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Malignant extracellular vesicles carrying MMP1 mRNA facilitate peritoneal dissemination in ovarian cancer

Author

Listed:
  • Akira Yokoi

    (National Cancer Center Research Institute
    Nagoya University Graduate School of Medicine)

  • Yusuke Yoshioka

    (National Cancer Center Research Institute)

  • Yusuke Yamamoto

    (National Cancer Center Research Institute)

  • Mitsuya Ishikawa

    (National Cancer Center Hospital)

  • Shun-ichi Ikeda

    (National Cancer Center Hospital)

  • Tomoyasu Kato

    (National Cancer Center Hospital)

  • Tohru Kiyono

    (National Cancer Center Research Institute)

  • Fumitaka Takeshita

    (Fundamental Innovative Oncology Core Center (FIOC), National Cancer Center Research Institute)

  • Hiroaki Kajiyama

    (Nagoya University Graduate School of Medicine)

  • Fumitaka Kikkawa

    (Nagoya University Graduate School of Medicine)

  • Takahiro Ochiya

    (National Cancer Center Research Institute)

Abstract

Advanced ovarian cancers are highly metastatic due to frequent peritoneal dissemination, resulting in dismal prognosis. Here we report the functions of cancer-derived extracellular vesicles (EVs), which are emerging as important mediators of tumour metastasis. The EVs from highly metastatic cells strongly induce metastatic behaviour in moderately metastatic tumours. Notably, the cancer EVs efficiently induce apoptotic cell death in human mesothelial cells in vitro and in vivo, thus resulting in the destruction of the peritoneal mesothelium barrier. Whole transcriptome analysis shows that MMP1 is significantly elevated in mesothelial cells treated with highly metastatic cancer EVs and intact MMP1 mRNAs are selectively packaged in the EVs. Importantly, MMP1 expression in ovarian cancer is tightly correlated with a poor prognosis. Moreover, MMP1 mRNA-carrying EVs exist in the ascites of cancer patients and these EVs also induce apoptosis in mesothelial cells. Our findings elucidate a previously unknown mechanism of peritoneal dissemination via EVs.

Suggested Citation

  • Akira Yokoi & Yusuke Yoshioka & Yusuke Yamamoto & Mitsuya Ishikawa & Shun-ichi Ikeda & Tomoyasu Kato & Tohru Kiyono & Fumitaka Takeshita & Hiroaki Kajiyama & Fumitaka Kikkawa & Takahiro Ochiya, 2017. "Malignant extracellular vesicles carrying MMP1 mRNA facilitate peritoneal dissemination in ovarian cancer," Nature Communications, Nature, vol. 8(1), pages 1-15, April.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms14470
    DOI: 10.1038/ncomms14470
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    Cited by:

    1. Zixiang Wang & Shourong Wang & Junchao Qin & Xiyu Zhang & Gang Lu & Hongbin Liu & Haiyang Guo & Ligang Wu & Victoria O. Shender & Changshun Shao & Beihua Kong & Zhaojian Liu, 2022. "Splicing factor BUD31 promotes ovarian cancer progression through sustaining the expression of anti-apoptotic BCL2L12," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Akira Yokoi & Kosuke Yoshida & Hirotaka Koga & Masami Kitagawa & Yukari Nagao & Mikiko Iida & Shota Kawaguchi & Min Zhang & Jun Nakayama & Yusuke Yamamoto & Yoshinobu Baba & Hiroaki Kajiyama & Takao Y, 2023. "Spatial exosome analysis using cellulose nanofiber sheets reveals the location heterogeneity of extracellular vesicles," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Z. L. Liu & X. Y. Meng & R. J. Bao & M. Y. Shen & J. J. Sun & W. D. Chen & F. Liu & Y. He, 2024. "Single cell deciphering of progression trajectories of the tumor ecosystem in head and neck cancer," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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