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Multicenter Systems Analysis of Human Blood Reveals Immature Neutrophils in Males and During Pregnancy

Jana Blazkova, Sarthak Gupta, Yudong Liu, Brice Gaudilliere, Edward A. Ganio, Christopher R. Bolen, Ron Saar-Dover, Gabriela K. Fragiadakis, Martin S. Angst, Sarfaraz Hasni, Nima Aghaeepour, David Stevenson, Nicole Baldwin, Esperanza Anguiano, Damien Chaussabel, Matthew C. Altman, Mariana J. Kaplan, Mark M. Davis and David Furman
J Immunol February 8, 2017, 1601855; DOI: https://doi.org/10.4049/jimmunol.1601855
Jana Blazkova
*Division of Translational Medicine, Department of Systems Biology, Sidra Medical and Research Center, 26999 Doha, Qatar;
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Sarthak Gupta
†Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD 20892;
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Yudong Liu
†Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD 20892;
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Brice Gaudilliere
‡Department of Anesthesiology, Perioperative and Pain Medicine, Stanford University School of Medicine, Stanford, CA 94305;
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  • ORCID record for Brice Gaudilliere
Edward A. Ganio
‡Department of Anesthesiology, Perioperative and Pain Medicine, Stanford University School of Medicine, Stanford, CA 94305;
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Christopher R. Bolen
§Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305;
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Ron Saar-Dover
§Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305;
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Gabriela K. Fragiadakis
§Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305;
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Martin S. Angst
‡Department of Anesthesiology, Perioperative and Pain Medicine, Stanford University School of Medicine, Stanford, CA 94305;
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Sarfaraz Hasni
†Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD 20892;
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Nima Aghaeepour
‡Department of Anesthesiology, Perioperative and Pain Medicine, Stanford University School of Medicine, Stanford, CA 94305;
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David Stevenson
¶Department of Pediatrics, Stanford University School of Medicine, Stanford, CA 94305;
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Nicole Baldwin
‖Baylor Scott and White Health, Dallas, TX 75246;
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Esperanza Anguiano
#The Jackson Laboratory for Genomic Medicine, Farmington, CT 06032;
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Damien Chaussabel
*Division of Translational Medicine, Department of Systems Biology, Sidra Medical and Research Center, 26999 Doha, Qatar;
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Matthew C. Altman
**Benaroya Research Institute at Virginia Mason, Seattle, WA 98101;
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Mariana J. Kaplan
†Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD 20892;
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Mark M. Davis
§Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305;
††Institute for Immunity, Transplantation of Infection, Stanford University School of Medicine, Stanford, CA 94305; and
‡‡Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA 94305
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David Furman
*Division of Translational Medicine, Department of Systems Biology, Sidra Medical and Research Center, 26999 Doha, Qatar;
§Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305;
††Institute for Immunity, Transplantation of Infection, Stanford University School of Medicine, Stanford, CA 94305; and
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Abstract

Despite clear differences in immune system responses and in the prevalence of autoimmune diseases between males and females, there is little understanding of the processes involved. In this study, we identified a gene signature of immature-like neutrophils, characterized by the overexpression of genes encoding for several granule-containing proteins, which was found at higher levels (up to 3-fold) in young (20–30 y old) but not older (60 to >89 y old) males compared with females. Functional and phenotypic characterization of peripheral blood neutrophils revealed more mature and responsive neutrophils in young females, which also exhibited an elevated capacity in neutrophil extracellular trap formation at baseline and upon microbial or sterile autoimmune stimuli. The expression levels of the immature-like neutrophil signature increased linearly with pregnancy, an immune state of increased susceptibility to certain infections. Using mass cytometry, we also find increased frequencies of immature forms of neutrophils in the blood of women during late pregnancy. Thus, our findings show novel sex differences in innate immunity and identify a common neutrophil signature in males and in pregnant women.

Footnotes

  • This work was supported by the Intramural Research Program at the National Institute of Arthritis and Musculoskeletal and Skin Diseases/National Institutes of Health (Project ZIA AR041199 to M.J.K.), the Ellison Foundation, National Institutes of Health Grant U19 AI090019 (both to M.M.D.), the Discovery Foundation (for the Baylor study), and intramural funds from the Sidra Medical and Research Center (to D.F.).

  • The online version of this article contains supplemental material.

  • Received November 4, 2016.
  • Accepted January 11, 2017.
  • Copyright © 2017 by The American Association of Immunologists, Inc.

This article is distributed under The American Association of Immunologists, Inc., Reuse Terms and Conditions for Author Choice articles.

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The Journal of Immunology: 209 (1)
The Journal of Immunology
Vol. 209, Issue 1
1 Jul 2022
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Multicenter Systems Analysis of Human Blood Reveals Immature Neutrophils in Males and During Pregnancy
Jana Blazkova, Sarthak Gupta, Yudong Liu, Brice Gaudilliere, Edward A. Ganio, Christopher R. Bolen, Ron Saar-Dover, Gabriela K. Fragiadakis, Martin S. Angst, Sarfaraz Hasni, Nima Aghaeepour, David Stevenson, Nicole Baldwin, Esperanza Anguiano, Damien Chaussabel, Matthew C. Altman, Mariana J. Kaplan, Mark M. Davis, David Furman
The Journal of Immunology February 8, 2017, 1601855; DOI: 10.4049/jimmunol.1601855

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Multicenter Systems Analysis of Human Blood Reveals Immature Neutrophils in Males and During Pregnancy
Jana Blazkova, Sarthak Gupta, Yudong Liu, Brice Gaudilliere, Edward A. Ganio, Christopher R. Bolen, Ron Saar-Dover, Gabriela K. Fragiadakis, Martin S. Angst, Sarfaraz Hasni, Nima Aghaeepour, David Stevenson, Nicole Baldwin, Esperanza Anguiano, Damien Chaussabel, Matthew C. Altman, Mariana J. Kaplan, Mark M. Davis, David Furman
The Journal of Immunology February 8, 2017, 1601855; DOI: 10.4049/jimmunol.1601855
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