Murine gut microbiota dysbiosis via enteric infection modulates the foreign body response to a distal biomaterial implant

B Brenda Yang (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) N Natalie Rutkowski (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) A Anna Ruta (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) E Elise Gray-Gaillard (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) D David R. Maestas (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) S Sean H. Kelly (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) K Kavita Krishnan (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) X Xinqun Wu (Department of Medicine, Johns Hopkins University School of Medicine) S Shaoguang Wu A Allen Chen (Department of Biomedical Engineering, Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University) J Joscelyn C. Mejías (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) J Joshua S. T. Hooks (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) I Isabel Vanderzee (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) P Patricia Mensah (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) N Nazmiye Celik (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) M Marie Eric (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) P Peter Abraham (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University) A Ada Tam (Department of Oncology and Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine) F Franck Housseau (Department of Oncology and Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine) D Drew M. Pardoll (Department of Oncology and Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine) C Cynthia L. Sears J Jennifer H. Elisseeff (Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University)

Abstract

The gut microbiota influences systemic immunity and the function of distal tissues, including the brain, liver, skin, lung, and muscle. However, the role of the gut microbiota in the foreign body response and fibrosis is largely unexplored. To investigate this connection, we perturbed the homeostasis of the murine gut microbiota via infection with the pathogenic bacterial species enterotoxigenic Bacteroides fragilis (ETBF) and implanted particulate material (mean particle size <600 μm) of the synthetic polymer polycaprolactone (PCL) into a distal muscle injury. ETBF infection in mice led to increased neutrophil and γδ T cell infiltration into the PCL implant site. ETBF infection alone promoted systemic inflammation, increased levels of neutrophils in lymphoid tissues, and altered skeletal muscle gene expression. At the PCL implant site, we found significant changes in the transcriptome of sorted stromal cells between infected and control mice, including differences related to ECM components such as proteoglycans and glycosaminoglycans. However, we did not observe ETBF-induced differences in fibrosis levels. These results demonstrate the ability of the gut microbiota to mediate long-distance effects such as immune and stromal responses to a distal biomaterial implant.

Article Details

Volume / Issue Vol. 122, Issue 20
Published May 20, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (22)

B

Brenda Yang

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

N

Natalie Rutkowski

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

A

Anna Ruta

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

E

Elise Gray-Gaillard

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

D

David R. Maestas

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

S

Sean H. Kelly

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

K

Kavita Krishnan

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

X

Xinqun Wu

Department of Medicine, Johns Hopkins University School of Medicine

S

Shaoguang Wu

A

Allen Chen

Department of Biomedical Engineering, Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University

J

Joscelyn C. Mejías

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

J

Joshua S. T. Hooks

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

I

Isabel Vanderzee

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

P

Patricia Mensah

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

N

Nazmiye Celik

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

M

Marie Eric

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

P

Peter Abraham

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University

A

Ada Tam

Department of Oncology and Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine

F

Franck Housseau

Department of Oncology and Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine

D

Drew M. Pardoll

Department of Oncology and Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine

C

Cynthia L. Sears

J

Jennifer H. Elisseeff

Department of Biomedical Engineering, Cellular and Molecular Medicine, or Ophthalmology, Translational Tissue Engineering Center, Johns Hopkins University