Frequent biallelic inactivation and transcriptional silencing of the DIRAS3 gene at 1p31 in oligodendroglial tumors with 1p loss

International Journal of Cancer

Volumn 122, Issue 11, 2008, Pages 2503-2510

  Riemenschneider, Markus J ^a   Reifenberger, Julia ^a   Reifenberger, Guido ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

1p; ARHI; DIRAS3; Methylation; Oligodendroglioma

Indexed keywords

DIRAS3 PROTEIN; GENE PRODUCT; MESSENGER RNA; MOLECULAR MARKER;

ALLELISM; ARTICLE; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CHROMOSOME 1P; CHROMOSOME LOSS; CONTROLLED STUDY; DIRAS3 GENE; DNA METHYLATION; GENE; GENE DELETION; GENE FREQUENCY; GENE INACTIVATION; GENE SILENCING; GLIOMA; HUMAN; HUMAN CELL; METHYLATION; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIOMA; PRIORITY JOURNAL; PROGNOSIS; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

ALLELES; ASTROCYTOMA; BRAIN NEOPLASMS; CHROMOSOMES, HUMAN, PAIR 1; CPG ISLANDS; DNA METHYLATION; DNA MUTATIONAL ANALYSIS; GENE SILENCING; GLIOMA; HUMANS; LOSS OF HETEROZYGOSITY; MICROSATELLITE REPEATS; MUTATION; OLIGODENDROGLIOMA; PREDICTIVE VALUE OF TESTS; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHO GTP-BINDING PROTEINS; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TUMOR MARKERS, BIOLOGICAL;

EID: 42549135582     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23409     Document Type: Article

References (33)

1. Yu Y, Xu F, Peng H, Fang X, Zhao S, Li Y, Cuevas B, Kuo WL, Gray JW, Siciliano M, Mills GB, Bast RC Jr. NOEY2 (ARHI): an imprinted putative tumor suppressor gene in ovarian and breast carcinomas. Proc Natl Acad Sci USA 1999;96:214-19.
2. Wang L, Hoque A, Luo RZ, Yuan J, Lu Z, Nishimoto A, Liu J, Sahin AA, Lippman SM, Bast RC Jr, Yu Y. Loss of the expression of the tumor suppressor gene ARHI is associated with progression of breast cancer. Clin Cancer Res 2003;9:3660-6.
3. Yu Y, Luo R, Lu Z, Wei Feng W, Badgwell D, Issa JP, Rosen DG, Liu J, Bast RC Jr. Biochemistry and biology of ARHI (DIRAS3): an imprinted tumor suppressor gene whose expression is lost in ovarian and breast cancers. Methods Enzymol 2005;407:455-68.
4. Bao JJ, Le XF, Wang RY, Yuan J, Wang L, Atkinson EN, LaPushin R, Andreeff M, Fang B, Yu Y, Bast RC Jr. Reexpression of the tumor suppressor gene ARHI induces apoptosis in ovarian and breast cancer cells through a caspase-independent calpain-dependent pathway. Cancer Res 2002;62:7264-72.
5. Nishimoto A, Yu Y, Lu Z, Mao X, Ren Z, Watowich SS, Mills GB, Liao WS, Chen X, Bast RC Jr, Luo RZ. A Ras homologue member I directly inhibits signal transducers and activators of transcription 3 translocation and activity in human breast and ovarian cancer cells. Cancer Res 2005;65:6701-10.
6. Luo RZ, Peng H, Xu F, Bao J, Pang Y, Pershad R, Issa JP, Liao WS, Bast RC Jr, Yu Y. Genomic structure and promoter characterization of an imprinted tumor suppressor gene ARHI. Biochim Biophys Acta 2001;1519:216-22.
7. Yuan J, Luo RZ, Fujii S, Wang L, Hu W, Andreeff M, Pan Y, Kadota M, Oshimura M, Sahin AA, Issa JP, Bast RC Jr, et al. Aberrant methylation and silencing of ARHI: an imprinted tumor suppressor gene in which the function is lost in breast cancers. Cancer Res 2003;63:4174-80.
8. Reifenberger J, Reifenberger G, Liu L, James CD, Wechsler W, Collins VP. Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol 1994;145:1175-90.
9. Cairncross JG, Ueki K, Zlatescu MC, Lisle DK, Finkelstein DM, Hammond RR, Silver JS, Stark PC, Macdonald DR, Ino Y, Ramsay DA, Louis DN. Specific genetic predictors of chemofherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst 1998;90:1473-9.
10. Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, Brachman D, Buckner J, Fink K, Souhami L, Laperierre N, Mehta M, Curran W. Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: Intergroup Radiation Therapy Oncology Group Trial 9402. J Clin Oncol 2006;24:2707-14.
11. van den Bent MJ, Carpentier AF, Brandes AA, Sanson M, Taphoorn MJ, Bernsen HJ, Frenay M, Tijssen CC, Grisold W, Sipos L, Haaxma-Reiche H, Kros JM, et al. Adjuvant procarbazine, lomustine, and vincristine improves progression-free survival but not overall survival in newly diagnosed anaplastic oligodendrogliomas and oligoastrocytomas: a randomized European Organization for Research and Treatment of Cancer phase III trial. J Clin Oncol 2006;24:2715-22.
12. Felsberg J, Erkwoh A, Sabel MC, Kirsch L, Fimmers R, Blaschke B, Schlegel U, Schramm J, Wiestler OD, Reifenberger G. Oligodendroglial tumors: refinement of candidate regions on chromosome arm 1p and correlation of 1p/19q status with survival. Brain Pathol 2004;14:121-30.
13. Jenkins RB, Blair H, Ballman KV, Giannini C, Arusell RM, Law M, Flynn H, Passe S, Felten S, Brown PD, Shaw EG, Buckner JC. 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;66:9852-61.
14. Kleihues P, Cavenee WK, eds. Pathology and genetics of tumours of the nervous system, 2nd edn. Lyon: IARC Press, 2000.
15. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, eds. WHO classification of tumours of the central nervous system, 3rd ed. Lyon: IARC Press, 2007.
16. van den Boom J, Wolter M, Kuick R, Misek DE, Youkilis AS, Wechsler DS, Sommer C, Reifenberger G, Hanash SM. Characterization of gene expression profiles associated with glioma progression using oligonucleotide-based microarray analysis and real-time reverse transcription-polymerase chain reaction. Am J Pathol 2003;163:1033-43.
17. Riemenschneider MJ, Koy TH, Reifenberger G. Expression of oligodendrocyte lineage genes in oligodendroglial and astrocytic gliomas. Acta Neuropathol (Berl) 2004;107:277-82.
18. Mueller W, Nutt CL, Ehrich M, Riemenschneider MJ, von Deimling A, van den Boom D, Louis DN. Downregulation of RUNX3 and TES by hypermethylation in glioblastoma. Oncogene 2007;26:583-93.
19. Xiong Z, Laird PW. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res 1997;25:2532-4.
20. Yu Y, Fujii S, Yuan J, Luo RZ, Wang L, Bao J, Kadota M, Oshimura M, Dent SR, Issa JP, Bast RC Jr. Epigenetic regulation of ARHI in breast and ovarian cancer cells. Ann N Y Acad Sci 2003;983:268-77.
21. Dalai I, Missiaglia E, Barbi S, Butturini G, Doglioni C, Falconi M, Scarpa A. Low expression of ARHI is associated with shorter progression-free survival in pancreatic endocrine tumors. Neoplasia 2007;9:181-3.
22. Field JK, Liloglou T, Warrak S, Burger M, Becker E, Berlin K, Nimmrich I, Maier S. Methylation discriminators in NSCLC identified by a microarray based approach. Int J Oncol 2005;27:105-11.
23. Weber F, Aldred MA, Morrison CD, Plass C, Frilling A, Broelsch CE, Waite KA, Eng C. Silencing of the maternally imprinted tumor suppressor ARHI contributes to follicular thyroid carcinogenesis. J Clin Endocrinol Metab 2005;90:1149-55.
24. Wang Y, Yu Q, Cho AH, Rondeau G, Welsh J, Adamson E, Mercola D, McClelland M. Survey of differentially methylated promoters in prostate cancer cell lines. Neoplasia 2005;7:748-60.
25. Santin AD, Zhan F, Cane S, Bellone S, Palmieri M, Thomas M, Burnett A, Roman JJ, Cannon MJ, Shaughnessy J Jr, Pecorelli S. Gene expression fingerprint of uterine serous papillary carcinoma: identification of novel molecular markers for uterine serous cancer diagnosis and therapy. Br J Cancer 2005;92:1561-73.
26. Nguyen C, Liang G, Nguyen TT, Tsao-Wei D, Groshen S, Lubbert M, Zhou JH, Benedict WF, Jones PA. Susceptibility of nonpromoter CpG islands to de novo methylation in normal and neoplastic cells. J Natl Cancer Inst 2001;93:1465-72.
27. Sanson M, Leuraud P, Marie Y, Delattre JY, Hoang-Xuan K. Preferential loss of paternal 19q, but not 1p, alleles in oligodendrogliomas. Ann Neurol 2002;52:105-7.
28. Hartmann C, Mueller W, Lass U, Stockhammer F, von Eckardstein K, Veelken J, Jeuken J, Wick W, von Deimling A. No preferential loss of paternal 19q alleles in oligodendroglial tumors. Ann Neurol 2003;54:256-8.
29. Lu Z, Luo RZ, Peng H, Rosen DG, Atkinson EN, Warneke C, Huang M, Nishmoto A, Liu J, Liao WS, Yu Y, Bast RC Jr. Transcriptional and posttranscriptional down-regulation of the imprinted tumor suppressor gene ARHI (DRAS3) in ovarian cancer. Clin Cancer Res 2006;12:2404-13.
30. Reifenberger G, Collins VP. Pathology and molecular genetics of astrocytic gliomas. J Mol Med 2004;82:656-70.
31. Riemenschneider MJ, Mueller W, Betensky RA, Mohapatra G, Louis DN. In situ analysis of integrin and growth factor receptor signaling pathways in human glioblastomas suggests overlapping relationships with focal adhesion kinase activation. Am J Pathol 2005;167:1379-87.
32. Riemenschneider MJ, Betensky RA, Pasedag SM, Louis DN. AKT activation in human glioblastomas enhances proliferation via TSC2 and S6 kinase signaling. Cancer Res 2006;66:5618-23.
33. Nicholas MK, Lukas RV, Jafri NF, Faoro L, Salgia R. Epidermal growth factor receptor - mediated signal transduction in the development and therapy of gliomas. Clin Cancer Res 2006;12:7261-70.