Sex-dependent gastrointestinal colonization resistance to MRSA is microbiota and Th17 dependent

Gastrointestinal (GI) colonization by methicillin-resistant Staphylococcus aureus (MRSA) is associated with a high risk of transmission and invasive disease in vulnerable populations. The immune and microbial factors that permit GI colonization remain unknown. Male sex is correlated with enhanced St...

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Main Authors: Alannah Lejeune, Chunyi Zhou, Defne Ercelen, Gregory Putzel, Xiaomin Yao, Alyson R Guy, Miranda Pawline, Magdalena Podkowik, Alejandro Pironti, Victor J Torres, Bo Shopsin, Ken Cadwell
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Language:English
Published: eLife Sciences Publications Ltd 2025-04-01
Series:eLife
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Online Access:https://elifesciences.org/articles/101606
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author Alannah Lejeune
Chunyi Zhou
Defne Ercelen
Gregory Putzel
Xiaomin Yao
Alyson R Guy
Miranda Pawline
Magdalena Podkowik
Alejandro Pironti
Victor J Torres
Bo Shopsin
Ken Cadwell
author_facet Alannah Lejeune
Chunyi Zhou
Defne Ercelen
Gregory Putzel
Xiaomin Yao
Alyson R Guy
Miranda Pawline
Magdalena Podkowik
Alejandro Pironti
Victor J Torres
Bo Shopsin
Ken Cadwell
author_sort Alannah Lejeune
collection DOAJ
description Gastrointestinal (GI) colonization by methicillin-resistant Staphylococcus aureus (MRSA) is associated with a high risk of transmission and invasive disease in vulnerable populations. The immune and microbial factors that permit GI colonization remain unknown. Male sex is correlated with enhanced Staphylococcus aureus nasal carriage, skin and soft tissue infections, and bacterial sepsis. Here, we established a mouse model of sexual dimorphism during GI colonization by MRSA. Our results show that in contrast to male mice that were susceptible to persistent colonization, female mice rapidly cleared MRSA from the GI tract following oral inoculation in a manner dependent on the gut microbiota. This colonization resistance displayed by female mice was mediated by an increase in IL-17A+ CD4+ T cells (Th17) and dependent on neutrophils. Ovariectomy of female mice increased MRSA burden, but gonadal female mice that have the Y chromosome retained enhanced Th17 responses and colonization resistance. Our study reveals a novel intersection between sex and gut microbiota underlying colonization resistance against a major widespread pathogen.
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institution OA Journals
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language English
publishDate 2025-04-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj-art-8fc2dc5432bc449480fbdffb0db944922025-08-20T02:08:40ZengeLife Sciences Publications LtdeLife2050-084X2025-04-011310.7554/eLife.101606Sex-dependent gastrointestinal colonization resistance to MRSA is microbiota and Th17 dependentAlannah Lejeune0Chunyi Zhou1Defne Ercelen2Gregory Putzel3Xiaomin Yao4Alyson R Guy5Miranda Pawline6Magdalena Podkowik7Alejandro Pironti8Victor J Torres9https://orcid.org/0000-0002-7126-0489Bo Shopsin10https://orcid.org/0009-0001-7729-8584Ken Cadwell11https://orcid.org/0000-0002-5860-0661Department of Microbiology, New York University School of Medicine, New York, United States; Department of Medicine, Division of Infectious Diseases, New York University School of Medicine, New York, United StatesDepartment of Microbiology, New York University School of Medicine, New York, United States; Department of Medicine, Division of Infectious Diseases, New York University School of Medicine, New York, United StatesDepartment of Medicine, Division of Gastroenterology and Hepatology, New York University Langone Health, New York, United StatesDepartment of Microbiology, New York University School of Medicine, New York, United States; Antimicrobial-Resistant Pathogens Program, New York University School of Medicine, New York, United StatesDepartment of Medicine, Division of Infectious Diseases, New York University School of Medicine, New York, United StatesNYU-Regeneron Veterinary Postdoctoral Training Program in Laboratory Animal Medicine, Division of Comparative Medicine, New York University School of Medicine, New York, United StatesDepartment of Medicine, Division of Gastroenterology and Hepatology, New York University Langone Health, New York, United StatesDepartment of Medicine, Division of Infectious Diseases, New York University School of Medicine, New York, United States; Antimicrobial-Resistant Pathogens Program, New York University School of Medicine, New York, United StatesDepartment of Microbiology, New York University School of Medicine, New York, United States; Antimicrobial-Resistant Pathogens Program, New York University School of Medicine, New York, United StatesDepartment of Microbiology, New York University School of Medicine, New York, United States; Department of Host-Microbe Interactions, St. Jude Children’s Research Hospital, Memphis, United StatesDepartment of Microbiology, New York University School of Medicine, New York, United States; Department of Medicine, Division of Infectious Diseases, New York University School of Medicine, New York, United States; Antimicrobial-Resistant Pathogens Program, New York University School of Medicine, New York, United StatesDepartment of Medicine, Division of Gastroenterology and Hepatology, University of Pennsylvania Perelman School of Medicine, Philadelphia, United States; Department of Pathobiology, University of Pennsylvania Perelman School of Veterinary Medicine, Philadelphia, United StatesGastrointestinal (GI) colonization by methicillin-resistant Staphylococcus aureus (MRSA) is associated with a high risk of transmission and invasive disease in vulnerable populations. The immune and microbial factors that permit GI colonization remain unknown. Male sex is correlated with enhanced Staphylococcus aureus nasal carriage, skin and soft tissue infections, and bacterial sepsis. Here, we established a mouse model of sexual dimorphism during GI colonization by MRSA. Our results show that in contrast to male mice that were susceptible to persistent colonization, female mice rapidly cleared MRSA from the GI tract following oral inoculation in a manner dependent on the gut microbiota. This colonization resistance displayed by female mice was mediated by an increase in IL-17A+ CD4+ T cells (Th17) and dependent on neutrophils. Ovariectomy of female mice increased MRSA burden, but gonadal female mice that have the Y chromosome retained enhanced Th17 responses and colonization resistance. Our study reveals a novel intersection between sex and gut microbiota underlying colonization resistance against a major widespread pathogen.https://elifesciences.org/articles/101606MRSAmicrobiotaGI tractsex hormoneTh17colonization resistance
spellingShingle Alannah Lejeune
Chunyi Zhou
Defne Ercelen
Gregory Putzel
Xiaomin Yao
Alyson R Guy
Miranda Pawline
Magdalena Podkowik
Alejandro Pironti
Victor J Torres
Bo Shopsin
Ken Cadwell
Sex-dependent gastrointestinal colonization resistance to MRSA is microbiota and Th17 dependent
eLife
MRSA
microbiota
GI tract
sex hormone
Th17
colonization resistance
title Sex-dependent gastrointestinal colonization resistance to MRSA is microbiota and Th17 dependent
title_full Sex-dependent gastrointestinal colonization resistance to MRSA is microbiota and Th17 dependent
title_fullStr Sex-dependent gastrointestinal colonization resistance to MRSA is microbiota and Th17 dependent
title_full_unstemmed Sex-dependent gastrointestinal colonization resistance to MRSA is microbiota and Th17 dependent
title_short Sex-dependent gastrointestinal colonization resistance to MRSA is microbiota and Th17 dependent
title_sort sex dependent gastrointestinal colonization resistance to mrsa is microbiota and th17 dependent
topic MRSA
microbiota
GI tract
sex hormone
Th17
colonization resistance
url https://elifesciences.org/articles/101606
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