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Interleukin-11 is a Marker for Both Cancer- and Inflammation-Associated Fibroblasts that Contribute to Colorectal Cancer Progression

Takashi Nishina, Yutaka Deguchi, Wakami Takeda, View ORCID ProfileMasato Ohtsuka, View ORCID ProfileDaisuke Ohshima, Soh Yamazaki, Mika Kawauchi, Eri Nakamura, View ORCID ProfileChiharu Nishiyama, View ORCID ProfileYuko Kojima, View ORCID ProfileSatomi Adachi-Akahane, Mizuho Hasegawa, Mizuho Nakayama, Masanobu Oshima, View ORCID ProfileHideo Yagita, Kazutoshi Shibuya, View ORCID ProfileTetuo Mikami, View ORCID ProfileNaohiro Inohara, View ORCID ProfileNorihiro Tada, View ORCID ProfileHiroyasu Nakano
doi: https://doi.org/10.1101/2020.01.25.919795
Takashi Nishina
1Department of Biochemistry, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
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  • For correspondence: takashi.nishina@med.toho-u.ac.jp hiroyasu.nakano@med.toho-u.ac.jp
Yutaka Deguchi
1Department of Biochemistry, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
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Wakami Takeda
1Department of Biochemistry, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
2Laboratory of Molecular Biology and Immunology, Department of Biological Science and Technology, Faculty of Industrial Science and Technology, Tokyo University of Science, 6-3-1 Niijuku, Katsushika-ku, Tokyo, 125–8585, Japan.
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Masato Ohtsuka
3Department of Molecular Life Science, Division of Basic Medical Science and Molecular Medicine, School of Medicine, Tokai University, 143 Shimokasuya, Isehara, Kanagawa, 259-1193, Japan.
4The Institute of Medical Sciences, Tokai University, 143 Shimokasuya, Isehara, Kanagawa, 259-1193, Japan.
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  • ORCID record for Masato Ohtsuka
Daisuke Ohshima
5Department of Physiology, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
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Soh Yamazaki
1Department of Biochemistry, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
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Mika Kawauchi
1Department of Biochemistry, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
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Eri Nakamura
6Research Institute for Diseases of Old Age, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan.
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Chiharu Nishiyama
2Laboratory of Molecular Biology and Immunology, Department of Biological Science and Technology, Faculty of Industrial Science and Technology, Tokyo University of Science, 6-3-1 Niijuku, Katsushika-ku, Tokyo, 125–8585, Japan.
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Yuko Kojima
7Laboratory of Morphology and Image Analysis, Research Support Center, Juntendo University Graduate School of Medicine, Tokyo 113-8421, Japan.
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Satomi Adachi-Akahane
5Department of Physiology, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
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  • ORCID record for Satomi Adachi-Akahane
Mizuho Hasegawa
8Department of Pathology, University of Michigan Medical School, Ann Arbor, MI 48109, USA.
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Mizuho Nakayama
9WPI Nano Life Science Institute (WPI-Nano LSI), Division of Genetics, Cancer Research Institute, Kanazawa University, Kanazawa, Ishikawa 920-1192, Japan.
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Masanobu Oshima
9WPI Nano Life Science Institute (WPI-Nano LSI), Division of Genetics, Cancer Research Institute, Kanazawa University, Kanazawa, Ishikawa 920-1192, Japan.
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Hideo Yagita
10Department of Immunology, Juntendo University Graduate School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan.
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Kazutoshi Shibuya
11Department of Surgical Pathology, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
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Tetuo Mikami
12Department of Pathology, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
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Naohiro Inohara
8Department of Pathology, University of Michigan Medical School, Ann Arbor, MI 48109, USA.
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Norihiro Tada
6Research Institute for Diseases of Old Age, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan.
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Hiroyasu Nakano
1Department of Biochemistry, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
13Host Defense Research Center, Toho University School of Medicine, 5-21-16 Omori-Nishi, Ota-ku, Tokyo 143-8540, Japan.
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  • ORCID record for Hiroyasu Nakano
  • For correspondence: takashi.nishina@med.toho-u.ac.jp hiroyasu.nakano@med.toho-u.ac.jp
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SUMMARY

Interleukin (IL)-11 is a member of the IL-6 family of cytokines and involved in multiple cellular responses, including tumor development. However, the origin and functions of IL-11-producing (IL-11+) cells are not fully understood. To characterize IL-11+ cells in vivo, we generated Il11 reporter mice. IL-11+ cells appeared in the colon of three murine tumor models, and a murine acute colitis model. Il11ra1 or Il11 deletion attenuated the development of colitis-associated colorectal cancer. IL-11+ cells expressed fibroblast markers, and genes associated with cell proliferation and tissue repair. IL-11 induced STAT3 phosphorylation in colonic fibroblasts, suggesting the activation of IL-11+ fibroblasts. Analysis using the human cancer database revealed that genes enriched in IL-11+ fibroblasts were elevated in human colorectal cancer, and correlated with reduced disease-free survival. Together, our results suggested that tumor cells induced IL-11+ fibroblasts, and that a feed-forward loop between IL-11 and IL-11+ fibroblasts might contribute to tumor development.

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  • ↵14 Lead contact.

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Posted January 26, 2020.
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Interleukin-11 is a Marker for Both Cancer- and Inflammation-Associated Fibroblasts that Contribute to Colorectal Cancer Progression
Takashi Nishina, Yutaka Deguchi, Wakami Takeda, Masato Ohtsuka, Daisuke Ohshima, Soh Yamazaki, Mika Kawauchi, Eri Nakamura, Chiharu Nishiyama, Yuko Kojima, Satomi Adachi-Akahane, Mizuho Hasegawa, Mizuho Nakayama, Masanobu Oshima, Hideo Yagita, Kazutoshi Shibuya, Tetuo Mikami, Naohiro Inohara, Norihiro Tada, Hiroyasu Nakano
bioRxiv 2020.01.25.919795; doi: https://doi.org/10.1101/2020.01.25.919795
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Interleukin-11 is a Marker for Both Cancer- and Inflammation-Associated Fibroblasts that Contribute to Colorectal Cancer Progression
Takashi Nishina, Yutaka Deguchi, Wakami Takeda, Masato Ohtsuka, Daisuke Ohshima, Soh Yamazaki, Mika Kawauchi, Eri Nakamura, Chiharu Nishiyama, Yuko Kojima, Satomi Adachi-Akahane, Mizuho Hasegawa, Mizuho Nakayama, Masanobu Oshima, Hideo Yagita, Kazutoshi Shibuya, Tetuo Mikami, Naohiro Inohara, Norihiro Tada, Hiroyasu Nakano
bioRxiv 2020.01.25.919795; doi: https://doi.org/10.1101/2020.01.25.919795

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