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Activity-Based Probe for Screening of High-Colibactin Producers from Clinical Samples

  • Yuichiro Hirayama
    Yuichiro Hirayama
    Department of Pharmaceutical Sciences, University of Shizuoka, Shizuoka 422-8526, Japan
  • Yuta Tsunematsu
    Yuta Tsunematsu
    Department of Pharmaceutical Sciences, University of Shizuoka, Shizuoka 422-8526, Japan
  • Yuko Yoshikawa
    Yuko Yoshikawa
    School of Veterinary Medicine, Faculty of Veterinary Science, Nippon Veterinary and Life Science University, Tokyo 180-8602, Japan
  • Ryota Tamafune
    Ryota Tamafune
    Department of Pharmaceutical Sciences, University of Shizuoka, Shizuoka 422-8526, Japan
  • Nobuo Matsuzaki
    Nobuo Matsuzaki
    Department of Pharmaceutical Sciences, University of Shizuoka, Shizuoka 422-8526, Japan
  • Yuji Iwashita
    Yuji Iwashita
    Department of Tumor Pathology, Hamamatsu University School of Medicine, Shizuoka 431-3192, Japan
  • Ippei Ohnishi
    Ippei Ohnishi
    Division of Pathology, Iwata City Hospital, Iwata 438-8550, Japan
  • Fumihiko Tanioka
    Fumihiko Tanioka
    Division of Pathology, Iwata City Hospital, Iwata 438-8550, Japan
  • Michio Sato
    Michio Sato
    Department of Pharmaceutical Sciences, University of Shizuoka, Shizuoka 422-8526, Japan
    More by Michio Sato
  • Noriyuki Miyoshi
    Noriyuki Miyoshi
    Graduate School of Nutritional and Environmental Sciences, University of Shizuoka, Shizuoka 422-8526, Japan
  • Michihiro Mutoh
    Michihiro Mutoh
    Epidemiology and Prevention Division, Center for Public Health Sciences, National Cancer Center, Tokyo 104-0045, Japan
  • Hideki Ishikawa
    Hideki Ishikawa
    Department of Molecular-Targeting Cancer Prevention, Kyoto Prefectural University of Medicine, Kyoto 602-8566, Japan
  • Haruhiko Sugimura
    Haruhiko Sugimura
    Department of Tumor Pathology, Hamamatsu University School of Medicine, Shizuoka 431-3192, Japan
  • Keiji Wakabayashi
    Keiji Wakabayashi
    Graduate Division of Nutritional and Environmental Sciences, University of Shizuoka, Shizuoka 422-8526, Japan
  • , and 
  • Kenji Watanabe*
    Kenji Watanabe
    Department of Pharmaceutical Sciences, University of Shizuoka, Shizuoka 422-8526, Japan
    *E-mail: [email protected]
Cite this: Org. Lett. 2019, 21, 12, 4490–4494
Publication Date (Web):June 13, 2019
https://doi.org/10.1021/acs.orglett.9b01345
Copyright © 2019 American Chemical Society

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    Abstract

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    While high-colibactin-producing Escherichia coli is thought to be associated with colorectal oncogenesis, this study is complicated part due to an inability to isolate colibactin adequately. Here, we created fluorescent probes activated by ClbP, the colibactin-maturing peptidase, to identify high-colibactin-producing strains. Our probe served as a valuable clinical diagnostic tool that allowed simple high-throughput diagnostic screening of clinical samples. Furthermore, the probe also allowed identification of high-colibactin producers that would help advance our understanding of colibactin biosynthesis.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.orglett.9b01345.

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    Cited By

    This article is cited by 16 publications.

    1. Yuichiro Hirayama, Michio Sato, Kenji Watanabe. Advancing the Biosynthetic and Chemical Understanding of the Carcinogenic Risk Factor Colibactin and Its Producers. Biochemistry 2022, 61 (24) , 2782-2790. https://doi.org/10.1021/acs.biochem.2c00229
    2. Tao Zhou, Yuichiro Hirayama, Yuta Tsunematsu, Nanami Suzuki, Seiji Tanaka, Nahoko Uchiyama, Yukihiro Goda, Yuko Yoshikawa, Yuji Iwashita, Michio Sato, Noriyuki Miyoshi, Michihiro Mutoh, Hideki Ishikawa, Haruhiko Sugimura, Keiji Wakabayashi, Kenji Watanabe. Isolation of New Colibactin Metabolites from Wild-Type Escherichia coli and In Situ Trapping of a Mature Colibactin Derivative. Journal of the American Chemical Society 2021, 143 (14) , 5526-5533. https://doi.org/10.1021/jacs.1c01495
    3. Tao Zhou, Takayuki Ando, Akihiro Kudo, Michio Sato, Noriyuki Miyoshi, Michihiro Mutoh, Hideki Ishikawa, Keiji Wakabayashi, Kenji Watanabe. Screening method toward ClbP-specific inhibitors. Genes and Environment 2023, 45 (1) https://doi.org/10.1186/s41021-023-00264-7
    4. José A. Velilla, Grace E. Kenney, Rachelle Gaudet. Structure and function of prodrug-activating peptidases. Biochimie 2023, 205 , 124-135. https://doi.org/10.1016/j.biochi.2022.07.019
    5. Walaa K. Mousa. The microbiome-product colibactin hits unique cellular targets mediating host–microbe interaction. Frontiers in Pharmacology 2022, 13 https://doi.org/10.3389/fphar.2022.958012
    6. Jian-Wei Tang, Xin Liu, Wei Ye, Zhong-Rui Li, Pei-Yuan Qian. Biosynthesis and bioactivities of microbial genotoxin colibactins. Natural Product Reports 2022, 39 (5) , 991-1014. https://doi.org/10.1039/D1NP00050K
    7. Yuichiro HIRAYAMA, Kenji WATANABE. Elucidation of the Complete Chemical Structure of Colibactin, a Carcinogenic Risk Factor Produced by E. coli:Detection and Structure Determination of Trace and Unstable Unknown Natural Products. KAGAKU TO SEIBUTSU 2022, 60 (3) , 123-130. https://doi.org/10.1271/kagakutoseibutsu.60.123
    8. Motoki Iwasaki, Rieko Kanehara, Taiki Yamaji, Ryoko Katagiri, Michihiro Mutoh, Yuta Tsunematsu, Michio Sato, Kenji Watanabe, Koji Hosomi, Yasuo Kakugawa, Hiroaki Ikematsu, Kinichi Hotta, Jun Kunisawa, Keiji Wakabayashi, Takahisa Matsuda. Association of Escherichia coli containing polyketide synthase in the gut microbiota with colorectal neoplasia in Japan. Cancer Science 2022, 113 (1) , 277-286. https://doi.org/10.1111/cas.15196
    9. Daiki Watanabe, Haruka Murakami, Harumi Ohno, Kumpei Tanisawa, Kana Konishi, Kikue Todoroki-Mori, Yuta Tsunematsu, Michio Sato, Yuji Ogata, Noriyuki Miyoshi, Naoto Kubota, Jun Kunisawa, Keiji Wakabayashi, Tetsuya Kubota, Kenji Watanabe, Motohiko Miyachi. Stool pattern is associated with not only the prevalence of tumorigenic bacteria isolated from fecal matter but also plasma and fecal fatty acids in healthy Japanese adults. BMC Microbiology 2021, 21 (1) https://doi.org/10.1186/s12866-021-02255-6
    10. Yuta Tsunematsu, Koji Hosomi, Jun Kunisawa, Michio Sato, Noriko Shibuya, Emiko Saito, Haruka Murakami, Yuko Yoshikawa, Yuji Iwashita, Noriyuki Miyoshi, Michihiro Mutoh, Hideki Ishikawa, Haruhiko Sugimura, Motohiko Miyachi, Keiji Wakabayashi, Kenji Watanabe. Mother-to-infant transmission of the carcinogenic colibactin-producing bacteria. BMC Microbiology 2021, 21 (1) https://doi.org/10.1186/s12866-021-02292-1
    11. Keita Kouzu, Hironori Tsujimoto, Yoji Kishi, Hideki Ueno, Nariyoshi Shinomiya. Role of Microbial Infection-Induced Inflammation in the Development of Gastrointestinal Cancers. Medicines 2021, 8 (8) , 45. https://doi.org/10.3390/medicines8080045
    12. Nicol Strakova, Kristyna Korena, Renata Karpiskova. Klebsiella pneumoniae producing bacterial toxin colibactin as a risk of colorectal cancer development - A systematic review. Toxicon 2021, 197 , 126-135. https://doi.org/10.1016/j.toxicon.2021.04.007
    13. Daiki Watanabe, Haruka Murakami, Harumi Ohno, Kumpei Tanisawa, Kana Konishi, Yuta Tsunematsu, Michio Sato, Noriyuki Miyoshi, Keiji Wakabayashi, Kenji Watanabe, Motohiko Miyachi. Association between dietary intake and the prevalence of tumourigenic bacteria in the gut microbiota of middle-aged Japanese adults. Scientific Reports 2020, 10 (1) https://doi.org/10.1038/s41598-020-72245-7
    14. Masanobu Kawanishi, Chiaki Shimohara, Yoshimitsu Oda, Yuuta Hisatomi, Yuta Tsunematsu, Michio Sato, Yuichiro Hirayama, Noriyuki Miyoshi, Yuji Iwashita, Yuko Yoshikawa, Haruhiko Sugimura, Michihiro Mutoh, Hideki Ishikawa, Keiji Wakabayashi, Takashi Yagi, Kenji Watanabe. Genotyping of a gene cluster for production of colibactin and in vitro genotoxicity analysis of Escherichia coli strains obtained from the Japan Collection of Microorganisms. Genes and Environment 2020, 42 (1) https://doi.org/10.1186/s41021-020-00149-z
    15. Yuko Yoshikawa, Yuta Tsunematsu, Nobuo Matsuzaki, Yuichiro Hirayama, Fumi Higashiguchi, Michio Sato, Yuji Iwashita, Noriyuki Miyoshi, Michihiro Mutoh, Hideki Ishikawa, Haruhiko Sugimura, Keiji Wakabayashi, Kenji Watanabe. Characterization of Colibactin-Producing Escherichia coli Isolated from Japanese Patients with Colorectal Cancer. Japanese Journal of Infectious Diseases 2020, 73 (6) , 437-442. https://doi.org/10.7883/yoken.JJID.2020.066
    16. Masanobu Kawanishi, Yuuta Hisatomi, Yoshimitsu Oda, Chiaki Shimohara, Yuta Tsunematsu, Michio Sato, Yuichiro Hirayama, Noriyuki Miyoshi, Yuji Iwashita, Yuko Yoshikawa, Haruhiko Sugimura, Michihiro Mutoh, Hideki Ishikawa, Keiji Wakabayashi, Takashi Yagi, Kenji Watanabe. In vitro genotoxicity analyses of colibactin-producing E. coli isolated from a Japanese colorectal cancer patient. The Journal of Toxicological Sciences 2019, 44 (12) , 871-876. https://doi.org/10.2131/jts.44.871

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