Lower female survival from an opportunistic infection reveals progesterone-driven sex bias in trained immunity.

Burkholderia gladioli CP: Immunology glycolytic capacity innate immune memory oppotunistic infection progesterone progesterone receptor sex as a biological variable sex bias trained immunity

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
29 08 2023
Historique:
received: 19 01 2023
revised: 08 06 2023
accepted: 03 08 2023
medline: 4 9 2023
pubmed: 17 8 2023
entrez: 17 8 2023
Statut: ppublish

Résumé

Immune responses differ between females and males, although such sex-based variance is incompletely understood. Observing that bacteremia of the opportunistic pathogen Burkholderia gladioli caused many more deaths of female than male mice bearing genetic deficiencies in adaptive immunity, we determined that this was associated with sex bias in the innate immune memory response called trained immunity. Female attenuation of trained immunity varies with estrous cycle stage and correlates with serum progesterone, a hormone that decreases glycolytic capacity and recall cytokine secretion induced by antigen non-specific stimuli. Progesterone receptor antagonism rescues female trained immune responses and survival from controlled B. gladioli infection to magnitudes similar to those of males. These data demonstrate progesterone-dependent sex bias in trained immunity where attenuation of female responses is associated with survival outcomes from opportunistic infection.

Identifiants

pubmed: 37590139
pii: S2211-1247(23)01018-5
doi: 10.1016/j.celrep.2023.113007
pmc: PMC10528383
mid: NIHMS1928299
pii:
doi:

Substances chimiques

Progesterone 4G7DS2Q64Y

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

113007

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM103841
Pays : United States
Organisme : NCI NIH HHS
ID : R33 CA228979
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM008396
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA244314
Pays : United States

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

J Clin Microbiol. 1989 Feb;27(2):270-3
pubmed: 2915020
J Autoimmun. 2007 Feb;28(1):1-6
pubmed: 17261360
Science. 2014 Sep 26;345(6204):1250684
pubmed: 25258083
Cell Host Microbe. 2011 May 19;9(5):355-61
pubmed: 21575907
Nat Immunol. 2001 Sep;2(9):777-80
pubmed: 11526384
Gastroenterol Hepatol (N Y). 2019 Nov;15(11):593-605
pubmed: 31802985
Comp Med. 2004 Feb;54(1):93-9
pubmed: 15027624
J Mol Med (Berl). 2020 Jun;98(6):819-831
pubmed: 32350546
Mol Endocrinol. 1995 Nov;9(11):1441-54
pubmed: 8584021
Curr Pediatr Rev. 2019;15(4):197-206
pubmed: 31242834
Cell Host Microbe. 2012 Aug 16;12(2):223-32
pubmed: 22901542
Clin Rev Allergy Immunol. 2019 Jun;56(3):308-321
pubmed: 28963611
Cell Rep. 2016 Dec 6;17(10):2562-2571
pubmed: 27926861
J Leukoc Biol. 2022 Aug;112(2):279-288
pubmed: 35040511
PLoS One. 2014 Dec 17;9(12):e115564
pubmed: 25518000
Cell Host Microbe. 2020 Aug 12;28(2):322-334.e5
pubmed: 32544459
Steroids. 1998 Feb;63(2):111-6
pubmed: 9516722
Immunol Lett. 2009 Aug 15;125(2):151-5
pubmed: 19607861
Mol Endocrinol. 2006 Nov;20(11):2724-33
pubmed: 16772530
Br J Pharmacol. 2020 Oct;177(19):4375-4385
pubmed: 32698249
PLoS One. 2012;7(4):e35538
pubmed: 22514749
Cell. 2018 Jan 11;172(1-2):135-146.e9
pubmed: 29328908
Arterioscler Thromb Vasc Biol. 2014 Aug;34(8):1731-8
pubmed: 24903093
J Reprod Immunol. 2013 Mar;97(1):43-50
pubmed: 23432871
Science. 2014 Sep 26;345(6204):1251086
pubmed: 25258085
J Clin Virol. 2020 Jun;127:104370
pubmed: 32344321
Endocrinology. 1992 Sep;131(3):1458-66
pubmed: 1505477
J Innate Immun. 2014;6(2):152-8
pubmed: 24192057
Nat Rev Immunol. 2017 Aug;17(8):469-482
pubmed: 28627518
Cell. 1992 Mar 6;68(5):869-77
pubmed: 1547488
Int Immunol. 2013 Sep;25(9):521-9
pubmed: 23728775
Biomedicines. 2022 Jan 21;10(2):
pubmed: 35203438
Nat Rev Immunol. 2016 Oct;16(10):626-38
pubmed: 27546235
Mol Aspects Med. 2021 Feb;77:100897
pubmed: 32891423
Int Immunol. 2007 Mar;19(3):287-96
pubmed: 17289656
J Am Assoc Lab Anim Sci. 2019 Mar 1;58(2):246-250
pubmed: 30764891
Sci Rep. 2015 Oct 19;5:15224
pubmed: 26477569
Crit Care. 2020 Jul 9;24(1):405
pubmed: 32646459
Reproduction. 2007 May;133(5):1035-44
pubmed: 17616732
Endocr Res. 2009;34(4):101-8
pubmed: 19878070
Cell. 2018 Jan 11;172(1-2):147-161.e12
pubmed: 29328910
Endocrinology. 1993 Jun;132(6):2371-9
pubmed: 8504742
J Cyst Fibros. 2007 Jul;6(4):267-73
pubmed: 17137846
Biol Reprod. 2001 Sep;65(3):680-8
pubmed: 11514328
Science. 2000 Sep 8;289(5485):1751-4
pubmed: 10976068
Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17537-42
pubmed: 22988082
J Leukoc Biol. 2018 Sep;104(3):573-578
pubmed: 30153369
J Biol Chem. 1996 Mar 15;271(11):6217-24
pubmed: 8626413
Proc Natl Acad Sci U S A. 2021 Oct 19;118(42):
pubmed: 34663697
Mucosal Immunol. 2010 Sep;3(5):496-505
pubmed: 20505661

Auteurs

Alexander P Earhart (AP)

Department of Molecular Microbiology & Immunology, School of Medicine, University of Missouri, Columbia, MO 65212, USA.

Natalia G Karasseva (NG)

Department of Molecular Microbiology & Immunology, School of Medicine, University of Missouri, Columbia, MO 65212, USA.

Kathryn M Storey (KM)

Division of Biological Sciences, College of Arts & Science, University of Missouri, Columbia, MO 65212, USA.

Benjamin Olthoff (B)

Department of Biomedical Sciences, College of Veterinary Medicine, University of Missouri, Columbia, MO 65212, USA.

Md Bodruzzaman Sarker (MB)

Division of Animal Sciences, College of Agriculture, Food & Natural Resources, University of Missouri, Columbia, MO 65212, USA.

Kimberly G Laffey (KG)

Department of Molecular Microbiology & Immunology, School of Medicine, University of Missouri, Columbia, MO 65212, USA.

Margaret J Lange (MJ)

Department of Molecular Microbiology & Immunology, School of Medicine, University of Missouri, Columbia, MO 65212, USA.

R Scott Rector (RS)

Department of Nutrition and Exercise Physiology, School of Medicine, University of Missouri, Columbia, MO 65212, USA; Department of Medicine, School of Medicine, University of Missouri, Columbia, MO 65212, USA; Research Service, Harry S. Truman Memorial VA Hospital, University of Missouri, Columbia, MO 65212, USA; NextGen Precision Health Institute, University of Missouri, Columbia, MO 65212, USA.

Laura C Schulz (LC)

Department of Obstetrics, Gynecology, & Women's Health, School of Medicine, University of Missouri, Columbia, MO 65212, USA.

Diana Gil (D)

Department of Molecular Microbiology & Immunology, School of Medicine, University of Missouri, Columbia, MO 65212, USA; NextGen Precision Health Institute, University of Missouri, Columbia, MO 65212, USA; Department of Surgery, School of Medicine, University of Missouri, Columbia, MO 65212, USA; Department of Chemical & Biomedical Engineering, College of Engineering, University of Missouri, Columbia, MO 65212, USA.

Claudia M Neuhauser (CM)

Division of Research, Department of Mathematics, University of Houston, Houston, TX 77204, USA.

Adam G Schrum (AG)

Department of Molecular Microbiology & Immunology, School of Medicine, University of Missouri, Columbia, MO 65212, USA; Division of Animal Sciences, College of Agriculture, Food & Natural Resources, University of Missouri, Columbia, MO 65212, USA; NextGen Precision Health Institute, University of Missouri, Columbia, MO 65212, USA; Department of Surgery, School of Medicine, University of Missouri, Columbia, MO 65212, USA; Department of Chemical & Biomedical Engineering, College of Engineering, University of Missouri, Columbia, MO 65212, USA. Electronic address: schruma@health.missouri.edu.

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Classifications MeSH