Upregulation of S100A10 in metastasized breast cancer stem cells

Hisano Yanagi; Takashi Watanabe; Tatsunori Nishimura; Takanori Hayashi; Seishi Kono; Hitomi Tsuchida; Munetsugu Hirata; Yuko Kijima; Shintaro Takao; Seiji Okada; Motoshi Suzuki; Kazuyoshi Imaizumi; Kenji Kawada; Hironobu Minami; Noriko Gotoh; Yohei Shimono

doi:10.1111/cas.14659

Upregulation of S100A10 in metastasized breast cancer stem cells

Hisano Yanagi, Takashi Watanabe, Tatsunori Nishimura, Takanori Hayashi, Seishi Kono, Hitomi Tsuchida, Munetsugu Hirata, Yuko Kijima, Shintaro Takao, Seiji Okada, Motoshi Suzuki, Kazuyoshi Imaizumi, Kenji Kawada, Hironobu Minami, Noriko Gotoh, Yohei Shimono

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

Abstract

Metastatic progression remains the major cause of death in human breast cancer. Cancer cells with cancer stem cell (CSC) properties drive initiation and growth of metastases at distant sites. We have previously established the breast cancer patient-derived tumor xenograft (PDX) mouse model in which CSC marker CD44⁺ cancer cells formed spontaneous microscopic metastases in the liver. In this PDX mouse, the expression levels of S100A10 and its family proteins were much higher in the CD44⁺ cancer cells metastasized to the liver than those at the primary site. Knockdown of S100A10 in breast cancer cells suppressed and overexpression of S100A10 in breast cancer PDX cells enhanced their invasion abilities and 3D organoid formation capacities in vitro. Mechanistically, S100A10 regulated the matrix metalloproteinase activity and the expression levels of stem cell–related genes. Finally, constitutive knockdown of S100A10 significantly reduced their metastatic ability to the liver in vivo. These findings suggest that S100A10 functions as a metastasis promoter of breast CSCs by conferring both invasion ability and CSC properties in breast cancers.

Original language	English
Pages (from-to)	4359-4370
Number of pages	12
Journal	Cancer science
Volume	111
Issue number	12
DOIs	https://doi.org/10.1111/cas.14659
Publication status	Published - 12-2020

All Science Journal Classification (ASJC) codes

Oncology
Cancer Research

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Yanagi, Hisano ; Watanabe, Takashi ; Nishimura, Tatsunori ; Hayashi, Takanori ; Kono, Seishi ; Tsuchida, Hitomi ; Hirata, Munetsugu ; Kijima, Yuko ; Takao, Shintaro ; Okada, Seiji ; Suzuki, Motoshi ; Imaizumi, Kazuyoshi ; Kawada, Kenji ; Minami, Hironobu ; Gotoh, Noriko ; Shimono, Yohei. / Upregulation of S100A10 in metastasized breast cancer stem cells. In: Cancer science. 2020 ; Vol. 111, No. 12. pp. 4359-4370.

@article{f0f7bbd091074494b429fc69d6eafe73,

title = "Upregulation of S100A10 in metastasized breast cancer stem cells",

abstract = "Metastatic progression remains the major cause of death in human breast cancer. Cancer cells with cancer stem cell (CSC) properties drive initiation and growth of metastases at distant sites. We have previously established the breast cancer patient-derived tumor xenograft (PDX) mouse model in which CSC marker CD44+ cancer cells formed spontaneous microscopic metastases in the liver. In this PDX mouse, the expression levels of S100A10 and its family proteins were much higher in the CD44+ cancer cells metastasized to the liver than those at the primary site. Knockdown of S100A10 in breast cancer cells suppressed and overexpression of S100A10 in breast cancer PDX cells enhanced their invasion abilities and 3D organoid formation capacities in vitro. Mechanistically, S100A10 regulated the matrix metalloproteinase activity and the expression levels of stem cell–related genes. Finally, constitutive knockdown of S100A10 significantly reduced their metastatic ability to the liver in vivo. These findings suggest that S100A10 functions as a metastasis promoter of breast CSCs by conferring both invasion ability and CSC properties in breast cancers.",

author = "Hisano Yanagi and Takashi Watanabe and Tatsunori Nishimura and Takanori Hayashi and Seishi Kono and Hitomi Tsuchida and Munetsugu Hirata and Yuko Kijima and Shintaro Takao and Seiji Okada and Motoshi Suzuki and Kazuyoshi Imaizumi and Kenji Kawada and Hironobu Minami and Noriko Gotoh and Yohei Shimono",

note = "Funding Information: We thank Drs. Masao Maeda (Fujita Health University, Japan), Atsushi Enomoto (Nagoya University, Japan), Hidemasa Goto (Mie University, Japan), Miki Nishio, Junko Mukohyama, Jyunji Otani, and Tomohiko Maehama (Kobe University, Japan) for their superior supports and discussions. This work was supported by grants from (1) the Japan Society for the Promotion of Science (JSPS KAKENHI) (15K14381, 18K07231, and Japan‐Belgium Research Cooperative Program to YS; 19K23900 and 20K07600 to TW), (2) the Princess Takamatsu Cancer Research Fund (to YS), (3) the Fujita Health University (to YS), (4) the Cancer Research Institute of Kanazawa University (to YS), and (5) the Promotion and Mutual Aid Corporation for Private Schools of Japan (to YS). ",

year = "2020",

month = dec,

doi = "10.1111/cas.14659",

language = "English",

volume = "111",

pages = "4359--4370",

journal = "Cancer Science",

issn = "1347-9032",

publisher = "Wiley-Blackwell",

number = "12",

}

Upregulation of S100A10 in metastasized breast cancer stem cells. / Yanagi, Hisano; Watanabe, Takashi; Nishimura, Tatsunori; Hayashi, Takanori; Kono, Seishi; Tsuchida, Hitomi; Hirata, Munetsugu ; Kijima, Yuko; Takao, Shintaro; Okada, Seiji; Suzuki, Motoshi ; Imaizumi, Kazuyoshi ; Kawada, Kenji; Minami, Hironobu; Gotoh, Noriko; Shimono, Yohei.

In: Cancer science, Vol. 111, No. 12, 12.2020, p. 4359-4370.

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

TY - JOUR

T1 - Upregulation of S100A10 in metastasized breast cancer stem cells

AU - Yanagi, Hisano

AU - Watanabe, Takashi

AU - Nishimura, Tatsunori

AU - Hayashi, Takanori

AU - Kono, Seishi

AU - Tsuchida, Hitomi

AU - Hirata, Munetsugu

AU - Kijima, Yuko

AU - Takao, Shintaro

AU - Okada, Seiji

AU - Suzuki, Motoshi

AU - Imaizumi, Kazuyoshi

AU - Kawada, Kenji

AU - Minami, Hironobu

AU - Gotoh, Noriko

AU - Shimono, Yohei

N1 - Funding Information: We thank Drs. Masao Maeda (Fujita Health University, Japan), Atsushi Enomoto (Nagoya University, Japan), Hidemasa Goto (Mie University, Japan), Miki Nishio, Junko Mukohyama, Jyunji Otani, and Tomohiko Maehama (Kobe University, Japan) for their superior supports and discussions. This work was supported by grants from (1) the Japan Society for the Promotion of Science (JSPS KAKENHI) (15K14381, 18K07231, and Japan‐Belgium Research Cooperative Program to YS; 19K23900 and 20K07600 to TW), (2) the Princess Takamatsu Cancer Research Fund (to YS), (3) the Fujita Health University (to YS), (4) the Cancer Research Institute of Kanazawa University (to YS), and (5) the Promotion and Mutual Aid Corporation for Private Schools of Japan (to YS).

PY - 2020/12

Y1 - 2020/12

N2 - Metastatic progression remains the major cause of death in human breast cancer. Cancer cells with cancer stem cell (CSC) properties drive initiation and growth of metastases at distant sites. We have previously established the breast cancer patient-derived tumor xenograft (PDX) mouse model in which CSC marker CD44+ cancer cells formed spontaneous microscopic metastases in the liver. In this PDX mouse, the expression levels of S100A10 and its family proteins were much higher in the CD44+ cancer cells metastasized to the liver than those at the primary site. Knockdown of S100A10 in breast cancer cells suppressed and overexpression of S100A10 in breast cancer PDX cells enhanced their invasion abilities and 3D organoid formation capacities in vitro. Mechanistically, S100A10 regulated the matrix metalloproteinase activity and the expression levels of stem cell–related genes. Finally, constitutive knockdown of S100A10 significantly reduced their metastatic ability to the liver in vivo. These findings suggest that S100A10 functions as a metastasis promoter of breast CSCs by conferring both invasion ability and CSC properties in breast cancers.

AB - Metastatic progression remains the major cause of death in human breast cancer. Cancer cells with cancer stem cell (CSC) properties drive initiation and growth of metastases at distant sites. We have previously established the breast cancer patient-derived tumor xenograft (PDX) mouse model in which CSC marker CD44+ cancer cells formed spontaneous microscopic metastases in the liver. In this PDX mouse, the expression levels of S100A10 and its family proteins were much higher in the CD44+ cancer cells metastasized to the liver than those at the primary site. Knockdown of S100A10 in breast cancer cells suppressed and overexpression of S100A10 in breast cancer PDX cells enhanced their invasion abilities and 3D organoid formation capacities in vitro. Mechanistically, S100A10 regulated the matrix metalloproteinase activity and the expression levels of stem cell–related genes. Finally, constitutive knockdown of S100A10 significantly reduced their metastatic ability to the liver in vivo. These findings suggest that S100A10 functions as a metastasis promoter of breast CSCs by conferring both invasion ability and CSC properties in breast cancers.

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