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Research Brief

Histone H3.3 Mutations Drive Pediatric Glioblastoma through Upregulation of MYCN

Lynn Bjerke, Alan Mackay, Meera Nandhabalan, Anna Burford, Alexa Jury, Sergey Popov, Dorine A. Bax, Diana Carvalho, Kathryn R. Taylor, Maria Vinci, Ilirjana Bajrami, Imelda M. McGonnell, Christopher J. Lord, Rui M. Reis, Darren Hargrave, Alan Ashworth, Paul Workman and Chris Jones
Lynn Bjerke
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Alan Mackay
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Meera Nandhabalan
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Anna Burford
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Alexa Jury
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Sergey Popov
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Dorine A. Bax
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Diana Carvalho
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Kathryn R. Taylor
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Maria Vinci
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Ilirjana Bajrami
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Imelda M. McGonnell
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Christopher J. Lord
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Rui M. Reis
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Darren Hargrave
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Alan Ashworth
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Paul Workman
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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Chris Jones
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
1Divisions of Molecular Pathology and 2Cancer Therapeutics, and 3Breakthrough Breast Cancer Research Centre and CRUK Gene Function Laboratory, Division of Breast Cancer Research, The Institute of Cancer Research; 4Royal Veterinary College; 5Great Ormond Street Hospital, London, United Kingdom; 6University of Coimbra, Coimbra; 7ICVS, University of Minho, Braga, Portugal; and 8Molecular Oncology Research Center, Barretos Cancer Hospital, Barretos SP, Brazil
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DOI: 10.1158/2159-8290.CD-12-0426 Published May 2013
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Abstract

Children and young adults with glioblastoma (GBM) have a median survival rate of only 12 to 15 months, and these GBMs are clinically and biologically distinct from histologically similar cancers in older adults. They are defined by highly specific mutations in the gene encoding the histone H3.3 variant H3F3A, occurring either at or close to key residues marked by methylation for regulation of transcription—K27 and G34. Here, we show that the cerebral hemisphere-specific G34 mutation drives a distinct expression signature through differential genomic binding of the K36 trimethylation mark (H3K36me3). The transcriptional program induced recapitulates that of the developing forebrain, and involves numerous markers of stem-cell maintenance, cell-fate decisions, and self-renewal. Critically, H3F3A G34 mutations cause profound upregulation of MYCN, a potent oncogene that is causative of GBMs when expressed in the correct developmental context. This driving aberration is selectively targetable in this patient population through inhibiting kinases responsible for stabilization of the protein.

Significance: We provide the mechanistic explanation for how the first histone gene mutation in human disease biology acts to deliver MYCN, a potent tumorigenic initiator, into a stem-cell compartment of the developing forebrain, selectively giving rise to incurable cerebral hemispheric GBM. Using synthetic lethal approaches to these mutant tumor cells provides a rational way to develop novel and highly selective treatment strategies. Cancer Discov; 3(5); 512–19. ©2013 AACR.

See related commentary by Huang and Weiss, p. 484

This article is highlighted in the In This Issue feature, p. 471

Footnotes

  • Note: Supplementary data for this article are available at Cancer Discovery Online (http://cancerdiscovery.aacrjournals.org/).

  • Received September 20, 2012.
  • Revision received January 25, 2013.
  • Accepted January 28, 2013.
  • ©2013 American Association for Cancer Research.
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Cancer Discovery: 3 (5)
May 2013
Volume 3, Issue 5
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Histone H3.3 Mutations Drive Pediatric Glioblastoma through Upregulation of MYCN
Lynn Bjerke, Alan Mackay, Meera Nandhabalan, Anna Burford, Alexa Jury, Sergey Popov, Dorine A. Bax, Diana Carvalho, Kathryn R. Taylor, Maria Vinci, Ilirjana Bajrami, Imelda M. McGonnell, Christopher J. Lord, Rui M. Reis, Darren Hargrave, Alan Ashworth, Paul Workman and Chris Jones
Cancer Discov May 1 2013 (3) (5) 512-519; DOI: 10.1158/2159-8290.CD-12-0426

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Histone H3.3 Mutations Drive Pediatric Glioblastoma through Upregulation of MYCN
Lynn Bjerke, Alan Mackay, Meera Nandhabalan, Anna Burford, Alexa Jury, Sergey Popov, Dorine A. Bax, Diana Carvalho, Kathryn R. Taylor, Maria Vinci, Ilirjana Bajrami, Imelda M. McGonnell, Christopher J. Lord, Rui M. Reis, Darren Hargrave, Alan Ashworth, Paul Workman and Chris Jones
Cancer Discov May 1 2013 (3) (5) 512-519; DOI: 10.1158/2159-8290.CD-12-0426
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