<i>NUDT15</i> variants confer high incidence of second malignancies in children with acute lymphoblastic leukemia

  • Masanori Yoshida
    Department of Pediatric Hematology and Oncology Research, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Kazuhiko Nakabayashi
    Department of Maternal-Fetal Biology, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Wentao Yang
    Department of Pharmacy and Pharmaceutical Sciences, St. Jude Children’s Research Hospital, Memphis, USA;
  • Aiko Sato-Otsubo
    Department of Pediatric Hematology and Oncology Research, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Shin-ichi Tsujimoto
    Department of Pediatric Hematology and Oncology Research, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Hiroko Ogata-Kawata
    Department of Maternal-Fetal Biology, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Tomoko Kawai
    Department of Maternal-Fetal Biology, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Keisuke Ishiwata
    Department of Maternal-Fetal Biology, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Mika Sakamoto
    Medical Genome Center, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Kohji Okamura
    Department of Systems BioMedicine, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Kaoru Yoshida
    Department of Pediatric Hematology and Oncology Research, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Ryota Shirai
    Department of Pediatric Hematology and Oncology Research, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Tomoo Osumi
    Department of Pediatric Hematology and Oncology Research, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Takaya Moriyama
    Department of Pharmacy and Pharmaceutical Sciences, St. Jude Children’s Research Hospital, Memphis, USA;
  • Rina Nishii
    Department of Pharmacy and Pharmaceutical Sciences, St. Jude Children’s Research Hospital, Memphis, USA;
  • Hiroyuki Takahashi
    Department of Pediatrics, Toho University, Tokyo, Japan;
  • Chikako Kiyotani
    Children’s Cancer Center, National Center for Child Health and Development, Tokyo, Japan;
  • Yoko Shioda
    Children’s Cancer Center, National Center for Child Health and Development, Tokyo, Japan;
  • Keita Terashima
    Children’s Cancer Center, National Center for Child Health and Development, Tokyo, Japan;
  • Sae Ishimaru
    Department of Hematology/Oncology, Tokyo Metropolitan Children’s Medical Center, Tokyo, Japan;
  • Yuki Yuza
    Department of Hematology/Oncology, Tokyo Metropolitan Children’s Medical Center, Tokyo, Japan;
  • Masatoshi Takagi
    Department of Pediatrics and Developmental Biology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, Japan;
  • Yuki Arakawa
    Department of Hematology/Oncology, Saitama Children’s Medical Center, Saitama, Japan;
  • Akitoshi Kinoshita
    Department of Pediatrics, St. Marianna University School of Medicine, Kawasaki, Japan;
  • Moeko Hino
    Department of Pediatrics, Chiba University Hospital, Chiba, Japan;
  • Toshihiko Imamura
    Department of Pediatrics, Kyoto Prefectural University of Medicine, Graduate School of Medical Science, Kyoto, Japan;
  • Daisuke Hasegawa
    Department of Pediatrics, St. Luke’s International Hospital, Tokyo, Japan;
  • Yozo Nakazawa
    Department of Pediatrics, Shinshu University School of Medicine, Matsumoto, Japan;
  • Mayuko Okuya
    Department of Pediatrics, Dokkyo Medical University School of Medicine, Shimotsuga, Japan;
  • Harumi Kakuda
    Department of Hematology/Oncology, Chiba Children’s Hospital, Chiba, Japan;
  • Nao Takasugi
    Department of Pediatrics, Graduate School of Medicine, the University of Tokyo, Tokyo, Japan;
  • Akiko Inoue
    Department of Pediatrics, Osaka Medical and Pharmaceutical University, Takatsuki, Japan;
  • Kentaro Ohki
    Department of Pediatric Hematology and Oncology Research, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Takako Yoshioka
    Department of Pathology, National Center for Child Health and Development, Tokyo, Japan;
  • Shuichi Ito
    Department of Pediatrics, Graduate School of Medicine, Yokohama City University, Yokohama, Japan;
  • Daisuke Tomizawa
    Children’s Cancer Center, National Center for Child Health and Development, Tokyo, Japan;
  • Katsuyoshi Koh
    Department of Hematology/Oncology, Saitama Children’s Medical Center, Saitama, Japan;
  • Kimikazu Matsumoto
    Children’s Cancer Center, National Center for Child Health and Development, Tokyo, Japan;
  • Masashi Sanada
    Clinical Research Center, National Hospital Organization Nagoya Medical Center, Nagoya, Japan;
  • Nobutaka Kiyokawa
    Department of Pediatric Hematology and Oncology Research, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Akira Ohara
    Department of Pediatrics, Toho University, Tokyo, Japan;
  • Seishi Ogawa
    Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan;
  • Atsushi Manabe
    Department of Pediatrics, Hokkaido University Graduate School of Medicine, Sapporo, Japan;
  • Akira Niwa
    Department of Clinical Application, Center for iPS Cell Research and Application, Kyoto University, Kyoto, Japan; and
  • Kenichiro Hata
    Department of Maternal-Fetal Biology, Research Institute, National Center for Child Health and Development, Tokyo, Japan;
  • Jun J. Yang
    Department of Oncology, St. Jude Children’s Research Hospital, Memphis, USA
  • Motohiro Kato
    Department of Pediatric Hematology and Oncology Research, Research Institute, National Center for Child Health and Development, Tokyo, Japan;

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<jats:title>Abstract</jats:title> <jats:p>The effect of genetic variation on second malignant neoplasms (SMNs) remains unclear. First, we identified the pathogenic germline variants in cancer-predisposing genes among 15 children with SMNs after childhood leukemia/lymphoma using whole-exome sequencing. Because the prevalence was low, we focused on the association between SMNs and NUDT15 in primary acute lymphoblastic leukemia (ALL) cases. NUDT15 is one of the 6-mercaptopurine (6-MP) metabolic genes, and its variants are common in East Asian individuals. The prevalence of NUDT15 hypomorphic variants was higher in patients with SMNs (n = 14; 42.9%) than in the general population in the gnomAD database (19.7%; P = .042). In the validation study with a cohort of 438 unselected patients with ALL, the cumulative incidence of SMNs was significantly higher among those with (3.0%; 95% confidence interval [CI], 0.6% to 9.4%) than among those without NUDT15 variants (0.3%; 95% CI, 0.0% to 1.5%; P = .045). The 6-MP dose administered to patients with ALL with a NUDT15 variant was higher than that given to those without SMNs (P = .045). The 6-MP–related mutational signature was observed in SMN specimens after 6-MP exposure. In cells exposed to 6-MP, a higher level of 6-MP induced DNA damage in NUDT15-knockdown induced pluripotent stem cells. Our study indicates that NUDT15 variants may confer a risk of SMNs after treatment with 6-MP in patients with ALL.</jats:p>

収録刊行物

  • Blood Advances

    Blood Advances 5 (23), 5420-5428, 2021-12-13

    American Society of Hematology

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