Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination
Iana H. Haralambieva, Richard B. Kennedy, Whitney L. Simon, Krista M. Goergen, Diane E. Grill, Inna G. Ovsyannikova, Gregory A. Poland
Background MicroRNAs are important mediators of post-transcriptional regulation of gene expression through RNA degradation and translational repression, and are emerging biomarkers of immune system activation/response after vaccination. Methods We performed Next Generation Sequencing (mRNA-Seq) of intracellular miRNAs in measles virus-stimulated B and CD4+ T cells from high and low antibody responders to measles vaccine. Negative binomial generalized estimating equation (GEE) models were used for miRNA assessment and the DIANA tool was used for gene/target prediction and pathway enrichment analysis. Results We identified a set of B cell-specific miRNAs (e.g., miR-151a-5p, miR-223, miR-29, miR-15a-5p, miR-199a-3p, miR-103a, and miR-15a/16 cluster) and biological processes/pathways, including regulation of adherens junction proteins, Fc-receptor signaling pathway, phosphatidylinositol-mediated signaling pathway, growth factor signaling pathway/pathways, transcriptional regulation, apoptosis and virus-related processes, significantly associated with neutralizing antibody titers after measles vaccination. No CD4+ T cell-specific miRNA expression differences between high and low antibody responders were found. Conclusion Our study demonstrates that miRNA expression directly or indirectly influences humoral immunity to measles vaccination and suggests that B cell-specific miRNAs may serve as useful predictive biomarkers of vaccine humoral immune response.
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measles Agriculture & Biology 100%
MicroRNA Chemical Compounds 86%
Measles Medicine & Life Sciences 80%
humoral immunity Agriculture & Biology 76%
Humoral Immunity Medicine & Life Sciences 72%
microRNA Agriculture & Biology 71%
B-lymphocytes Agriculture & Biology 69%
vaccination Agriculture & Biology 63%
Haralambieva, I. H., Kennedy, R. B., Simon, W. L., Goergen, K. M., Grill, D. E., Ovsyannikova, I. G., & Poland, G. A. (2018). Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination. PloS one, 13(1), [e0191812]. https://doi.org/10.1371/journal.pone.0191812
Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination. / Haralambieva, Iana H.; Kennedy, Richard B.; Simon, Whitney L.; Goergen, Krista M.; Grill, Diane E.; Ovsyannikova, Inna G.; Poland, Gregory A.
Haralambieva, IH, Kennedy, RB, Simon, WL, Goergen, KM, Grill, DE, Ovsyannikova, IG & Poland, GA 2018, 'Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination', PloS one, vol. 13, no. 1, e0191812. https://doi.org/10.1371/journal.pone.0191812
Haralambieva IH, Kennedy RB, Simon WL, Goergen KM, Grill DE, Ovsyannikova IG et al. Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination. PloS one. 2018 Jan;13(1). e0191812. https://doi.org/10.1371/journal.pone.0191812
Haralambieva, Iana H. ; Kennedy, Richard B. ; Simon, Whitney L. ; Goergen, Krista M. ; Grill, Diane E. ; Ovsyannikova, Inna G. ; Poland, Gregory A. / Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination. In: PloS one. 2018 ; Vol. 13, No. 1.
@article{aa024e68fb4148e9a37acb92d3398d78,
title = "Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination",
abstract = "Background MicroRNAs are important mediators of post-transcriptional regulation of gene expression through RNA degradation and translational repression, and are emerging biomarkers of immune system activation/response after vaccination. Methods We performed Next Generation Sequencing (mRNA-Seq) of intracellular miRNAs in measles virus-stimulated B and CD4+ T cells from high and low antibody responders to measles vaccine. Negative binomial generalized estimating equation (GEE) models were used for miRNA assessment and the DIANA tool was used for gene/target prediction and pathway enrichment analysis. Results We identified a set of B cell-specific miRNAs (e.g., miR-151a-5p, miR-223, miR-29, miR-15a-5p, miR-199a-3p, miR-103a, and miR-15a/16 cluster) and biological processes/pathways, including regulation of adherens junction proteins, Fc-receptor signaling pathway, phosphatidylinositol-mediated signaling pathway, growth factor signaling pathway/pathways, transcriptional regulation, apoptosis and virus-related processes, significantly associated with neutralizing antibody titers after measles vaccination. No CD4+ T cell-specific miRNA expression differences between high and low antibody responders were found. Conclusion Our study demonstrates that miRNA expression directly or indirectly influences humoral immunity to measles vaccination and suggests that B cell-specific miRNAs may serve as useful predictive biomarkers of vaccine humoral immune response.",
author = "Haralambieva, {Iana H.} and Kennedy, {Richard B.} and Simon, {Whitney L.} and Goergen, {Krista M.} and Grill, {Diane E.} and Ovsyannikova, {Inna G.} and Poland, {Gregory A.}",
note = "Funding Information: Research reported in this publication was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health under Award Number R01AI033144. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank the Mayo Clinic Vaccine Research Group staff and the study participants. We thank Caroline L. Vitse for her editorial assistance with this manuscript. Publisher Copyright: {\textcopyright} 2018 Haralambieva et al. 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.",
T1 - Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination
AU - Haralambieva, Iana H.
AU - Kennedy, Richard B.
AU - Simon, Whitney L.
AU - Goergen, Krista M.
AU - Grill, Diane E.
AU - Ovsyannikova, Inna G.
AU - Poland, Gregory A.
N1 - Funding Information: Research reported in this publication was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health under Award Number R01AI033144. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank the Mayo Clinic Vaccine Research Group staff and the study participants. We thank Caroline L. Vitse for her editorial assistance with this manuscript. Publisher Copyright: © 2018 Haralambieva et al. 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.
N2 - Background MicroRNAs are important mediators of post-transcriptional regulation of gene expression through RNA degradation and translational repression, and are emerging biomarkers of immune system activation/response after vaccination. Methods We performed Next Generation Sequencing (mRNA-Seq) of intracellular miRNAs in measles virus-stimulated B and CD4+ T cells from high and low antibody responders to measles vaccine. Negative binomial generalized estimating equation (GEE) models were used for miRNA assessment and the DIANA tool was used for gene/target prediction and pathway enrichment analysis. Results We identified a set of B cell-specific miRNAs (e.g., miR-151a-5p, miR-223, miR-29, miR-15a-5p, miR-199a-3p, miR-103a, and miR-15a/16 cluster) and biological processes/pathways, including regulation of adherens junction proteins, Fc-receptor signaling pathway, phosphatidylinositol-mediated signaling pathway, growth factor signaling pathway/pathways, transcriptional regulation, apoptosis and virus-related processes, significantly associated with neutralizing antibody titers after measles vaccination. No CD4+ T cell-specific miRNA expression differences between high and low antibody responders were found. Conclusion Our study demonstrates that miRNA expression directly or indirectly influences humoral immunity to measles vaccination and suggests that B cell-specific miRNAs may serve as useful predictive biomarkers of vaccine humoral immune response.
AB - Background MicroRNAs are important mediators of post-transcriptional regulation of gene expression through RNA degradation and translational repression, and are emerging biomarkers of immune system activation/response after vaccination. Methods We performed Next Generation Sequencing (mRNA-Seq) of intracellular miRNAs in measles virus-stimulated B and CD4+ T cells from high and low antibody responders to measles vaccine. Negative binomial generalized estimating equation (GEE) models were used for miRNA assessment and the DIANA tool was used for gene/target prediction and pathway enrichment analysis. Results We identified a set of B cell-specific miRNAs (e.g., miR-151a-5p, miR-223, miR-29, miR-15a-5p, miR-199a-3p, miR-103a, and miR-15a/16 cluster) and biological processes/pathways, including regulation of adherens junction proteins, Fc-receptor signaling pathway, phosphatidylinositol-mediated signaling pathway, growth factor signaling pathway/pathways, transcriptional regulation, apoptosis and virus-related processes, significantly associated with neutralizing antibody titers after measles vaccination. No CD4+ T cell-specific miRNA expression differences between high and low antibody responders were found. Conclusion Our study demonstrates that miRNA expression directly or indirectly influences humoral immunity to measles vaccination and suggests that B cell-specific miRNAs may serve as useful predictive biomarkers of vaccine humoral immune response.