Frontiers in Microbiology (Sep 2020)
Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells
- Koji Hosomi,
- Koji Hosomi,
- Naoko Shibata,
- Naoko Shibata,
- Naoko Shibata,
- Naoko Shibata,
- Atsushi Shimoyama,
- Tomoya Uto,
- Takahiro Nagatake,
- Takahiro Nagatake,
- Yoko Tojima,
- Yoko Tojima,
- Tomomi Nishino,
- Tomomi Nishino,
- Haruko Takeyama,
- Haruko Takeyama,
- Koichi Fukase,
- Hiroshi Kiyono,
- Hiroshi Kiyono,
- Hiroshi Kiyono,
- Hiroshi Kiyono,
- Jun Kunisawa,
- Jun Kunisawa,
- Jun Kunisawa,
- Jun Kunisawa,
- Jun Kunisawa,
- Jun Kunisawa,
- Jun Kunisawa,
- Jun Kunisawa,
- Jun Kunisawa,
- Jun Kunisawa,
- Jun Kunisawa
Affiliations
- Koji Hosomi
- Laboratory of Vaccine Materials, Center for Vaccine and Adjuvant Research, Ibaraki, Japan
- Koji Hosomi
- Laboratory of Gut Environmental System, National Institutes of Biomedical Innovation, Health, and Nutrition (NIBIOHN), Ibaraki, Japan
- Naoko Shibata
- Laboratory of Vaccine Materials, Center for Vaccine and Adjuvant Research, Ibaraki, Japan
- Naoko Shibata
- Laboratory of Gut Environmental System, National Institutes of Biomedical Innovation, Health, and Nutrition (NIBIOHN), Ibaraki, Japan
- Naoko Shibata
- International Research and Development Center for Mucosal Vaccines, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan
- Naoko Shibata
- Research Organization for Nano and Life Innovation, Waseda University, Tokyo, Japan
- Atsushi Shimoyama
- Graduate School of Science, Osaka University, Toyonaka, Japan
- Tomoya Uto
- Graduate School of Science, Osaka University, Toyonaka, Japan
- Takahiro Nagatake
- Laboratory of Vaccine Materials, Center for Vaccine and Adjuvant Research, Ibaraki, Japan
- Takahiro Nagatake
- Laboratory of Gut Environmental System, National Institutes of Biomedical Innovation, Health, and Nutrition (NIBIOHN), Ibaraki, Japan
- Yoko Tojima
- Laboratory of Vaccine Materials, Center for Vaccine and Adjuvant Research, Ibaraki, Japan
- Yoko Tojima
- Laboratory of Gut Environmental System, National Institutes of Biomedical Innovation, Health, and Nutrition (NIBIOHN), Ibaraki, Japan
- Tomomi Nishino
- Laboratory of Vaccine Materials, Center for Vaccine and Adjuvant Research, Ibaraki, Japan
- Tomomi Nishino
- Laboratory of Gut Environmental System, National Institutes of Biomedical Innovation, Health, and Nutrition (NIBIOHN), Ibaraki, Japan
- Haruko Takeyama
- Research Organization for Nano and Life Innovation, Waseda University, Tokyo, Japan
- Haruko Takeyama
- Department of Life Science and Medical Bioscience, Waseda University, Tokyo, Japan
- Koichi Fukase
- Graduate School of Science, Osaka University, Toyonaka, Japan
- Hiroshi Kiyono
- International Research and Development Center for Mucosal Vaccines, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan
- Hiroshi Kiyono
- IMSUT Distinguished Professor Unit, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan
- Hiroshi Kiyono
- Graduate School of Medicine, Chiba University, Chuo City, Japan
- Hiroshi Kiyono
- 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
- Jun Kunisawa
- Laboratory of Vaccine Materials, Center for Vaccine and Adjuvant Research, Ibaraki, Japan
- Jun Kunisawa
- Laboratory of Gut Environmental System, National Institutes of Biomedical Innovation, Health, and Nutrition (NIBIOHN), Ibaraki, Japan
- Jun Kunisawa
- International Research and Development Center for Mucosal Vaccines, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan
- Jun Kunisawa
- Research Organization for Nano and Life Innovation, Waseda University, Tokyo, Japan
- Jun Kunisawa
- IMSUT Distinguished Professor Unit, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan
- Jun Kunisawa
- Graduate School of Medicine, Chiba University, Chuo City, Japan
- Jun Kunisawa
- 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
- Jun Kunisawa
- 0Graduate School of Medicine, Osaka University, Suita, Japan
- Jun Kunisawa
- 1Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Japan
- Jun Kunisawa
- 2Graduate School of Density, Osaka University, Suita, Japan
- Jun Kunisawa
- 3Graduate School of Medicine, Kobe University, Kobe, Japan
- DOI
- https://doi.org/10.3389/fmicb.2020.561005
- Journal volume & issue
-
Vol. 11
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.
Keywords
- inducible nitric oxide synmase
- lipopolysaccharid
- mitochondrial respiration
- lymphoid-tissue-resident commensal bacteria
- apoptosis
- dendritic cells
