TY - JOUR
T1 - Lymphoid Tissue–Resident Alcaligenes Establish an Intracellular Symbiotic Environment by Creating a Unique Energy Shift in Dendritic Cells
AU - Hosomi, Koji
AU - Shibata, Naoko
AU - Shimoyama, Atsushi
AU - Uto, Tomoya
AU - Nagatake, Takahiro
AU - Tojima, Yoko
AU - Nishino, Tomomi
AU - Takeyama, Haruko
AU - Fukase, Koichi
AU - Kiyono, Hiroshi
AU - Kunisawa, Jun
N1 - Funding Information:
Funding. This work was supported by the Ministry of Education, Culture, Sports, Science, and Technology of Japan and the Japan Society for the Promotion of Science under grant nos. JP18H02150, JP18H02674, JP17K09604 to JK, JP18K17997, JP18H05280 to KH, JP16H01885 to KF, JP17K17686, JP17J07480 to NS, JP18H04620 to AS, JP15H05836 to KF, JP20K05749 to AS, JP20H04776 to AS, and JP18H05280 to KH; the Japan Agency for Medical Research and Development (AMED) under grant nos. JP17fk0108223h0002, JP17ek0410032s0102, JP17fk0108207h0002, JP17ek0210078h0002, JP17ak0101068h0 001, JP17gm1010006s0101, JP18ck0106243h0003, JP19ek041006 2h0001 to JK, JP19jm0110012h0005 to HK, JP19lm0203082, 17pc0101001h0001, 19jm0110012h0005, and 119fk0108051j0003 to KH; the Ministry of Health, Labour, and Welfare of Japan under grant no. JP19KA3001 to KH; the Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries, and Food Industry (JK); the Terumo Foundation for Life Sciences and Arts (JK); the ONO Medical Research Foundation (JK); the Canon Foundation (JK); and Cross-ministerial Strategic Innovation Promotion Program (JK); the Joint Research Project of the Institute of Medical Science, the University of Tokyo (JK and HK). None of these funding sources had a role in study design; in the collection, analysis, and interpretation of data; or in the writing of the report.
Publisher Copyright:
© Copyright © 2020 Hosomi, Shibata, Shimoyama, Uto, Nagatake, Tojima, Nishino, Takeyama, Fukase, Kiyono and Kunisawa.
PY - 2020/9/24
Y1 - 2020/9/24
N2 - 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.
AB - 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.
KW - apoptosis
KW - dendritic cells
KW - inducible nitric oxide synmase
KW - lipopolysaccharid
KW - lymphoid-tissue-resident commensal bacteria
KW - mitochondrial respiration
UR - http://www.scopus.com/inward/record.url?scp=85092282256&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85092282256&partnerID=8YFLogxK
U2 - 10.3389/fmicb.2020.561005
DO - 10.3389/fmicb.2020.561005
M3 - Article
AN - SCOPUS:85092282256
SN - 1664-302X
VL - 11
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
M1 - 561005
ER -