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PMID: 26944199 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Gut Microbiota-Induced Immunoglobulin G Controls Systemic Infection by Symbiotic Bacteria and Pathogens.

Immunity ·Vol. 44 ·No. 3 ·2016-03-15 ·Pages 647-658

Zeng MY, Cisalpino D, Varadarajan S, Hellman J, Warren HS, Cascalho M, Inohara N, Núñez G

Abstract

The gut microbiota is compartmentalized in the intestinal lumen and induces local immune responses, but it remains unknown whether the gut microbiota can induce systemic response and contribute to systemic immunity. We report that selective gut symbiotic gram-negative bacteria were able to disseminate systemically to induce immunoglobulin G (IgG) response, which primarily targeted gram-negative bacterial antigens and conferred protection against systemic infections by E. coli and Salmonella by directly coating bacteria to promote killing by phagocytes. T cells and Toll-like receptor 4 on B cells were important in the generation of microbiota-specific IgG. We identified murein lipoprotein (MLP), a highly conserved gram-negative outer membrane protein, as a major antigen that induced systemic IgG homeostatically in both mice and humans. Administration of anti-MLP IgG conferred crucial protection against systemic Salmonella infection. Thus, our findings reveal an important function for the gut microbiota in combating systemic infection through the induction of protective IgG.

MeSH Terms
Animals Bacterial Load/genetics Gram-Negative Bacteria/immunology Gram-Negative Bacterial Infections/immunology Homeostasis/genetics Host-Pathogen Interactions Immunoglobulin G/genetics,metabolism Intestines/immunology,microbiology Mice Mice, Inbred C57BL Mice, Knockout Microbiota Peptidoglycan/immunology Toll-Like Receptor 2/genetics Toll-Like Receptor 4/genetics
Chemicals
Immunoglobulin G Peptidoglycan Tlr2 protein, mouse Tlr4 protein, mouse Toll-Like Receptor 2 Toll-Like Receptor 4
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Zeng Melody Y
Department of Pathology and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, MI 48109, USA.
Cisalpino Daniel
Department of Pathology and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Department of Microbiology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG 31270-901, Brazil.
Varadarajan Saranyaraajan
Department of Pathology and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, MI 48109, USA.
Hellman Judith
Department of Anesthesia and Perioperative Care, Division of Critical Care Medicine, University of California, San Francisco, San Francisco, CA 94110, USA.
Warren H Shaw
Infectious Disease Unit, Massachusetts General Hospital, Boston, MA 02114, USA.
Cascalho Marilia
Transplantation Biology, Department of Surgery and Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109, USA.
Inohara Naohiro
Department of Pathology and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, MI 48109, USA.
Núñez Gabriel
Department of Pathology and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, MI 48109, USA. Electronic address: gabriel.nunez@umich.edu.
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Article Info
Journal
Immunity
Abbr.
Immunity
ISSN
1097-4180
Published
2016-03-15
Epub
2016-00-02
Pages
647-658
Language
English
Region
United States
NLM ID
9432918
PMCID
PMC4794373
Subset
IM
Grants
NIDDK NIH HHS · DK095782 · United States
NIDDK NIH HHS · R01 DK091191 · United States
NIDDK NIH HHS · T32DK094775 · United States
NHLBI NIH HHS · T32 HL007517 · United States
NIGMS NIH HHS · R01 GM59694 · United States
NIDDK NIH HHS · NIH 5P30DK034933 · United States
NIGMS NIH HHS · R01 GM059694 · United States
NIDDK NIH HHS · DK091191 · United States
NIAID NIH HHS · R21 AI117561 · United States
NHLBI NIH HHS · T32HL007517 · United States
NIDDK NIH HHS · P30 DK034933 · United States
NIAID NIH HHS · 5R21AI117561 · United States
NIDDK NIH HHS · R01 DK095782 · United States
NIDDK NIH HHS · T32 DK094775 · United States
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