight: (i) the important targets of ERα in regulatory regions of the immunoglobulin heavy chain locus that influence antibody production, and (ii) the complexity of mechanisms by which estrogen instructs sex-biased antibody production profiles.
AbstractList Nuclear hormone receptors including the estrogen receptor (ERα) and the retinoic acid receptor regulate a plethora of biological functions including reproduction, circulation and immunity. To understand how estrogen and other nuclear hormones influence antibody production, we characterized total serum antibody isotypes in female and male mice of C57BL/6J, BALB/cJ and C3H/HeJ mouse strains. Antibody levels were higher in females compared to males in all strains and there was a female preference for IgG2b production. Sex-biased patterns were influenced by vitamin levels, and by antigen specificity toward influenza virus or pneumococcus antigens. To help explain sex biases, we examined the direct effects of estrogen on immunoglobulin heavy chain sterile transcript production among purified, lipopolysaccharide-stimulated B cells. Supplemental estrogen in B-cell cultures significantly increased immunoglobulin heavy chain sterile transcripts. Chromatin immunoprecipitation analyses of activated B cells identified significant ERα binding to estrogen response elements (EREs) centered within enhancer elements of the immunoglobulin heavy chain locus, including the Eµ enhancer and hypersensitive site 1,2 (HS1,2) in the 3' regulatory region. The ERE in HS1,2 was conserved across animal species, and in humans marked a site of polymorphism associated with the estrogen-augmented autoimmune disease, lupus. Taken together, the results highlight: (i) the important targets of ERα in regulatory regions of the immunoglobulin heavy chain locus that influence antibody production, and (ii) the complexity of mechanisms by which estrogen instructs sex-biased antibody production profiles.
Nuclear hormones influence antibody production quantitatively and qualitatively Nuclear hormone receptors including the estrogen receptor (ERα) and the retinoic acid receptor regulate a plethora of biological functions including reproduction, circulation and immunity. To understand how estrogen and other nuclear hormones influence antibody production, we characterized total serum antibody isotypes in female and male mice of C57BL/6J, BALB/cJ and C3H/HeJ mouse strains. Antibody levels were higher in females compared to males in all strains and there was a female preference for IgG2b production. Sex-biased patterns were influenced by vitamin levels, and by antigen specificity toward influenza virus or pneumococcus antigens. To help explain sex biases, we examined the direct effects of estrogen on immunoglobulin heavy chain sterile transcript production among purified, lipopolysaccharide-stimulated B cells. Supplemental estrogen in B-cell cultures significantly increased immunoglobulin heavy chain sterile transcripts. Chromatin immunoprecipitation analyses of activated B cells identified significant ERα binding to estrogen response elements (EREs) centered within enhancer elements of the immunoglobulin heavy chain locus, including the Eµ enhancer and hypersensitive site 1,2 (HS1,2) in the 3′ regulatory region. The ERE in HS1,2 was conserved across animal species, and in humans marked a site of polymorphism associated with the estrogen-augmented autoimmune disease, lupus. Taken together, the results highlight: (i) the important targets of ERα in regulatory regions of the immunoglobulin heavy chain locus that influence antibody production, and (ii) the complexity of mechanisms by which estrogen instructs sex-biased antibody production profiles.
Nuclear hormones influence antibody production quantitatively and qualitatively Abstract Nuclear hormone receptors including the estrogen receptor (ERα) and the retinoic acid receptor regulate a plethora of biological functions including reproduction, circulation and immunity. To understand how estrogen and other nuclear hormones influence antibody production, we characterized total serum antibody isotypes in female and male mice of C57BL/6J, BALB/cJ and C3H/HeJ mouse strains. Antibody levels were higher in females compared to males in all strains and there was a female preference for IgG2b production. Sex-biased patterns were influenced by vitamin levels, and by antigen specificity toward influenza virus or pneumococcus antigens. To help explain sex biases, we examined the direct effects of estrogen on immunoglobulin heavy chain sterile transcript production among purified, lipopolysaccharide-stimulated B cells. Supplemental estrogen in B-cell cultures significantly increased immunoglobulin heavy chain sterile transcripts. Chromatin immunoprecipitation analyses of activated B cells identified significant ERα binding to estrogen response elements (EREs) centered within enhancer elements of the immunoglobulin heavy chain locus, including the Eµ enhancer and hypersensitive site 1,2 (HS1,2) in the 3′ regulatory region. The ERE in HS1,2 was conserved across animal species, and in humans marked a site of polymorphism associated with the estrogen-augmented autoimmune disease, lupus. Taken together, the results highlight: (i) the important targets of ERα in regulatory regions of the immunoglobulin heavy chain locus that influence antibody production, and (ii) the complexity of mechanisms by which estrogen instructs sex-biased antibody production profiles.
Abstract Nuclear hormone receptors including the estrogen receptor (ERα) and the retinoic acid receptor regulate a plethora of biological functions including reproduction, circulation and immunity. To understand how estrogen and other nuclear hormones influence antibody production, we characterized total serum antibody isotypes in female and male mice of C57BL/6J, BALB/cJ and C3H/HeJ mouse strains. Antibody levels were higher in females compared to males in all strains and there was a female preference for IgG2b production. Sex-biased patterns were influenced by vitamin levels, and by antigen specificity toward influenza virus or pneumococcus antigens. To help explain sex biases, we examined the direct effects of estrogen on immunoglobulin heavy chain sterile transcript production among purified, lipopolysaccharide-stimulated B cells. Supplemental estrogen in B-cell cultures significantly increased immunoglobulin heavy chain sterile transcripts. Chromatin immunoprecipitation analyses of activated B cells identified significant ERα binding to estrogen response elements (EREs) centered within enhancer elements of the immunoglobulin heavy chain locus, including the Eµ enhancer and hypersensitive site 1,2 (HS1,2) in the 3′ regulatory region. The ERE in HS1,2 was conserved across animal species, and in humans marked a site of polymorphism associated with the estrogen-augmented autoimmune disease, lupus. Taken together, the results highlight: (i) the important targets of ERα in regulatory regions of the immunoglobulin heavy chain locus that influence antibody production, and (ii) the complexity of mechanisms by which estrogen instructs sex-biased antibody production profiles.
Author Maul, Robert W
Sealy, Robert E
Surman, Sherri L
Neale, Geoff
Hurwitz, Julia L
Xu, Beisi
Gearhart, Patricia J
Jones, Bart G
Penkert, Rhiannon R
AuthorAffiliation 2 Laboratory of Molecular Biology and Immunology, National Institute on Aging, National Institutes of Health, Baltimore, MD, USA
3 Hartwell Center for Bioinformatics & Biotechnology, St. Jude Children’s Research Hospital, Memphis, USA
5 Department of Microbiology, Immunology and Biochemistry, University of Tennessee Health Science Center, Memphis, USA
1 Department of Infectious Diseases, St. Jude Children’s Research Hospital, Danny Thomas Place, Memphis, USA
4 Computational Biology, St. Jude Children’s Research Hospital, Memphis, USA
AuthorAffiliation_xml – name: 3 Hartwell Center for Bioinformatics & Biotechnology, St. Jude Children’s Research Hospital, Memphis, USA
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  fullname: Penkert, Rhiannon R
  organization: Department of Infectious Diseases, St. Jude Children’s Research Hospital, Danny Thomas Place, Memphis, USA
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  fullname: Neale, Geoff
  organization: Hartwell Center for Bioinformatics & Biotechnology, St. Jude Children’s Research Hospital, Memphis, USA
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  surname: Xu
  fullname: Xu, Beisi
  organization: Computational Biology, St. Jude Children’s Research Hospital, Memphis, USA
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  surname: Gearhart
  fullname: Gearhart, Patricia J
  organization: Laboratory of Molecular Biology and Immunology, National Institute on Aging, National Institutes of Health, Baltimore, MD, USA
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  surname: Hurwitz
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  email: julia.hurwitz@stjude.org
  organization: Department of Infectious Diseases, St. Jude Children’s Research Hospital, Danny Thomas Place, Memphis, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30407507$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright The Japanese Society for Immunology. 2018. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2018
The Japanese Society for Immunology. 2018. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
The Author(s) 2018. Published by Oxford University Press on behalf of The Japanese Society for Immunology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2018
Copyright_xml – notice: The Japanese Society for Immunology. 2018. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2018
– notice: The Japanese Society for Immunology. 2018. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
– notice: The Author(s) 2018. Published by Oxford University Press on behalf of The Japanese Society for Immunology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2018
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Issue 3
Keywords vaccine
female
ligand
male
nuclear hormone receptor
Language English
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PublicationTitle International immunology
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Snippet Nuclear hormones influence antibody production quantitatively and qualitatively Abstract Nuclear hormone receptors including the estrogen receptor (ERα) and...
Nuclear hormone receptors including the estrogen receptor (ERα) and the retinoic acid receptor regulate a plethora of biological functions including...
Abstract Nuclear hormone receptors including the estrogen receptor (ERα) and the retinoic acid receptor regulate a plethora of biological functions including...
Nuclear hormones influence antibody production quantitatively and qualitatively Nuclear hormone receptors including the estrogen receptor (ERα) and the...
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SubjectTerms Animals
Antibody Formation - genetics
Antibody Formation - immunology
Binding Sites
Enhancer Elements, Genetic
Immunoglobulin Heavy Chains - genetics
Immunoglobulin Heavy Chains - immunology
Mice
Mice, Inbred BALB C
Mice, Inbred C3H
Mice, Inbred C57BL
Original Research
Receptors, Estrogen - metabolism
Response Elements - genetics
Response Elements - immunology
Sex Characteristics
Title Complex sex-biased antibody responses: estrogen receptors bind estrogen response elements centered within immunoglobulin heavy chain gene enhancers
URI https://www.ncbi.nlm.nih.gov/pubmed/30407507
https://search.proquest.com/docview/2131238711
https://pubmed.ncbi.nlm.nih.gov/PMC6400052
Volume 31
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