Home LiteratureArticle Details
PMID: 22389665 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mesenchymal transition and PDGFRA amplification/mutation are key distinct oncogenic events in pediatric diffuse intrinsic pontine gliomas.

PloS one ·Vol. 7 ·No. 2 ·2012-00-00 ·Pages e30313

Puget S, Philippe C, Bax DA, Job B, Varlet P, Junier MP, Andreiuolo F, Carvalho D, Reis R, Guerrini-Rousseau L, Roujeau T, Dessen P, Richon C, Lazar V, Le Teuff G, Sainte-Rose C, Geoerger B, Vassal G, Jones C, Grill J

Abstract

Diffuse intrinsic pontine glioma (DIPG) is one of the most frequent malignant pediatric brain tumor and its prognosis is universaly fatal. No significant improvement has been made in last thirty years over the standard treatment with radiotherapy. To address the paucity of understanding of DIPGs, we have carried out integrated molecular profiling of a large series of samples obtained with stereotactic biopsy at diagnosis. While chromosomal imbalances did not distinguish DIPG and supratentorial tumors on CGHarrays, gene expression profiling revealed clear differences between them, with brainstem gliomas resembling midline/thalamic tumours, indicating a closely-related origin. Two distinct subgroups of DIPG were identified. The first subgroup displayed mesenchymal and pro-angiogenic characteristics, with stem cell markers enrichment consistent with the possibility to grow tumor stem cells from these biopsies. The other subgroup displayed oligodendroglial features, and appeared largely driven by PDGFRA, in particular through amplification and/or novel missense mutations in the extracellular domain. Patients in this later group had a significantly worse outcome with an hazard ratio for early deaths, ie before 10 months, 8 fold greater that the ones in the other subgroup (p = 0.041, Cox regression model). The worse outcome of patients with the oligodendroglial type of tumors was confirmed on a series of 55 paraffin-embedded biopsy samples at diagnosis (median OS of 7.73 versus 12.37 months, p = 0.045, log-rank test). Two distinct transcriptional subclasses of DIPG with specific genomic alterations can be defined at diagnosis by oligodendroglial differentiation or mesenchymal transition, respectively. Classifying these tumors by signal transduction pathway activation and by mutation in pathway member genes may be particularily valuable for the development of targeted therapies.

MeSH Terms
Brain Stem Neoplasms/genetics,metabolism,pathology Epithelial-Mesenchymal Transition/genetics Gene Expression Profiling/methods Humans Immunohistochemistry In Vitro Techniques Mutation Receptor, Platelet-Derived Growth Factor alpha/genetics,metabolism Signal Transduction/genetics Snail Family Transcription Factors Transcription Factors/genetics,metabolism
Chemicals
Snail Family Transcription Factors Transcription Factors Receptor, Platelet-Derived Growth Factor alpha
Authors & Affiliations
20 authors, click to expand affiliations / ORCID
Puget Stephanie
Department of Neurosurgery, Necker-Sick Children Hospital, University Paris V Descartes, Paris, France.
Philippe Cathy
Bax Dorine A
Job Bastien
Varlet Pascale
Junier Marie-Pierre
Andreiuolo Felipe
Carvalho Dina
Reis Ricardo
Guerrini-Rousseau Lea
Roujeau Thomas
Dessen Philippe
Richon Catherine
Lazar Vladimir
Le Teuff Gwenael
Sainte-Rose Christian
Geoerger Birgit
Vassal Gilles
Jones Chris
Grill Jacques
References (78)
78 references, click to expand
  1. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies.
    Science. 2007 Oct 12;318(5848):287-90 PMID: 17872411
  2. Magnetic resonance scans should replace biopsies for the diagnosis of diffuse brain stem gliomas: a report from the Children's Cancer Group.
    Neurosurgery. 1993 Dec;33(6):1026-9; discussion 1029-30 PMID: 8133987
  3. Stereotactic biopsy of diffuse pontine lesions in children.
    J Neurosurg. 2007 Jul;107(1 Suppl):1-4 PMID: 17647306
  4. STAC: A method for testing the significance of DNA copy number aberrations across multiple array-CGH experiments.
    Genome Res. 2006 Sep;16(9):1149-58 PMID: 16899652
  5. Clinical relevance of tumor cells with stem-like properties in pediatric brain tumors.
    PLoS One. 2011 Jan 28;6(1):e16375 PMID: 21297991
  6. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response.
    Nature. 2006 Dec 7;444(7120):756-60 PMID: 17051156
  7. ERBB1 is amplified and overexpressed in high-grade diffusely infiltrative pediatric brain stem glioma.
    Clin Cancer Res. 2003 Sep 1;9(10 Pt 1):3620-4 PMID: 14506149
  8. Hedgehog-responsive candidate cell of origin for diffuse intrinsic pontine glioma.
    Proc Natl Acad Sci U S A. 2011 Mar 15;108(11):4453-8 PMID: 21368213
  9. Intratumoral concentrations of imatinib after oral administration in patients with glioblastoma multiforme.
    J Neurooncol. 2010 Apr;97(2):241-5 PMID: 19768386
  10. Sox10 has a broad expression pattern in gliomas and enhances platelet-derived growth factor-B--induced gliomagenesis.
    Mol Cancer Res. 2007 Sep;5(9):891-7 PMID: 17855658
  11. Anaplastic oligodendrogliomas with 1p19q codeletion have a proneural gene expression profile.
    Mol Cancer. 2008 May 20;7:41 PMID: 18492260
  12. Radial glia cells are candidate stem cells of ependymoma.
    Cancer Cell. 2005 Oct;8(4):323-35 PMID: 16226707
  13. Advances toward an understanding of brainstem gliomas.
    J Clin Oncol. 2006 Mar 10;24(8):1266-72 PMID: 16525181
  14. Expression profiling of ependymomas unravels localization and tumor grade-specific tumorigenesis.
    Cancer. 2009 Sep 1;115(17):3955-68 PMID: 19536879
  15. Molecular properties of CD133+ glioblastoma stem cells derived from treatment-refractory recurrent brain tumors.
    J Neurooncol. 2009 Aug;94(1):1-19 PMID: 19468690
  16. Gene expression profiling of gliomas strongly predicts survival.
    Cancer Res. 2004 Sep 15;64(18):6503-10 PMID: 15374961
  17. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1.
    Cancer Cell. 2010 Jan 19;17(1):98-110 PMID: 20129251
  18. Thalamic tumors in children: a reappraisal.
    J Neurosurg. 2007 May;106(5 Suppl):354-62 PMID: 17566201
  19. A distinct spectrum of copy number aberrations in pediatric high-grade gliomas.
    Clin Cancer Res. 2010 Jul 1;16(13):3368-77 PMID: 20570930
  20. Prospective evaluation of radiotherapy with concurrent and adjuvant temozolomide in children with newly diagnosed diffuse intrinsic pontine glioma.
    Int J Radiat Oncol Biol Phys. 2010 May 1;77(1):113-8 PMID: 19647954
  21. Developmental genetics of vertebrate glial-cell specification.
    Nature. 2010 Nov 11;468(7321):214-22 PMID: 21068830
  22. HIF-1α inhibition by siRNA or chetomin in human malignant glioma cells: effects on hypoxic radioresistance and monitoring via CA9 expression.
    BMC Cancer. 2010 Nov 04;10:605 PMID: 21050481
  23. The transcriptional network for mesenchymal transformation of brain tumours.
    Nature. 2010 Jan 21;463(7279):318-25 PMID: 20032975
  24. Neuronal differentiation distinguishes supratentorial and infratentorial childhood ependymomas.
    Neuro Oncol. 2010 Nov;12(11):1126-34 PMID: 20615923
  25. Molecular analysis of ex-vivo CD133+ GBM cells revealed a common invasive and angiogenic profile but different proliferative signatures among high grade gliomas.
    BMC Cancer. 2010 Aug 24;10:454 PMID: 20735813
  26. EGFRvIII deletion mutations in pediatric high-grade glioma and response to targeted therapy in pediatric glioma cell lines.
    Clin Cancer Res. 2009 Sep 15;15(18):5753-61 PMID: 19737945
  27. The central nervous system-restricted transcription factor Olig2 opposes p53 responses to genotoxic damage in neural progenitors and malignant glioma.
    Cancer Cell. 2011 Mar 8;19(3):359-71 PMID: 21397859
  28. IDH1 and IDH2 mutations in gliomas.
    N Engl J Med. 2009 May 21;360(21):2248; author reply 2249 PMID: 19458374
  29. Sox10 directs neural stem cells toward the oligodendrocyte lineage by decreasing Suppressor of Fused expression.
    Proc Natl Acad Sci U S A. 2010 Dec 14;107(50):21795-800 PMID: 21098272
  30. Whole-genome profiling of pediatric diffuse intrinsic pontine gliomas highlights platelet-derived growth factor receptor alpha and poly (ADP-ribose) polymerase as potential therapeutic targets.
    J Clin Oncol. 2010 Mar 10;28(8):1337-44 PMID: 20142589
  31. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function.
    J Neurosci. 2008 Jan 2;28(1):264-78 PMID: 18171944
  32. PDGF-B induces a homogeneous class of oligodendrogliomas from embryonic neural progenitors.
    Int J Cancer. 2009 May 15;124(10):2251-9 PMID: 19165863
  33. Diffuse brainstem glioma in children: critical review of clinical trials.
    Lancet Oncol. 2006 Mar;7(3):241-8 PMID: 16510333
  34. Molecular profiling identifies prognostic subgroups of pediatric glioblastoma and shows increased YB-1 expression in tumors.
    J Clin Oncol. 2007 Apr 1;25(10):1196-208 PMID: 17401009
  35. Oligodendrocyte progenitor cells can act as cell of origin for experimental glioma.
    Oncogene. 2009 Jun 11;28(23):2266-75 PMID: 19421151
  36. Magnetic resonance imaging compared with biopsy in the diagnosis of brainstem diseases of childhood: a multicenter review.
    J Neurosurg. 2007 Feb;106(2 Suppl):111-9 PMID: 17330536
  37. Regulation of invasive behavior by vascular endothelial growth factor is HEF1-dependent.
    Oncogene. 2010 Aug 5;29(31):4449-59 PMID: 20498643
  38. PDGFRA gene rearrangements are frequent genetic events in PDGFRA-amplified glioblastomas.
    Genes Dev. 2010 Oct 1;24(19):2205-18 PMID: 20889717
  39. DR-Integrator: a new analytic tool for integrating DNA copy number and gene expression data.
    Bioinformatics. 2010 Feb 1;26(3):414-6 PMID: 20031972
  40. Oncogenic BRAF mutation with CDKN2A inactivation is characteristic of a subset of pediatric malignant astrocytomas.
    Cancer Res. 2010 Jan 15;70(2):512-9 PMID: 20068183
  41. Oncogenic and ligand-dependent activation of KIT/PDGFRA in surgical samples of imatinib-treated gastrointestinal stromal tumours (GISTs).
    J Pathol. 2009 Jan;217(1):103-12 PMID: 18973210
  42. Three paths to better tyrosine kinase inhibition behind the blood-brain barrier in treating chronic myelogenous leukemia and glioblastoma with imatinib.
    Transl Oncol. 2010 Feb;3(1):13-5 PMID: 20165690
  43. Outcome and prognostic features in pediatric gliomas: a review of 6212 cases from the Surveillance, Epidemiology, and End Results database.
    Cancer. 2009 Dec 15;115(24):5761-70 PMID: 19813274
  44. Sox10 is necessary for oligodendrocyte survival following axon wrapping.
    Glia. 2010 Jun;58(8):996-1006 PMID: 20229602
  45. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles.
    Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50 PMID: 16199517
  46. Genome-wide profiling using single-nucleotide polymorphism arrays identifies novel chromosomal imbalances in pediatric glioblastomas.
    Neuro Oncol. 2010 Feb;12(2):153-63 PMID: 20150382
  47. Epidermal growth factor receptor activation in glioblastoma through novel missense mutations in the extracellular domain.
    PLoS Med. 2006 Dec;3(12):e485 PMID: 17177598
  48. Pontine glioma. To biopsy or not to biopsy: that is the question.
    Br J Neurosurg. 2008 Oct;22(5):624 PMID: 19016113
  49. Molecular genetics of pediatric brain stem gliomas. Application of PCR techniques to small and archival brain tumor specimens.
    J Neuropathol Exp Neurol. 1993 Sep;52(5):507-15 PMID: 8103086
  50. Integrated molecular genetic profiling of pediatric high-grade gliomas reveals key differences with the adult disease.
    J Clin Oncol. 2010 Jun 20;28(18):3061-8 PMID: 20479398
  51. Critical role for transcriptional repressor Snail2 in transformation by oncogenic RAS in colorectal carcinoma cells.
    Oncogene. 2010 Aug 19;29(33):4658-70 PMID: 20562906
  52. Loss of suppressor-of-fused function promotes tumorigenesis.
    Oncogene. 2007 Sep 27;26(44):6442-7 PMID: 17452975
  53. Prognostic but not predictive role of platelet-derived growth factor receptors in patients with recurrent glioblastoma.
    Int J Cancer. 2011 Apr 15;128(8):1981-8 PMID: 20589679
  54. The Role of B-RAF Mutations in Melanoma and the Induction of EMT via Dysregulation of the NF-κB/Snail/RKIP/PTEN Circuit.
    Genes Cancer. 2010 May;1(5):409-420 PMID: 20827424
  55. Imatinib mesylate radiosensitizes human glioblastoma cells through inhibition of platelet-derived growth factor receptor.
    Blood Cells Mol Dis. 2005 Mar-Apr;34(2):181-5 PMID: 15727903
  56. Phase I/II study of imatinib mesylate for recurrent malignant gliomas: North American Brain Tumor Consortium Study 99-08.
    Clin Cancer Res. 2006 Aug 15;12(16):4899-907 PMID: 16914578
  57. Tumorigenesis in the brain: location, location, location.
    Cancer Res. 2007 Jun 15;67(12):5579-82 PMID: 17575119
  58. Brain accumulation of dasatinib is restricted by P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and can be enhanced by elacridar treatment.
    Clin Cancer Res. 2009 Apr 1;15(7):2344-51 PMID: 19276246
  59. Prospective collection of tissue samples at autopsy in children with diffuse intrinsic pontine glioma.
    Cancer. 2010 Oct 1;116(19):4632-7 PMID: 20589749
  60. Target-driven exploratory study of imatinib mesylate in children with solid malignancies by the Innovative Therapies for Children with Cancer (ITCC) European Consortium.
    Eur J Cancer. 2009 Sep;45(13):2342-51 PMID: 19362466
  61. Gleevec-mediated inhibition of Rad51 expression and enhancement of tumor cell radiosensitivity.
    Cancer Res. 2003 Nov 1;63(21):7377-83 PMID: 14612536
  62. Phase I trial of imatinib in children with newly diagnosed brainstem and recurrent malignant gliomas: a Pediatric Brain Tumor Consortium report.
    Neuro Oncol. 2007 Apr;9(2):145-60 PMID: 17293590
  63. The proneural molecular signature is enriched in oligodendrogliomas and predicts improved survival among diffuse gliomas.
    PLoS One. 2010 Sep 03;5(9):e12548 PMID: 20838435
  64. Identification of tumor-specific molecular signatures in intracranial ependymoma and association with clinical characteristics.
    J Clin Oncol. 2006 Nov 20;24(33):5223-33 PMID: 17114655
  65. Homozygous loss of ADAM3A revealed by genome-wide analysis of pediatric high-grade glioma and diffuse intrinsic pontine gliomas.
    Neuro Oncol. 2011 Feb;13(2):212-22 PMID: 21138945
  66. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis.
    Cancer Cell. 2006 Mar;9(3):157-73 PMID: 16530701
  67. Brainstem stereotactic biopsy sampling in children.
    J Neurosurg. 2006 Feb;104(2 Suppl):108-14 PMID: 16506498
  68. Glial progenitors in the brainstem give rise to malignant gliomas by platelet-derived growth factor stimulation.
    Glia. 2010 Jul;58(9):1050-65 PMID: 20468047
  69. IDH1 mutations are common in malignant gliomas arising in adolescents: a report from the Children's Oncology Group.
    Childs Nerv Syst. 2011 Jan;27(1):87-94 PMID: 20725730
  70. Innovative Therapies for Children with Cancer pediatric phase I study of erlotinib in brainstem glioma and relapsing/refractory brain tumors.
    Neuro Oncol. 2011 Jan;13(1):109-18 PMID: 20974795
  71. Small molecule inhibitors in children with malignant gliomas.
    Pediatr Blood Cancer. 2009 Sep;53(3):312-7 PMID: 19434732
  72. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells.
    Stem Cells. 2009 Sep;27(9):2059-68 PMID: 19544473
  73. Glioblastoma models reveal the connection between adult glial progenitors and the proneural phenotype.
    PLoS One. 2011;6(5):e20041 PMID: 21625383
  74. Preclinical evaluation of radiation and perifosine in a genetically and histologically accurate model of brainstem glioma.
    Cancer Res. 2010 Mar 15;70(6):2548-57 PMID: 20197468
  75. An ANOCEF genomic and transcriptomic microarray study of the response to radiotherapy or to alkylating first-line chemotherapy in glioblastoma patients.
    Mol Cancer. 2010 Sep 07;9:234 PMID: 20822523
  76. Expression of glioma-associated antigens in pediatric brain stem and non-brain stem gliomas.
    J Neurooncol. 2008 Jul;88(3):245-50 PMID: 18324354
  77. Conditional deletion of Stat3 promotes neurogenesis and inhibits astrogliogenesis in neural stem cells.
    Biochem Biophys Res Commun. 2010 Apr 9;394(3):843-7 PMID: 20303333
  78. Distinct genetic signatures among pilocytic astrocytomas relate to their brain region origin.
    Cancer Res. 2007 Feb 1;67(3):890-900 PMID: 17283119
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2012-00-00
Epub
2012-00-28
Pages
e30313
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC3289615
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]