Mechanism of leukaemia pathogenesis by gain-of-function mutations in microRNA miR-142.

• Project/Area Number: 23K21285
• Project/Area Number (Other): 21H02391 (2021-2023)
• Research Category: Grant-in-Aid for Scientific Research (B)
• Allocation Type: Multi-year Fund (2024); Single-year Grants (2021-2023)
• Section: 一般
• Review Section: Basic Section 42040:Laboratory animal science-related
• Research Institution: Kumamoto University
• Principal Investigator: Araki Kimi 熊本大学, 生命資源研究・支援センター, 教授 (90211705)
• Co-Investigator(Kenkyū-buntansha): 吉信 公美子 熊本大学, 生命資源研究・支援センター, 助教 (20274730) ; 要 匡 国立研究開発法人国立成育医療研究センター, ゲノム医療研究部, 部長 (40264288) ; 高橋 智 筑波大学, 医学医療系, 教授 (50271896) ; 指田 吾郎 熊本大学, 国際先端医学研究機構, 特定事業教員(教授) (70349447) ; 荒木 正健 熊本大学, 生命資源研究・支援センター, 特任准教授 (80271609)
• Project Period (FY): 2024-04-01 – 2025-03-31
• Project Status: Completed (Fiscal Year 2024)
• Budget Amount: ¥17,290,000 (Direct Cost: ¥13,300,000、Indirect Cost: ¥3,990,000); Fiscal Year 2024: ¥3,510,000 (Direct Cost: ¥2,700,000、Indirect Cost: ¥810,000); Fiscal Year 2023: ¥3,770,000 (Direct Cost: ¥2,900,000、Indirect Cost: ¥870,000); Fiscal Year 2022: ¥4,290,000 (Direct Cost: ¥3,300,000、Indirect Cost: ¥990,000); Fiscal Year 2021: ¥5,720,000 (Direct Cost: ¥4,400,000、Indirect Cost: ¥1,320,000)
• Keywords: マイクロRNA / 機能獲得型遺伝子変異 / 白血病 / 遺伝子変異 / 機能獲得方変異

Outline of Research at the Start

マイクロRNA (miRNA) は、8塩基程度のシード配列がターゲット遺伝子と結合することでその遺伝子の発現を制御する小さいRNA分子である。発がんでは、多くの遺伝子に変異が見られるが、miRNAの変異が直接発癌に関わる報告はまだない。我々は、ヒトの成人急性白血病で発見されたmiRNAの変異をマウスに導入すると、白血病を発症することを見出した。この変異miRNAが、多段階で発癌へと至るどの時期に、どのような他のがん遺伝子と協調して白血病の発症へ導くのかを解明する。

Outline of Final Research Achievements

MicroRNAs (miRNAs) are small RNA molecules that bind to target mRNAs and regulate their expression. Although there have been many reports of miRNAs showing altered expression during carcinogenic processes, there are no reports of miRNA mutations directly causing carcinogenesis. miR-142 is a miRNA expressed mainly in the haematopoietic system and its sequence is 100% identical in mice and humans. We generated mice with a point mutation (A55G) in the seed region of miRNA-142-3p, reported in patients with acute myeloid leukaemia, and found that the mutated blood cells cause T-cell leukaemia. We also found that simultaneous introduction of an Idh2 mutation resulted in myeloid leukaemia, which is more similar to the human condition.

Academic Significance and Societal Importance of the Research Achievements

これまでに様々ながん細胞においてmiRNAの一塩基変異の発生が報告されているが、それらではmiRNAの発現変動のみを解析しており、現在までに直接がん化を誘導するmiRNAの遺伝子変異については報告がない。我々の作製したmiR-142点変異マウスでは、野生型miR-142が減少したことによる従来の標的遺伝子の発現上昇と、変異型miR-142によって新たに標的となった遺伝子の発現抑制の両方が起こることで、血球の分化異常をきたし白血病を発症することが明らかになった。
本研究は、miRNAにはseed配列の一塩基変異のみでがんが誘導される機能獲得型変異が存在することを証明する世界初の報告である。

Research Products

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  • Author(s): Zhu Xingliang、Joo Yuyoung、Bossi Simone、McDevitt Ross A.、Xie Aoji、Wang Yue、Xue Yutong、Su Shuaikun、Lee Seung Kyu、Sah Nirnath、Zhang Shiliang、Ye Rong、Pinto Alejandro、Zhang Yongqing、Araki Kimi、Araki Masatake、Morales Marisela、Mattson Mark P.、van Praag Henriette、Wang Weidong
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  • Journal Title: Biology of Reproduction Volume: 110 Issue: 4 Pages: 750-760
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  • Journal Title: Journal of Investigative Dermatology Volume: - Issue: 8 Pages: 1890-1893
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  • Journal Title: Proceedings of the National Academy of Sciences Volume: 121 Issue: 13
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• [Journal Article] Atypical heat shock transcription factor HSF5 is critical for male meiotic prophase under non-stress conditions (2024)
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• [Journal Article] TIF1β activates leukemic transcriptional program in HSCs and promotes BCR::ABL1-induced myeloid leukemia (2024)
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  • Journal Title: Leukemia Volume: 38 Issue: 6 Pages: 1275-1286
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• [Journal Article] Chromatin modifier Hmga2 promotes adult hematopoietic stem cell function and blood regeneration in stress conditions (2024)
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  • Journal Title: The EMBO Journal Volume: 43 Issue: 13 Pages: 2661-2684
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  • Journal Title: Nucleic acids research Volume: 52 Issue: 15 Pages: 9230-9246
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• [Journal Article] Hepatic SerpinA1 improves energy and glucose metabolism through regulation of preadipocyte proliferation and UCP1 expression (2024)
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• [Journal Article] A gain‐of‐function mutation in microRNA-142 is sufficient to cause the development of T‐cell leukemia in mice. (2023)
  • Author(s): Kawano Shingo、Araki Kimi、Bai Jie、Furukawa Imari、Tateishi Keigo、Yoshinobu Kumiko、Usuki Shingo、Nimmo Rachael A.、Kaname Tadashi、Yoshihara Masaharu、Takahashi Satoru、Sashida Goro、Araki Masatake
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• [Journal Article] Tmem161a regulates bone formation and bone strength through the P38 MAPK pathway (2023)
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• [Journal Article] Fibroblast growth factor 18 stimulates the proliferation of hepatic stellate cells, thereby inducing liver fibrosis (2023)
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  • Journal Title: Molecular Cell Volume: 83 Issue: 24 Pages: 4479-4493
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• [Journal Article] EPLINβ Is Involved in the Assembly of Cadherin-catenin Complexes in Osteoblasts and Affects Bone Formation (2022)
  • Author(s): Miyazaki Shihoko、Funamoto Taro、Sekimoto Tomohisa、Kurogi Syuji、Ohta Tomomi、Nagai Takuya、Tajima Takuya、Imasaka Mai、Yoshinobu Kumiko、Araki Kimi、Araki Masatake、Choijookhuu Narantsog、Hishikawa Yoshitaka、Chosa Etsuo
  • Journal Title: ACTA HISTOCHEMICA ET CYTOCHEMICA Volume: 55 Issue: 3 Pages: 99-110
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  • Year and Date: 2022-06-29
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• [Journal Article] Generation of transgenic mice expressing a FRET biosensor, SMART, that responds to necroptosis (2022)
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  • Journal Title: Communications Biology Volume: 5 Issue: 1 Pages: 1331-1331
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• [Journal Article] Independent origins of fetal liver haematopoietic stem and progenitor cells (2022)
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  • Journal Title: Nature Volume: 609 Issue: 7928 Pages: 779-784
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• [Journal Article] IκBζ controls IL-17-triggered gene expression program in intestinal epithelial cells that restricts colonization of SFB and prevents Th17-associated pathologies (2022)
  • Author(s): Yamazaki Soh、Inohara Naohiro、Ohmuraya Masaki、Tsuneoka Yousuke、Yagita Hideo、Katagiri Takaharu、Nishina Takashi、Mikami Tetuo、Funato Hiromasa、Araki Kimi、Nakano Hiroyasu
  • Journal Title: Mucosal Immunology Volume: 15 Issue: 6 Pages: 1321-1337
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• [Journal Article] The polyol pathway is an evolutionarily conserved system for sensing glucose uptake. (2022)
  • Author(s): *Sano, H., Nakamura, A., Yamane, M., Niwa, H., Nishimura, T., Takemoto, K., Ishiguro, K., Aoki, H., Kato, Y., and Kojima, M.
  • Journal Title: PLOS Biology Volume: 20 Issue: 6 Pages: 1-25
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• [Journal Article] Thalamocortical axons control the cytoarchitecture of neocortical layers by area-specific supply of VGF (2022)
  • Author(s): Sato Haruka、Hatakeyama Jun、Iwasato Takuji、Araki Kimi、Yamamoto Nobuhiko、Shimamura Kenji
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• [Journal Article] Resistance to chemical carcinogenesis induction via a dampened inflammatory response in naked mole-rats (2022)
  • Author(s): Oka K, Fujioka S, Kawamura Y, Komohara Y, Chujo T, Sekiguchi K, Yamamura Y, Oiwa Y, Omamiuda-Ishikawa N, Komaki S, Sutoh Y, Sakurai S, Tomizawa K, Bono H, Shimizu A, Araki K, Yamamoto T, Yamada Y, Oshiumi H, Miura K.
  • Journal Title: Communications Biology Volume: 5 Issue: 1 Pages: 287-287
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• [Journal Article] FBXO47 is essential for preventing the synaptonemal complex from premature disassembly in mouse male meiosis (2022)
  • Author(s): Tanno N, Takemoto K, Takada-Horisawa Y, Shimada R., Fujimura S, Tani N., Takeda N., Araki K, Ishiguro K
  • Journal Title: iScience Volume: 25 Issue: 4 Pages: 104008-104008
  • DOI: 10.1016/j.isci.2022.104008
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• [Journal Article] Functional Polymorphism in Pak1?3′ Untranslated Region Alters Skin Tumor Susceptibility by Alternative Polyadenylation (2022)
  • Author(s): Okumura Kazuhiro、Saito Megumi、Isogai Eriko、Tokunaga Yurika、Hasegawa Yoshinori、Araki Kimi、Wakabayashi Yuichi
  • Journal Title: Journal of Investigative Dermatology Volume: XXX Issue: 9 Pages: 2323-2333
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• [Journal Article] The acidic domain of Hmga2 and the domain's linker region are critical for driving self-renewal of hematopoietic stem cell. (2022)
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  • DOI: 10.1007/s12185-021-03274-9
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• [Journal Article] MicroRNA-142 Critically Regulates Group 2 Innate Lymphoid Cell Homeostasis and Function (2021)
  • Author(s): Roberts Luke B.、Jowett Geraldine M.、Read Emily、Zabinski Tomas、Berkachy Rita、Selkirk Murray E.、Jackson Ian、Niazi Umar、Anandagoda Nelomi、Araki Masatake、Araki Kimi、Kasturiarachchi Jagath、James Chela、Enver Tariq、Nimmo Rachael、Reis Rita、Howard Jane K.、Neves Joana F.、Lord Graham M.
  • Journal Title: The Journal of Immunology Volume: 206 Issue: 11 Pages: 2725-2739
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• [Journal Article] RUNX1-ETO (RUNX1-RUNX1T1) induces myeloid leukemia in mice in an age-dependent manner (2021)
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  • Author(s): Takeda Iyo、Araki Masatake、Ishiguro Kei‐ichiro、Ohga Toshinori、Takada Kouki、Yamaguchi Yusuke、Hashimoto Koichi、Kai Takuma、Nakagata Naomi、Imasaka Mai、Yoshinobu Kumiko、Araki Kimi
  • Journal Title: Genes to Cells Volume: 26 Issue: 11 Pages: 874-890
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• [Journal Article] LincRNA‐p21 exon 1 expression correlates with Cdkn1a expression in vivo (2021)
  • Author(s): Furuhata, R., Imasaka, M., Sugimoto, M., Yoshinobu, K., Araki, M., Araki, K.
  • Journal Title: Genes to Cells Volume: 27 Issue: 1 Pages: 14-24
  • DOI: 10.1111/gtc.12906
  • Peer Reviewed
• [Presentation] マウスゲノムにおいて外来遺伝子発現に適した新たなSafe harborの探索と置換システムの構築 (2024)
  • Author(s): 徳安 碧、古畑 理樹、吉信 公美子、荒木 正健、荒木 喜美
  • Organizer: 第71回日本実験動物学会総会
• [Presentation] 精巣上体で発現するPateファミリー遺伝子が協調して精子成熟をサポートする (2024)
  • Author(s): 篠原 日菜 、平 歩夢 、荒木 喜美 、伊川 正人 、野田 大地
  • Organizer: 第71回日本実験動物学会総会
• [Presentation] Danforth's short tail マウスにおいて異所性発現を誘導するエンハンサー領域の解析 (2024)
  • Author(s): 徳安碧 , 松羅由香 , 杉本道彦 , 荒木正健 , 荒木喜美
  • Organizer: 日本遺伝学会第96回大会
• [Presentation] グルタル酸血症 2 型モ デルマウスの作製および薬剤投与による病態改善の試み (2024)
  • Author(s): 篠原涼介 ,上戸佳那 , 大平恵里花 ,立石圭冴 ,吉信公美子 ,松本志郎 ,荒木喜美 ,荒木正健
  • Organizer: 日本遺伝学会第96回大会
• [Presentation] miRNA-142の機能獲得型点変異による白血病発症について (2024)
  • Author(s): 荒木正健 河野慎吾 吉信公美子 要 匡 吉原雅大 高橋智 白潔 指田吾郎 荒木喜美
  • Organizer: 先端モデル動物支援プラットフォーム成果発表会
• [Presentation] マウス ES 細胞における KRAB-ZFPs クラスター領域欠損 ES 細胞株の樹立と解析 (2023)
  • Author(s): 米盛 匠海 ,平山 愛理 ,徳安 碧 ,吉信 公美子 ,荒木 正健 ,荒木 喜美
  • Organizer: 日本遺伝学会第95回大会
• [Presentation] Danforth’s short tail (Sd)マウスではレトロトランスポゾン挿入が近隣エンハンサー活性を変化させている (2023)
  • Author(s): 荒木喜美 德安碧 平山愛理 仙波圭 荒木正健
  • Organizer: 第46回日本分子生物学会年会
  • Invited
• [Presentation] マウスゲノムにおいて外来遺伝子発現に適した新たなSafe Harborの探索と置換システムの構築 (2023)
  • Author(s): 德安碧 古畑理樹 吉信公美子 荒木正健 荒木喜美
  • Organizer: 第46回日本分子生物学会年会
• [Presentation] Trap clone accumulated area (TCAA) may be involved in the maintenance of pluripotency of mouse ES cells. (2023)
  • Author(s): Masatake Araki, Keika Saitou, Runa Ikeda, Kumiko Yoshinobu, Mariko Yamane, Hitoshi Niwa, Kimi Araki
  • Organizer: 36th International Mammalian Genome Conference
  • Int'l Joint Research
• [Presentation] Dysregulation of the autoregulatory enhancer region cause ectopic expression of Ptf1a in Danforth's short tail (Sd) mice. (2023)
  • Author(s): Midori Tokuyasu, Airi Hirayama, Takumi Yonemori, Michihiko Sugimoto, Masatake Araki, Kimi Araki
  • Organizer: 36th International Mammalian Genome Conference
  • Int'l Joint Research
• [Presentation] microRNA-142の機能獲得型変異による白血病発症メカニズムの解析 (2022)
  • Author(s): 河野慎吾、荒木正健、荒木喜美、指田吾郎
  • Organizer: 第81回日本癌学会学術総会
• [Presentation] KRAB-ZFPsクラスターはマウス亜種間ハイブリッドES細胞の樹立効率と転移因子発現に影響する (2022)
  • Author(s): 平山愛理、徳安碧、吉信公美子、荒木正健、荒木喜美
  • Organizer: 日本遺伝学会第94回大会
• [Presentation] マウスゲノムにおいて外来遺伝子発現に適した新たなSafe Harborの探索と痴漢システムの構築 (2022)
  • Author(s): 徳安碧、古畑理樹、吉信公美子、荒木正健、荒木喜美
  • Organizer: 日本遺伝学会第94回大会
• [Presentation] マウスゲノムにおいて遺伝子は無いのに遺伝子トラップクローンが集積している領域（TCAA）の機能解析 (2022)
  • Author(s): 荒木正健、池田琉那、齋藤桂花、久場兼裕、北元優梨、吉信公美子、山根万里子、丹羽仁史、荒木喜美
  • Organizer: 日本遺伝学会第94回大会
• [Presentation] miR-142の機能獲得型変異による白血病発症メカニズムの解析 (2022)
  • Author(s): 河野慎吾、白潔、指田吾郎、古河いまり、吉信公美子、北元優梨、高橋智、要匡、荒木喜美、荒木正健
  • Organizer: 第69回日本実験動物学会総会
• [Presentation] ゲノム編集を用いた2-3MbにもわたるKRAB-ZFPクラスター領域の欠損アレルの作製 (2021)
  • Author(s): 荒木喜美、吉信公美子、荒木正健
  • Organizer: 日本ゲノム編集学会
• [Presentation] LincRNA-p21遺伝子領域における転写は隣接するCdkn1aの転写活性化に重要である。 (2021)
  • Author(s): 古畑理樹、今坂舞、荒木正健、吉信公美子、荒木喜美
  • Organizer: 日本遺伝学会
• [Remarks] 生命資源研究・支援センター 疾患モデル分野
  • URL: https://irda-genetics.kuma-u.jp/
• [Remarks] 熊本大学 生命資源研究・支援センター 疾患モデル分野
  • URL: http://irda-genetics.kuma-u.jp/index.html
• [Remarks] 生命資源研究・支援センター 疾患モデル分野
  • URL: http://irda-genetics.kuma-u.jp/