IMP dehydrogenase-2 drives aberrant nucleolar activity and promotes tumorigenesis in glioblastoma.


Journal

Nature cell biology
ISSN: 1476-4679
Titre abrégé: Nat Cell Biol
Pays: England
ID NLM: 100890575

Informations de publication

Date de publication:
08 2019
Historique:
received: 21 11 2018
accepted: 18 06 2019
entrez: 3 8 2019
pubmed: 3 8 2019
medline: 20 11 2019
Statut: ppublish

Résumé

In many cancers, high proliferation rates correlate with elevation of rRNA and tRNA levels, and nucleolar hypertrophy. However, the underlying mechanisms linking increased nucleolar transcription and tumorigenesis are only minimally understood. Here we show that IMP dehydrogenase-2 (IMPDH2), the rate-limiting enzyme for de novo guanine nucleotide biosynthesis, is overexpressed in the highly lethal brain cancer glioblastoma. This leads to increased rRNA and tRNA synthesis, stabilization of the nucleolar GTP-binding protein nucleostemin, and enlarged, malformed nucleoli. Pharmacological or genetic inactivation of IMPDH2 in glioblastoma reverses these effects and inhibits cell proliferation, whereas untransformed glia cells are unaffected by similar IMPDH2 perturbations. Impairment of IMPDH2 activity triggers nucleolar stress and growth arrest of glioblastoma cells even in the absence of functional p53. Our results reveal that upregulation of IMPDH2 is a prerequisite for the occurance of aberrant nucleolar function and increased anabolic processes in glioblastoma, which constitutes a primary event in gliomagenesis.

Identifiants

pubmed: 31371825
doi: 10.1038/s41556-019-0363-9
pii: 10.1038/s41556-019-0363-9
pmc: PMC6686884
mid: NIHMS1532281
doi:

Substances chimiques

RNA, Ribosomal 0
IMP Dehydrogenase EC 1.1.1.205
IMPDH2 protein, human EC 1.1.1.205

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1003-1014

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS102669
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS089815
Pays : United States
Organisme : NINDS NIH HHS
ID : R21 NS100077
Pays : United States
Organisme : NCI NIH HHS
ID : P50 CA211015
Pays : United States
Organisme : NCI NIH HHS
ID : P50 CA221747
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS073831
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS107071
Pays : United States

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Auteurs

Satoshi Kofuji (S)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.
Graduate School of Biomedical & Health Sciences, Hiroshima University, Hiroshima, Japan.

Akiyoshi Hirayama (A)

Institute for Advanced Biosciences, Keio University, Tsuruoka, Japan.

Alexander Otto Eberhardt (AO)

Institute of Biochemistry and Biophysics, Center for Molecular Biomedicine, Friedrich Schiller University Jena, Jena, Germany.
Leibniz-Institute on Aging-Fritz Lipmann Institute, Jena, Germany.

Risa Kawaguchi (R)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.
Artificial Intelligence Research Center, National Institute of Advanced Industrial Science and Technology, Tokyo, Japan.

Yuki Sugiura (Y)

Department of Biochemistry, Keio University School of Medicine, Tokyo, Japan.

Oltea Sampetrean (O)

Division of Gene Regulation, Institute for Advanced Medical Research, Keio University School of Medicine, Tokyo, Japan.

Yoshiki Ikeda (Y)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Mikako Warren (M)

Division of Pathology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Department of Pathology and Laboratory Medicine, Children's Hospital Los Angeles and Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.

Naoya Sakamoto (N)

Graduate School of Biomedical & Health Sciences, Hiroshima University, Hiroshima, Japan.

Shuji Kitahara (S)

Department of Anatomy and Developmental Biology, Tokyo Women's Medical University School of Medicine, Tokyo, Japan.

Hirofumi Yoshino (H)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Daisuke Yamashita (D)

Department of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL, USA.

Kazutaka Sumita (K)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Kara Wolfe (K)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Lisa Lange (L)

Institute of Biochemistry and Biophysics, Center for Molecular Biomedicine, Friedrich Schiller University Jena, Jena, Germany.
Leibniz-Institute on Aging-Fritz Lipmann Institute, Jena, Germany.

Satsuki Ikeda (S)

Institute for Advanced Biosciences, Keio University, Tsuruoka, Japan.

Hiroko Shimada (H)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Noriaki Minami (N)

Division of Gene Regulation, Institute for Advanced Medical Research, Keio University School of Medicine, Tokyo, Japan.

Akshiv Malhotra (A)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Shin Morioka (S)

Graduate School of Biomedical & Health Sciences, Hiroshima University, Hiroshima, Japan.

Yuki Ban (Y)

Graduate School of Biomedical & Health Sciences, Hiroshima University, Hiroshima, Japan.

Maya Asano (M)

Graduate School of Biomedical & Health Sciences, Hiroshima University, Hiroshima, Japan.

Victoria L Flanary (VL)

Department of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL, USA.

Annmarie Ramkissoon (A)

Cancer and Blood Diseases Institute, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.

Lionel M L Chow (LML)

Cancer and Blood Diseases Institute, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.

Juri Kiyokawa (J)

Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.

Tomoyuki Mashimo (T)

Department of Internal Medicine; Harold C. Simmons Comprehensive Cancer Center; Annette G. Strauss Center for Neuro-Oncology, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Greg Lucey (G)

Division of Neuropathology, Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA.

Sergey Mareninov (S)

Division of Neuropathology, Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA.

Tatsuya Ozawa (T)

Division of Human Biology, Solid Tumor and Translational Research, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.

Nobuyuki Onishi (N)

Division of Gene Regulation, Institute for Advanced Medical Research, Keio University School of Medicine, Tokyo, Japan.

Koichi Okumura (K)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Jumpei Terakawa (J)

Division of Transgenic Animal Science, Advanced Science Research Center, Kanazawa University, Kanazawa, Japan.

Takiko Daikoku (T)

Division of Transgenic Animal Science, Advanced Science Research Center, Kanazawa University, Kanazawa, Japan.

Trisha Wise-Draper (T)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Nazanin Majd (N)

Department of Neurology, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Kaori Kofuji (K)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Mika Sasaki (M)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Masaru Mori (M)

Institute for Advanced Biosciences, Keio University, Tsuruoka, Japan.

Yonehiro Kanemura (Y)

Department of Biomedical Research and Innovation, Institute for Clinical Research, National Hospital Organization Osaka National Hospital, Osaka, Japan.

Eric P Smith (EP)

Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA.

Dimitrios Anastasiou (D)

Cancer Metabolism Laboratory, The Francis Crick Institute, London, UK.

Hiroaki Wakimoto (H)

Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.

Eric C Holland (EC)

Division of Human Biology, Solid Tumor and Translational Research, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.

William H Yong (WH)

Division of Neuropathology, Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA.

Craig Horbinski (C)

Department of Pathology, University of Kentucky College of Medicine, Lexington, KY, USA.
Departments of Pathology and Neurosurgery, Northwestern University, Chicago, IL, USA.

Ichiro Nakano (I)

Department of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL, USA.

Ralph J DeBerardinis (RJ)

Howard Hughes Medical Institute; Children's Medical Center Research Institute; Department of Pediatrics and Eugene McDermott Center for Human Growth and Development, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Robert M Bachoo (RM)

Department of Internal Medicine; Harold C. Simmons Comprehensive Cancer Center; Annette G. Strauss Center for Neuro-Oncology, University of Texas Southwestern Medical Center, Dallas, TX, USA.
Department of Neurology and Neurotherapeutics, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Paul S Mischel (PS)

Ludwig Institute for Cancer Research; Department of Pathology; Moores Cancer Center, University of California San Diego School of Medicine, La Jolla, CA, USA.

Wataru Yasui (W)

Graduate School of Biomedical & Health Sciences, Hiroshima University, Hiroshima, Japan.

Makoto Suematsu (M)

Department of Biochemistry, Keio University School of Medicine, Tokyo, Japan.

Hideyuki Saya (H)

Division of Gene Regulation, Institute for Advanced Medical Research, Keio University School of Medicine, Tokyo, Japan.

Tomoyoshi Soga (T)

Institute for Advanced Biosciences, Keio University, Tsuruoka, Japan.
AMED-CREST, AMED, Tokyo, Japan.

Ingrid Grummt (I)

Division of Molecular Biology of the Cell II, German Cancer Research Center, DKFZ-ZMBH Alliance, Heidelberg, Germany.

Holger Bierhoff (H)

Institute of Biochemistry and Biophysics, Center for Molecular Biomedicine, Friedrich Schiller University Jena, Jena, Germany.
Leibniz-Institute on Aging-Fritz Lipmann Institute, Jena, Germany.

Atsuo T Sasaki (AT)

Division of Hematology and Oncology, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH, USA. atsuo.sasaki@uc.edu.
Institute for Advanced Biosciences, Keio University, Tsuruoka, Japan. atsuo.sasaki@uc.edu.
Department of Cancer Biology, University of Cincinnati College of Medicine, Cincinnati, OH, USA. atsuo.sasaki@uc.edu.
Department of Neurosurgery, Brain Tumor Center at UC Gardner Neuroscience Institute, Cincinnati, OH, USA. atsuo.sasaki@uc.edu.

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