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Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells

Authors
  • Hosomi, Koji1, 2
  • Shibata, Naoko1, 2, 3, 4
  • Shimoyama, Atsushi5
  • Uto, Tomoya5
  • Nagatake, Takahiro1, 2
  • Tojima, Yoko1, 2
  • Nishino, Tomomi1, 2
  • Takeyama, Haruko4, 6
  • Fukase, Koichi5
  • Kiyono, Hiroshi3, 7, 8, 9
  • Kunisawa, Jun1, 2, 3, 4, 7, 8, 9, 10, 11, 12, 13
  • 1 Laboratory of Vaccine Materials, Center for Vaccine and Adjuvant Research, Ibaraki , (Japan)
  • 2 Laboratory of Gut Environmental System, National Institutes of Biomedical Innovation, Health, and Nutrition (NIBIOHN), Ibaraki , (Japan)
  • 3 International Research and Development Center for Mucosal Vaccines, The Institute of Medical Science, The University of Tokyo, Tokyo , (Japan)
  • 4 Research Organization for Nano and Life Innovation, Waseda University, Tokyo , (Japan)
  • 5 Graduate School of Science, Osaka University, Toyonaka , (Japan)
  • 6 Department of Life Science and Medical Bioscience, Waseda University, Tokyo , (Japan)
  • 7 IMSUT Distinguished Professor Unit, The Institute of Medical Science, The University of Tokyo, Tokyo , (Japan)
  • 8 Graduate School of Medicine, Chiba University, Chuo City , (Japan)
  • 9 Department of Medicine, School of Medicine and Chiba University – UC San Diego Center for Mucosal Immunology, Allergy, and Vaccine, University of California, San Diego, San Diego, CA , (United States)
  • 10 Graduate School of Medicine, Osaka University, Suita , (Japan)
  • 11 Graduate School of Pharmaceutical Sciences, Osaka University, Suita , (Japan)
  • 12 Graduate School of Density, Osaka University, Suita , (Japan)
  • 13 Graduate School of Medicine, Kobe University, Kobe , (Japan)
Type
Published Article
Journal
Frontiers in Microbiology
Publisher
Frontiers Media SA
Publication Date
Sep 24, 2020
Volume
11
Identifiers
DOI: 10.3389/fmicb.2020.561005
PMID: 33101234
PMCID: PMC7545135
Source
PubMed Central
Keywords
License
Unknown

Abstract

Lymphoid-tissue–resident commensal bacteria (LRCs), including Alcaligenes faecalis , are present in intestinal lymphoid tissue including the Peyer’s patches (PPs) of mammals and modulate the host immune system. Although LRCs can colonize within dendritic cells (DCs), the mechanisms through which LRCs persist in DCs and the symbiotic relationships between LRCs and DCs remain to be investigated. Here, we show an intracellular symbiotic system in which the LRC Alcaligenes creates a unique energy shift in DCs. Whereas DCs showed low mitochondrial respiration when they were co-cultured with Escherichia coli , DCs carrying A. faecalis maintained increased mitochondrial respiration. Furthermore, E. coli induced apoptosis of DCs but A. faecalis did not. Regarding an underlying mechanism, A. faecalis —unlike E. coli —did not induce intracellular nitric oxide (NO) production in DCs due to the low activity of its lipopolysaccharide (LPS). Therefore, A. faecalis , an example of LRCs, may persist within intestinal lymphoid tissue because they elicit little NO production in DCs. In addition, the symbiotic DCs exhibit characteristic physiologic changes, including a low rate of apoptosis and increased mitochondrial respiration.

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