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PMID: 19333554 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

'Putting our heads together': insights into genomic conservation between human and canine intracranial tumors.

Journal of neuro-oncology ·Vol. 94 ·No. 3 ·2009-09-00 ·Pages 333-49

Thomas R, Duke SE, Wang HJ, Breen TE, Higgins RJ, Linder KE, Ellis P, Langford CF, Dickinson PJ, Olby NJ, Breen M

Abstract

Numerous attributes render the domestic dog a highly pertinent model for cancer-associated gene discovery. We performed microarray-based comparative genomic hybridization analysis of 60 spontaneous canine intracranial tumors to examine the degree to which dog and human patients exhibit aberrations of ancestrally related chromosome regions, consistent with a shared pathogenesis. Canine gliomas and meningiomas both demonstrated chromosome copy number aberrations (CNAs) that share evolutionarily conserved synteny with those previously reported in their human counterpart. Interestingly, however, genomic imbalances orthologous to some of the hallmark aberrations of human intracranial tumors, including chromosome 22/NF2 deletions in meningiomas and chromosome 1p/19q deletions in oligodendrogliomas, were not major events in the dog. Furthermore, and perhaps most significantly, we identified highly recurrent CNAs in canine intracranial tumors for which the human orthologue has been reported previously at low frequency but which have not, thus far, been associated intimately with the pathogenesis of the tumor. The presence of orthologous CNAs in canine and human intracranial cancers is strongly suggestive of their biological significance in tumor development and/or progression. Moreover, the limited genetic heterogenity within purebred dog populations, coupled with the contrasting organization of the dog and human karyotypes, offers tremendous opportunities for refining evolutionarily conserved regions of tumor-associated genomic imbalance that may harbor novel candidate genes involved in their pathogenesis. A comparative approach to the study of canine and human intracranial tumors may therefore provide new insights into their genetic etiology, towards development of more sophisticated molecular subclassification and tailored therapies in both species.

MeSH Terms
Animals Brain Neoplasms/genetics,pathology Chromosome Aberrations Chromosome Mapping Chromosomes, Human, Pair 1 Chromosomes, Human, Pair 22 Cluster Analysis Dogs Female Gene Expression Regulation, Neoplastic Genome/genetics Glioma/genetics,pathology Humans In Situ Hybridization, Fluorescence Male Meningeal Neoplasms/genetics,pathology Meningioma/genetics,pathology
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Thomas Rachael
Department of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27606, USA.
Duke Shannon E
Wang Huixia J
Breen Tessa E
Higgins Robert J
Linder Keith E
Ellis Peter
Langford Cordelia F
Dickinson Peter J
Olby Natasha J
Breen Matthew
References (59)
59 references, click to expand
  1. Genetic and epigenetic changes in the common 1p36 deletion in neuroblastoma tumours.
    Br J Cancer. 2007 Nov 19;97(10):1416-24 PMID: 17940511
  2. Neuro-oncology: new insights and advances in treatment.
    Lancet Neurol. 2008 Jan;7(1):14-6 PMID: 18093552
  3. Canine cytogenetics--from band to basepair.
    Cytogenet Genome Res. 2008;120(1-2):50-60 PMID: 18467825
  4. Oligodendrogliomas: reproducibility and prognostic value of histologic diagnosis and grading.
    J Neuropathol Exp Neurol. 2001 Mar;60(3):248-62 PMID: 11245209
  5. The human genome browser at UCSC.
    Genome Res. 2002 Jun;12(6):996-1006 PMID: 12045153
  6. Genetic structure of the purebred domestic dog.
    Science. 2004 May 21;304(5674):1160-4 PMID: 15155949
  7. Expression and sequence analysis of candidates for the 1p36.31 tumor suppressor gene deleted in neuroblastomas.
    Oncogene. 2008 Jan 31;27(6):803-10 PMID: 17667943
  8. Analysis of genomic alterations in benign, atypical, and anaplastic meningiomas: toward a genetic model of meningioma progression.
    Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14719-24 PMID: 9405679
  9. Canine neoplasia in the UK: estimates of incidence rates from a population of insured dogs.
    J Small Anim Pract. 2002 Jun;43(6):240-6 PMID: 12074288
  10. Loss of material from chromosome arm 1p during malignant progression of meningioma revealed by fluorescent in situ hybridization.
    Cancer. 1998 Jul 15;83(2):360-6 PMID: 9669820
  11. An integrated 4249 marker FISH/RH map of the canine genome.
    BMC Genomics. 2004 Sep 13;5:65 PMID: 15363096
  12. Identification by fluorescence of the G chromosome lost in human meningomas.
    Hereditas. 1972;71(1):163-8 PMID: 4142025
  13. Chromosome aberrations in canine multicentric lymphomas detected with comparative genomic hybridisation and a panel of single locus probes.
    Br J Cancer. 2003 Oct 20;89(8):1530-7 PMID: 14562028
  14. Concurrent loss of chromosome arm 1p and chromosome 3 predicts a decreased disease-free survival in uveal melanoma patients.
    Invest Ophthalmol Vis Sci. 2005 Jul;46(7):2253-7 PMID: 15980208
  15. Canine intracranial primary neoplasia: 173 cases (1986-2003).
    J Vet Intern Med. 2006 May-Jun;20(3):669-75 PMID: 16734106
  16. BAC array CGH distinguishes mutually exclusive alterations that define clinicogenetic subtypes of gliomas.
    Int J Cancer. 2008 Apr 15;122(8):1778-86 PMID: 18076069
  17. Morphology, immunohistochemistry, and genetic alterations in dog astrocytomas.
    Vet Pathol. 2004 Jan;41(1):10-9 PMID: 14715963
  18. Identification of genomic aberrations associated with shorter overall survival in patients with oligodendroglial tumors.
    Int J Cancer. 2007 Jun 1;120(11):2368-76 PMID: 17285580
  19. Comparative genomic hybridization analysis of genomic alterations in benign, atypical and anaplastic meningiomas.
    Acta Neurol Belg. 2002 Jun;102(2):53-62 PMID: 12161900
  20. Evolutionarily conserved cytogenetic changes in hematological malignancies of dogs and humans--man and his best friend share more than companionship.
    Chromosome Res. 2008;16(1):145-54 PMID: 18293109
  21. A role for telomeric and centromeric instability in the progression of chromosome aberrations in meningioma patients.
    Cancer. 2000 Jan 15;88(2):440-53 PMID: 10640979
  22. Faithful companions: a proposal for neurooncology trials in pet dogs.
    Cancer Res. 2007 May 15;67(10):4541-4 PMID: 17510377
  23. Expression of receptor tyrosine kinases VEGFR-1 (FLT-1), VEGFR-2 (KDR), EGFR-1, PDGFRalpha and c-Met in canine primary brain tumours.
    Vet Comp Oncol. 2006 Sep;4(3):132-40 PMID: 19754810
  24. Construction of a 2-Mb resolution BAC microarray for CGH analysis of canine tumors.
    Genome Res. 2005 Dec;15(12):1831-7 PMID: 16339382
  25. A genome assembly-integrated dog 1 Mb BAC microarray: a cytogenetic resource for canine cancer studies and comparative genomic analysis.
    Cytogenet Genome Res. 2008;122(2):110-21 PMID: 19096206
  26. Identification of a cancer stem cell in human brain tumors.
    Cancer Res. 2003 Sep 15;63(18):5821-8 PMID: 14522905
  27. Microarray analysis of differentially expressed genes of primary tumors in the canine central nervous system.
    Vet Pathol. 2005 Sep;42(5):550-8 PMID: 16145201
  28. Malignant progression in meningioma: documentation of a series and analysis of cytogenetic findings.
    J Neurosurg. 2004 Aug;101(2):210-8 PMID: 15309910
  29. A cytogenetically characterized, genome-anchored 10-Mb BAC set and CGH array for the domestic dog.
    J Hered. 2007;98(5):474-84 PMID: 17702974
  30. The 2007 WHO classification of tumours of the central nervous system.
    Acta Neuropathol. 2007 Aug;114(2):97-109 PMID: 17618441
  31. Chromosomal anomalies in oligodendroglial tumors are correlated with clinical features.
    Cancer. 2003 Mar 1;97(5):1276-84 PMID: 12599236
  32. Genome sequence, comparative analysis and haplotype structure of the domestic dog.
    Nature. 2005 Dec 8;438(7069):803-19 PMID: 16341006
  33. Identification of a minimal region of loss on the short arm of chromosome 1 in Wilms tumor.
    Genes Chromosomes Cancer. 2007 Apr;46(4):327-35 PMID: 17243164
  34. Identification of novel candidate target genes in amplicons of Glioblastoma multiforme tumors detected by expression and CGH microarray profiling.
    Mol Cancer. 2006 Sep 26;5:39 PMID: 17002787
  35. Imbalances of chromosome arm 1p in pediatric and adult germ cell tumors are caused by true allelic loss: a combined comparative genomic hybridization and microsatellite analysis.
    Genes Chromosomes Cancer. 2006 Nov;45(11):995-1006 PMID: 16897744
  36. Oligodendroglial tumors: refinement of candidate regions on chromosome arm 1p and correlation of 1p/19q status with survival.
    Brain Pathol. 2004 Apr;14(2):121-30 PMID: 15193024
  37. Identification of human brain tumour initiating cells.
    Nature. 2004 Nov 18;432(7015):396-401 PMID: 15549107
  38. The WHO classification of tumors of the nervous system.
    J Neuropathol Exp Neurol. 2002 Mar;61(3):215-25; discussion 226-9 PMID: 11895036
  39. Candidate glioblastoma development gene identification using concordance between copy number abnormalities and gene expression level changes.
    Genes Chromosomes Cancer. 2007 Oct;46(10):875-94 PMID: 17620294
  40. Comparative genomic hybridization in glioma: a meta-analysis of 509 cases.
    Cancer Genet Cytogenet. 2002 Jun;135(2):147-59 PMID: 12127399
  41. Magnetic resonance imaging and histological classification of intracranial meningiomas in 112 dogs.
    J Vet Intern Med. 2008 May-Jun;22(3):586-95 PMID: 18466258
  42. Breakpoint identification and smoothing of array comparative genomic hybridization data.
    Bioinformatics. 2004 Dec 12;20(18):3636-7 PMID: 15201182
  43. Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas.
    J Clin Oncol. 2000 Feb;18(3):636-45 PMID: 10653879
  44. Oligodendroglioma: a new chemosensitive tumor.
    J Clin Oncol. 1990 Dec;8(12):2090-1 PMID: 2230902
  45. Two types of chromosome 1p losses with opposite significance in gliomas.
    Ann Neurol. 2005 Sep;58(3):483-7 PMID: 16130103
  46. Malignant brain tumors: two steps forward.
    Clin Neurosurg. 2007;54:4-9 PMID: 18504889
  47. Glioblastoma multiforme: clinical findings, magnetic resonance imaging, and pathology in five dogs.
    Vet Pathol. 2003 Nov;40(6):659-69 PMID: 14608019
  48. Clinical relevance of 1p and 19q deletion for patients with WHO grade 2 and 3 gliomas.
    J Neurooncol. 2008 Jul;88(3):293-8 PMID: 18345516
  49. The DAPI banded karyotype of the domestic dog (Canis familiaris) generated using chromosome-specific paint probes.
    Chromosome Res. 1999;7(5):401-6 PMID: 10515215
  50. Clinical and pathologic features of oligodendrogliomas in two cats.
    Vet Pathol. 2000 Mar;37(2):160-7 PMID: 10714645
  51. Detailed assessment of copy number alterations revealing homozygous deletions in 1p and 13q in mantle cell lymphoma.
    Leuk Res. 2007 Sep;31(9):1219-30 PMID: 17161458
  52. Chromosomal instability in meningiomas.
    J Neuropathol Exp Neurol. 2005 Apr;64(4):312-22 PMID: 15835267
  53. Distinct B-cell and T-cell lymphoproliferative disease prevalence among dog breeds indicates heritable risk.
    Cancer Res. 2005 Jul 1;65(13):5654-61 PMID: 15994938
  54. Molecular subtypes of anaplastic oligodendroglioma: implications for patient management at diagnosis.
    Clin Cancer Res. 2001 Apr;7(4):839-45 PMID: 11309331
  55. Brain tumours: classification and genes.
    J Neurol Neurosurg Psychiatry. 2004 Jun;75 Suppl 2:ii2-11 PMID: 15146033
  56. Intracranial glioblastoma models in preclinical neuro-oncology: neuropathological characterization and tumor progression.
    J Neurooncol. 2007 Nov;85(2):133-48 PMID: 17874037
  57. Optimization of adenoviral vector-mediated transgene expression in the canine brain in vivo, and in canine glioma cells in vitro.
    Neuro Oncol. 2007 Jul;9(3):245-58 PMID: 17522335
  58. A t(1;19)(q10;p10) mediates the combined deletions of 1p and 19q and predicts a better prognosis of patients with oligodendroglioma.
    Cancer Res. 2006 Oct 15;66(20):9852-61 PMID: 17047046
  59. Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma.
    Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):20007-12 PMID: 18077431
Article Info
Journal
Journal of neuro-oncology
Abbr.
J Neurooncol
ISSN
1573-7373
Published
2009-09-00
Epub
2009-00-31
Pages
333-49
Language
English
Region
United States
NLM ID
8309335
PMCID
PMC3225023
Subset
IM
Grants
NINDS NIH HHS · R21 NS051190 · United States
NINDS NIH HHS · R21 NS051190-01 · United States
Wellcome Trust · United Kingdom
NINDS NIH HHS · NS051190 · United States
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