Persistent colonization of non-lymphoid tissue-resident macrophages by Stenotrophomonas maltophilia

Ichiro Takahashi; Koji Hosomi; Takahiro Nagatake; Hirokazu Toubou; Daiki Yamamoto; Ikue Hayashi; Yosuke Kurashima; Shintaro Sato; Naoko Shibata; Yoshiyuki Goto; Fumito Maruyama; Ichiro Nakagawa; Asaomi Kuwae; Akio Abe; Jun Kunisawa; Hiroshi Kiyono

doi:10.1093/intimm/dxz071

Persistent colonization of non-lymphoid tissue-resident macrophages by Stenotrophomonas maltophilia

Ichiro Takahashi, Koji Hosomi, Takahiro Nagatake, Hirokazu Toubou, Daiki Yamamoto, Ikue Hayashi, Yosuke Kurashima, Shintaro Sato, Naoko Shibata, Yoshiyuki Goto, Fumito Maruyama, Ichiro Nakagawa, Asaomi Kuwae, Akio Abe, Jun Kunisawa^*, Hiroshi Kiyono

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

3 Citations (Scopus)

Abstract

Accumulating evidence has revealed that lymphoid tissue-resident commensal bacteria (e.g. Alcaligenes spp.) survive within dendritic cells. We extended our previous study by investigating microbes that persistently colonize colonic macrophages. 16S rRNA-based metagenome analysis using DNA purified from murine colonic macrophages revealed the presence of Stenotrophomonas maltophilia. The in situ intracellular colonization by S. maltophilia was recapitulated in vitro by using bone marrow-derived macrophages (BMDMs). Co-culture of BMDMs with clinically isolated S. maltophilia led to increased mitochondrial respiration and robust IL-10 production. We further identified a 25-kDa protein encoded by the gene assigned as smlt2713 (recently renamed as SMLT-RS12935) and secreted by S. maltophilia as the factor responsible for enhanced IL-10 production by BMDMs. IL-10 production is critical for maintenance of the symbiotic condition, because intracellular colonization by S. maltophilia was impaired in IL-10-deficient BMDMs, and smlt2713-deficient S. maltophilia failed to persistently colonize IL-10-competent BMDMs. These findings indicate a novel commensal network between colonic macrophages and S. maltophilia that is mediated by IL-10 and smlt2713.

Original language	English
Pages (from-to)	133-141
Number of pages	9
Journal	International Immunology
Volume	32
Issue number	2
DOIs	https://doi.org/10.1093/intimm/dxz071
Publication status	Published - 2019 Nov 12
Externally published	Yes

Keywords

IL-10
colitis
gut-resident macrophage
intracellular commensal bacteria
symbiotic factor smlt2713

ASJC Scopus subject areas

Immunology and Allergy
Immunology

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10.1093/intimm/dxz071

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Takahashi, I., Hosomi, K., Nagatake, T., Toubou, H., Yamamoto, D., Hayashi, I., Kurashima, Y., Sato, S., Shibata, N., Goto, Y., Maruyama, F., Nakagawa, I., Kuwae, A., Abe, A., Kunisawa, J., & Kiyono, H. (2019). Persistent colonization of non-lymphoid tissue-resident macrophages by Stenotrophomonas maltophilia. International Immunology, 32(2), 133-141. https://doi.org/10.1093/intimm/dxz071

Takahashi, I, Hosomi, K, Nagatake, T, Toubou, H, Yamamoto, D, Hayashi, I, Kurashima, Y, Sato, S, Shibata, N, Goto, Y, Maruyama, F, Nakagawa, I, Kuwae, A, Abe, A, Kunisawa, J & Kiyono, H 2019, 'Persistent colonization of non-lymphoid tissue-resident macrophages by Stenotrophomonas maltophilia', International Immunology, vol. 32, no. 2, pp. 133-141. https://doi.org/10.1093/intimm/dxz071

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title = "Persistent colonization of non-lymphoid tissue-resident macrophages by Stenotrophomonas maltophilia",

abstract = "Accumulating evidence has revealed that lymphoid tissue-resident commensal bacteria (e.g. Alcaligenes spp.) survive within dendritic cells. We extended our previous study by investigating microbes that persistently colonize colonic macrophages. 16S rRNA-based metagenome analysis using DNA purified from murine colonic macrophages revealed the presence of Stenotrophomonas maltophilia. The in situ intracellular colonization by S. maltophilia was recapitulated in vitro by using bone marrow-derived macrophages (BMDMs). Co-culture of BMDMs with clinically isolated S. maltophilia led to increased mitochondrial respiration and robust IL-10 production. We further identified a 25-kDa protein encoded by the gene assigned as smlt2713 (recently renamed as SMLT-RS12935) and secreted by S. maltophilia as the factor responsible for enhanced IL-10 production by BMDMs. IL-10 production is critical for maintenance of the symbiotic condition, because intracellular colonization by S. maltophilia was impaired in IL-10-deficient BMDMs, and smlt2713-deficient S. maltophilia failed to persistently colonize IL-10-competent BMDMs. These findings indicate a novel commensal network between colonic macrophages and S. maltophilia that is mediated by IL-10 and smlt2713.",

keywords = "IL-10, colitis, gut-resident macrophage, intracellular commensal bacteria, symbiotic factor smlt2713",

author = "Ichiro Takahashi and Koji Hosomi and Takahiro Nagatake and Hirokazu Toubou and Daiki Yamamoto and Ikue Hayashi and Yosuke Kurashima and Shintaro Sato and Naoko Shibata and Yoshiyuki Goto and Fumito Maruyama and Ichiro Nakagawa and Asaomi Kuwae and Akio Abe and Jun Kunisawa and Hiroshi Kiyono",

note = "Funding Information: This research was supported, at least in part, by grants from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT) and the Japan Society for the Promotion of Science (JSPS; kakenhi JP15H05790, JP18H02150, JP18H02674, JP17K09604, JP26670241 and JP26293111 to J.K.; JP19K10088 to I.T.; JP19K07617 to T.N.; and JP18K17997 to K.H.); the Japan Agency for Medical Research and Development (AMED; JP15gm0410004h0106 to I.T.; JP18ek0410032s0103, JP18ak0101068h0002, JP19gm1010006s0103 and 19ek0410062h0001 to J.K.); the grant for Joint Research Project of the Institute of Medical Science, the University of Tokyo (to J.K. and H.K.); Cross-ministerial Strategic Innovation Promotion Program (SIP to J.K.); the Canon Foundation (to J.K.); and the Ministry of Health, Labour, and Welfare of Japan (grant number JP19KA3001 to K.H.). Publisher Copyright: {\textcopyright} 2019 The Author(s) 2019. Published by Oxford University Press on behalf of The Japanese Society for Immunology.",

year = "2019",

month = nov,

day = "12",

doi = "10.1093/intimm/dxz071",

language = "English",

volume = "32",

pages = "133--141",

journal = "International Immunology",

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publisher = "Oxford University Press",

number = "2",

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TY - JOUR

T1 - Persistent colonization of non-lymphoid tissue-resident macrophages by Stenotrophomonas maltophilia

AU - Takahashi, Ichiro

AU - Hosomi, Koji

AU - Nagatake, Takahiro

AU - Toubou, Hirokazu

AU - Yamamoto, Daiki

AU - Hayashi, Ikue

AU - Kurashima, Yosuke

AU - Sato, Shintaro

AU - Shibata, Naoko

AU - Goto, Yoshiyuki

AU - Maruyama, Fumito

AU - Nakagawa, Ichiro

AU - Kuwae, Asaomi

AU - Abe, Akio

AU - Kunisawa, Jun

AU - Kiyono, Hiroshi

N1 - Funding Information: This research was supported, at least in part, by grants from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT) and the Japan Society for the Promotion of Science (JSPS; kakenhi JP15H05790, JP18H02150, JP18H02674, JP17K09604, JP26670241 and JP26293111 to J.K.; JP19K10088 to I.T.; JP19K07617 to T.N.; and JP18K17997 to K.H.); the Japan Agency for Medical Research and Development (AMED; JP15gm0410004h0106 to I.T.; JP18ek0410032s0103, JP18ak0101068h0002, JP19gm1010006s0103 and 19ek0410062h0001 to J.K.); the grant for Joint Research Project of the Institute of Medical Science, the University of Tokyo (to J.K. and H.K.); Cross-ministerial Strategic Innovation Promotion Program (SIP to J.K.); the Canon Foundation (to J.K.); and the Ministry of Health, Labour, and Welfare of Japan (grant number JP19KA3001 to K.H.). Publisher Copyright: © 2019 The Author(s) 2019. Published by Oxford University Press on behalf of The Japanese Society for Immunology.

PY - 2019/11/12

Y1 - 2019/11/12

N2 - Accumulating evidence has revealed that lymphoid tissue-resident commensal bacteria (e.g. Alcaligenes spp.) survive within dendritic cells. We extended our previous study by investigating microbes that persistently colonize colonic macrophages. 16S rRNA-based metagenome analysis using DNA purified from murine colonic macrophages revealed the presence of Stenotrophomonas maltophilia. The in situ intracellular colonization by S. maltophilia was recapitulated in vitro by using bone marrow-derived macrophages (BMDMs). Co-culture of BMDMs with clinically isolated S. maltophilia led to increased mitochondrial respiration and robust IL-10 production. We further identified a 25-kDa protein encoded by the gene assigned as smlt2713 (recently renamed as SMLT-RS12935) and secreted by S. maltophilia as the factor responsible for enhanced IL-10 production by BMDMs. IL-10 production is critical for maintenance of the symbiotic condition, because intracellular colonization by S. maltophilia was impaired in IL-10-deficient BMDMs, and smlt2713-deficient S. maltophilia failed to persistently colonize IL-10-competent BMDMs. These findings indicate a novel commensal network between colonic macrophages and S. maltophilia that is mediated by IL-10 and smlt2713.

AB - Accumulating evidence has revealed that lymphoid tissue-resident commensal bacteria (e.g. Alcaligenes spp.) survive within dendritic cells. We extended our previous study by investigating microbes that persistently colonize colonic macrophages. 16S rRNA-based metagenome analysis using DNA purified from murine colonic macrophages revealed the presence of Stenotrophomonas maltophilia. The in situ intracellular colonization by S. maltophilia was recapitulated in vitro by using bone marrow-derived macrophages (BMDMs). Co-culture of BMDMs with clinically isolated S. maltophilia led to increased mitochondrial respiration and robust IL-10 production. We further identified a 25-kDa protein encoded by the gene assigned as smlt2713 (recently renamed as SMLT-RS12935) and secreted by S. maltophilia as the factor responsible for enhanced IL-10 production by BMDMs. IL-10 production is critical for maintenance of the symbiotic condition, because intracellular colonization by S. maltophilia was impaired in IL-10-deficient BMDMs, and smlt2713-deficient S. maltophilia failed to persistently colonize IL-10-competent BMDMs. These findings indicate a novel commensal network between colonic macrophages and S. maltophilia that is mediated by IL-10 and smlt2713.

KW - IL-10

KW - colitis

KW - gut-resident macrophage

KW - intracellular commensal bacteria

KW - symbiotic factor smlt2713

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U2 - 10.1093/intimm/dxz071

DO - 10.1093/intimm/dxz071

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SN - 0953-8178

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JO - International Immunology

JF - International Immunology

IS - 2

ER -

Persistent colonization of non-lymphoid tissue-resident macrophages by Stenotrophomonas maltophilia

Abstract

Keywords

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