CDKN2A Loss Is Associated with Shortened Overall Survival in Lower-Grade (World Health Organization Grades II-III) Astrocytomas

Journal of Neuropathology and Experimental Neurology

Volumn 74, Issue 5, 2015, Pages 442-452

  Reis, Gerald F ^b   Pekmezci, Melike ^b   Hansen, Helen M ^c   Rice, Terri ^c   Marshall, Roxanne E ^c   Molinaro, Annette M ^c   Phillips, Joanna J ^c   Vogel, Hannes ^a   Wiencke, John K ^c   Wrensch, Margaret R ^c   Walsh, Kyle M ^c   Perry, Arie ^b,c  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocytoma; ATRX; Biomarker; CDKN2A; IDH; Infiltrating glioma; Oligodendroglioma; p16; TP53

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; PROTEIN P53; ISOCITRATE DEHYDROGENASE; TUMOR MARKER;

ADULT; ARTICLE; ASTROCYTOMA; DIFFUSE ASTROCYTOMA; FEMALE; FOLLOW UP; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; GLIOBLASTOMA; HUMAN; INVESTIGATIVE PROCEDURES; MAJOR CLINICAL STUDY; MALE; OLIGODENDROGLIOMA; OVERALL SURVIVAL; PATHOLOGIST; PRIORITY JOURNAL; TUMOR CLASSIFICATION; WORLD HEALTH ORGANIZATION; BRAIN TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; MORTALITY; MUTATION; PHYSIOLOGY; SURVIVAL ANALYSIS;

ADULT; ASTROCYTOMA; BIOMARKERS, TUMOR; BRAIN NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; ISOCITRATE DEHYDROGENASE; MALE; MIDDLE AGED; MUTATION; SURVIVAL ANALYSIS;

EID: 84942046178     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0000000000000188     Document Type: Article

References (48)

1. Dolecek TA, Propp JM, Stroup NE, Kruchko C. CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the United States in 2005-2009. Neuro Oncol 2012;14(Suppl 5):v1-49
2. Louis DN, Cavenee WK, Ohgaki H, et al. WHO Classification of Tumours of the Central Nervous System. Lyon, France: IARC Press, 2007
3. Louis DN, Perry A, Burger P, et al. International Society of NeuropathologyVHaarlem consensus guidelines for nervous system tumor classification and grading. Brain Pathol 2014;24:429-35
4. Bourne TD, Schiff D. Update on molecular findings, management and outcome in low-grade gliomas. Nat Rev Neurol 2010;6:695-701
5. Parsons DW, Jones S, Zhang X, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008;321:1807-12
6. Yan H, Parsons DW, Jin G, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009;360:765-73
7. Hartmann C,Meyer J, Balss J, et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: A study of 1,010 diffuse gliomas. Acta Neuropathol 2009;118:469-74
8. Kannan K, Inagaki A, Silber J, et al. Whole-exome sequencing identifies ATRX mutation as a key molecular determinant in lower-grade glioma. Oncotarget 2012;3:1194-203
9. Heaphy CM, de Wilde RF, Jiao Y, et al. Altered telomeres in tumors with ATRX and DAXX mutations. Science 2011;333:425
10. Jiao Y, Killela PJ, Reitman ZJ, et al. Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas. Oncotarget 2012;3:709-22
11. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114:97-109
12. Okamoto Y, Di Patre PL, Burkhard C, et al. Population-based study on incidence, survival rates, and genetic alterations of low-grade diffuse astrocytomas and oligodendrogliomas. Acta Neuropathol 2004;108:49-56
13. Watanabe T, Nakamura M, Kros JM, et al. Phenotype versus genotype correlation in oligodendrogliomas and low-grade diffuse astrocytomas. Acta Neuropathol 2002;103:267-75
14. Reifenberger G, Louis DN. Oligodendroglioma: Toward molecular definitions in diagnostic neuro-oncology. J Neuropathol Exp Neurol 2003; 62:111-26
15. Killela PJ, Reitman ZJ, Jiao Y, et al. TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc Natl Acad Sci U S A 2013;110:6021-26
16. Sahm F, Reuss D, Koelsche C, et al. Farewell to oligoastrocytoma: In situ molecular genetics favor classification as either oligodendroglioma or astrocytoma. Acta Neuropathol 2014;128:551-59
17. Ohgaki H, Kleihues P. Genetic alterations and signaling pathways in the evolution of gliomas. Cancer Sci 2009;100:2235-41
18. Rasheed A, Herndon JE, Stenzel TT, et al. Molecular markers of prognosis in astrocytic tumors. Cancer 2002;94:2688-97
19. Perry A, Anderl K, Borell TJ, et al. Detection of p16, RB, CDK4, and p53 gene deletion and amplification by fluorescence in situ hybridization in 96 gliomas. Am J Clin Pathol 1999;112:801-9
20. Maruno M, Yoshimine T, Muhammad AK, Tokiyoshi K, Hayakawa T. Loss of heterozygosity of microsatellite loci on chromosome 9p in astrocytic tumors and its prognostic implications. J Neurooncol 1996;30:19-24
21. Ruas M, Peters G. The p16INK4a/CDKN2A tumor suppressor and its relatives. Biochim Biophys Acta 1998;1378:F115-77
22. Weinberg RA. The retinoblastoma protein and cell cycle control. Cell 1995;81:323-30
23. Sherr CJ, Roberts JM. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev 1999;13:1501-12
24. He J, Olson JJ, James CD. Lack of p16INK4 or retinoblastoma protein (pRb), or amplification-associated overexpression of cdk4 is observed in distinct subsets of malignant glial tumors and cell lines. Cancer Res 1995; 55:4833-36
25. Watanabe T, Yokoo H, Yokoo M, Yonekawa Y, Kleihues P, Ohgaki H. Concurrent inactivation of RB1 and TP53 pathways in anaplastic oligodendrogliomas. J Neuropathol Exp Neurol 2001;60:1181-89
26. Ueki K, Ono Y, Henson JW, Efird JT, von Deimling A, Louis DN. CDKN2/p16 or RB alterations occur in the majority of glioblastomas and are inversely correlated. Cancer Res 1996;56:150-53
27. Jeon YK, Park K, Park CK, Paek SH, Jung HW, Park SH. Chromosome 1p and 19q status and p53 and p16 expression patterns as prognostic indicators of oligodendroglial tumors: A clinicopathological study using fluorescence in situ hybridization. Neuropathology 2007;27:10-20
28. Bigner SH, Matthews MR, Rasheed BK, et al. Molecular genetic aspects of oligodendrogliomas including analysis by comparative genomic hybridization. Am J Pathol 1999;155:375-86
29. Perry A, Nobori T, Ru N, et al. Detection of p16 gene deletions in gliomas: A comparison of fluorescence in situ hybridization (FISH) versus quantitative PCR. J Neuropathol Exp Neurol 1997;56:999-1008
30. Fuller CE, Schmidt RE, Roth KA, et al. Clinical utility of fluorescence in situ hybridization (FISH) in morphologically ambiguous gliomas with hybrid oligodendroglial/astrocytic features. J Neuropathol Exp Neurol 2003;62:1118-28
31. Bortolotto S, Chiado-Piat L, Cavalla P, et al. CDKN2A/p16 inactivation in the prognosis of oligodendrogliomas. Int J Cancer 2000;88:554-57
32. Cairncross JG, Ueki K, Zlatescu MC, et al. Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst 1998;90:1473-79
33. Miettinen H, Kononen J, Sallinen P, et al. CDKN2/p16 predicts survival in oligodendrogliomas: Comparison with astrocytomas. J Neurooncol 1999;41:205-11
34. Wick W, Hartmann C, Engel C, et al. NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol 2009;27: 5874-80
35. Shibahara I, Sonoda Y, Kanamori M, Saito R, Kumabe T, Tominaga T. New insights into glioma classification based on isocitrate dehydrogenase 1 and 2 gene status. Brain Tumor Pathol 2011;28:203-8
36. Walsh KM, Codd V, Smirnov IV, et al. Variants near TERT and TERC influencing telomere length are associated with high-grade glioma risk. Nat Genet 2014;46:731-35
37. Rice T, Zheng S, Decker PA, et al. Inherited variant on chromosome 11q23 increases susceptibility to IDH-mutated but not IDH-normal gliomas regardless of grade or histology. Neuro Oncol 2013;15:535-41
38. Christensen BC, Smith AA, Zheng S, et al. DNA methylation, isocitrate dehydrogenase mutation, and survival in glioma. J Natl Cancer Inst 2011; 103:143-53
39. Wiencke JK, Aldape K, McMillan A, et al. Molecular features of adult glioma associated with patient race/ethnicity, age, and a polymorphism in O6-methylguanine-DNA-methyltransferase. Cancer Epidemiol Biomarkers Prev 2005;14:1774-83
40. Stacey SN, Sulem P, Jonasdottir A, et al. A germline variant in the TP53 polyadenylation signal confers cancer susceptibility. Nat Genet 2011;43: 1098-103
41. Perry A, Fuller CE, Banerjee R, Brat DJ, Scheithauer BW. Ancillary FISH analysis for 1p and 19q status: Preliminary observations in 287 gliomas and oligodendroglioma mimics. Front Biosci 2003;8:a1Ya9
42. Costello JF, Berger MS, Huang HS, Cavenee WK. Silencing of p16/CDKN2 expression in human gliomas by methylation and chromatin condensation. Cancer Res 1996;56:2405-10
43. Alves MK, Faria MH, Neves Filho EH, et al. CDKN2A promoter hypermethylation in astrocytomas is associated with age and sex. Int J Surg 2013;11:549-53
44. Liu XY, Gerges N, Korshunov A, et al. Frequent ATRX mutations and loss of expression in adult diffuse astrocytic tumors carrying IDH1/IDH2 and TP53 mutations. Acta Neuropathol 2012;124:615-25
45. Jiao Y, Shi C, Edil BH, et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 2011;331:1199-203
46. Schwartzentruber J, Korshunov A, Liu XY, et al. Driver mutations in histone H3. 3 and chromatin remodelling genes in paediatric glioblastoma. Nature 2012;482:226-31
47. Shay JW, Wright WE. Role of telomeres and telomerase in cancer. Semin Cancer Biol 2011;21:349-53
48. Walsh KM, Rice T, Decker PA, et al. Genetic variants in telomerase-related genes are associated with an older age at diagnosis in glioma patients: Evidence for distinct pathways of gliomagenesis. Neuro Oncol 2013;15: 1041-47