Frequent promoter hypermethylation of Wnt pathway inhibitor genes in malignant astrocytic gliomas

International Journal of Cancer

Volumn 126, Issue 11, 2010, Pages 2584-2593

  Götze, Silke ^a   Wolter, Marietta ^b   Reifenberger, Guido ^b   Müller, Oliver ^c   Sievers, Sonja ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF APPLIED SCIENCES KAISERSLAUTERN   (Germany)

Author keywords

DNA hypermethylation; Glioma; NKD; Wnt inhibitor

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; BETA CATENIN; DICKKOPF 1 PROTEIN; DICKKOPF 3 PROTEIN; GLYCOPROTEIN; MEMBRANE PROTEIN; SECRETED FRIZZLED RELATED PROTEIN 1; SECRETED FRIZZLED RELATED PROTEIN 2; SECRETED FRIZZLED RELATED PROTEIN 4; SECRETED FRIZZLED RELATED PROTEIN 5; TRICHOSTATIN A; UNCLASSIFIED DRUG; WNT PROTEIN; CARRIER PROTEIN; CTNNB1 PROTEIN, HUMAN; DNA; EYE PROTEIN; NKD1 PROTEIN, HUMAN; NKD2 PROTEIN, HUMAN; ONCOPROTEIN; SFRP1 PROTEIN, HUMAN; SFRP2 PROTEIN, HUMAN; SFRP4 PROTEIN, HUMAN; SFRP5 PROTEIN, HUMAN; SIGNAL PEPTIDE;

ADULT; AGED; ARTICLE; ASTROCYTOMA; CONTROLLED STUDY; EXON; FEMALE; GENE; GENE EXPRESSION; GENE MUTATION; GLIOBLASTOMA; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; METHYLATION; NKD1 GENE; NKD2 GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; DNA METHYLATION; GENETICS; GLIOMA; ISOLATION AND PURIFICATION; METASTASIS; MUTATION; PATHOLOGY; POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ASTROCYTOMA; BETA CATENIN; CARRIER PROTEINS; CELL LINE, TUMOR; DNA METHYLATION; DNA MUTATIONAL ANALYSIS; DNA, NEOPLASM; EXONS; EYE PROTEINS; GLIOBLASTOMA; GLIOMA; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MUTATION; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; WNT PROTEINS;

EID: 77951247981     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24981     Document Type: Article

References (45)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, eds. WHO classification of tumours of the central nervous system, 3rd ed. Lyon: IARC Press, 2007.
2. Ohgaki H, Kleihues P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol 2005;64:479-489 (Pubitemid 40781150)
3. Kleihues P, Ohgaki H. Primary and secondary glioblastomas: from concept to clinical diagnosis. Neuro Oncol 1999;1:44-51.
4. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol 2007;170:1445-1453 (Pubitemid 47339290)
5. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009;360:765-773
6. Krex D, Klink B, Hartmann C, von Deimling A, Pietsch T, Simon M, Sabel M, Steinbach JP, Heese O, Reifenberger G, Weller M, Schackert G. Long-term survival with glioblastoma multiforme. Brain 2007;130:2596-2606
7. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003. (Pubitemid 40349502)
8. Hegi ME, Liu L, Herman JG, Stupp R, Wick W, Weller M, Mehta MP, Gilbert MR. Correlation of O6-methylguanine methyltransferase (MGMT) promoter methylation with clinical outcomes in glioblastoma and clinical strategies to modulate MGMT activity. J Clin Oncol 2008;26:4189-4199
9. Polakis P. The many ways of Wnt in cancer. Curr Opin Genet Dev 2007;17:45-51.
10. Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer 2008;8:387-398 (Pubitemid 351589714)
11. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997;275:1787-1790 (Pubitemid 27136715)
12. Sareddy GR, Challa S, Panigrahi M, Babu PP. Wnt/beta-catenin/Tcf signaling pathway activation in malignant progression of rat gliomas induced by transplacental N-ethyl-N-nitrosourea exposure. Neurochem Res 2009;34:1278-88.
13. Utsuki S, Sato Y, Oka H, Tsuchiya B, Suzuki S, Fujii K. Relationship between the expression of E-, N-cadherins and beta-catenin and tumor grade in astrocytomas. J Neurooncol 2002;57:187-192 (Pubitemid 34692627)
14. Moon RT, Kohn AD, De Ferrari GV, Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat Rev Genet 2004;5:691-701. (Pubitemid 39150127)
15. Katoh M, Katoh M. WNT signaling pathway and stem cell signaling network. Clin Cancer Res 2007;13:4042-4045 (Pubitemid 47105963)
16. Chan CC, Zhang S, Cagatay T, Wharton KA, Jr. Cell-autonomous, myristyl-independent activity of the Drosophila Wnt/Wingless antagonist naked cuticle (Nkd). Dev Biol 2007;311:538-553 (Pubitemid 350046544)
17. Chan CC, Zhang S, Rousset R, Wharton KA, Jr. Drosophila naked cuticle (Nkd) engages the nuclear import adaptor Importin-alpha3 to antagonize Wnt/beta-catenin signaling. Dev Biol 2008;318:17-28.
18. Rousset R, Mack JA, Wharton KA, Jr, Axelrod JD, Cadigan KM, Fish MP, Nusse R, Scott MP. Naked cuticle targets dishevelled to antagonize Wnt signal transduction. Genes Dev 2001;15:658-671 (Pubitemid 32244896)
19. Zhang S, Cagatay T, Amanai M, Zhang M, Kline J, Castrillon DH, Ashfaq R, Oz OK, Wharton KA, Jr. Viable mice with compound mutations in the Wnt/Dvl pathway antagonists nkd1 and nkd2. Mol Cell Biol 2007;27:4454-4464
20. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, Chen WD, Pretlow TP, Yang B, Akiyama Y, Van Engeland M, Toyota M, Tokino T, et al. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 2004;36:417-422 (Pubitemid 38437267)
21. Nojima M, Suzuki H, Toyota M, Watanabe Y, Maruyama R, Sasaki S, Sasaki Y, Mita H, Nishikawa N, Yamaguchi K, Hirata K, Itoh F, et al. Frequent epigenetic inactivation of SFRP genes and constitutive activation of Wnt signaling in gastric cancer. Oncogene 2007;26:4699-4713 (Pubitemid 47067406)
22. Aguilera O, Fraga MF, Ballestar E, Paz MF, Herranz M, Espada J, Garcia JM, Munoz A, Esteller M, Gonzalez-Sancho JM. Epigenetic inactivation of the Wnt antagonist DICKKOPF-1 (DKK-1) gene in human colorectal cancer. Oncogene 2006;25:4116-4121 (Pubitemid 44024874)
23. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo JA, Navarro G, Barrios M, Andreu EJ, Prosper F, Heiniger A, Torres A. Transcriptional silencing of the Dickkopfs-3 (Dkk-3) gene by CpG hypermethylation in acute lymphoblastic leukaemia. Br J Cancer 2004;91:707-713 (Pubitemid 39141629)
24. Nikuseva-Martic T, Beros V, Pecina-Slaus N, Pecina HI, Bulic-Jakus F. Genetic changes of CDH1, APC, and CTNNB1 found in human brain tumors. Pathol Res Pract 2007;203:779-787
25. Pu P, Zhang Z, Kang C, Jiang R, Jia Z, Wang G, Jiang H. Downregulation of Wnt2 and beta-catenin by siRNA suppresses malignant glioma cell growth. Cancer Gene Ther 2009;16:351-361
26. van den BJ, 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 transcriptionpolymerase chain reaction. Am J Pathol 2003;163:1033-1043 (Pubitemid 37040139)
27. Suzuki H, Gabrielson E, Chen W, Anbazhagan R, Van Engeland M, Weijenberg MP, Herman JG, Baylin SB. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 2002;31:141-149
28. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002;18:1427-1431 (Pubitemid 35414532)
29. Zou H, Molina JR, Harrington JJ, Osborn NK, Klatt KK, Romero Y, Burgart LJ, Ahlquist DA. Aberrant methylation of secreted frizzled-related protein genes in esophageal adenocarcinoma and Barrett's esophagus. Int J Cancer 2005;116:584-591 (Pubitemid 41099195)
30. Schumann H, Holtz J, Zerkowski HR, Hatzfeld M. Expression of secreted frizzled related proteins 3 and 4 in human ventricular myocardium correlates with apoptosis related gene expression. Cardiovasc Res 2000;45:720-728 (Pubitemid 30047139)
31. Polakis P. The oncogenic activation of beta-catenin. Curr Opin Genet Dev 1999;9:15-21.
32. Yano H, Hara A, Shinoda J, Takenaka K, Yoshimi N, Mori H, Sakai N. Immunohistochemical analysis of beta-catenin in N-ethyl-N-nitrosourea-induced rat gliomas: implications in regulation of angiogenesis. Neurol Res 2000;22:527-532 (Pubitemid 30602560)
33. Mueller W, Lass U, Wellmann S, Kunitz F, von Deimling A. Mutation analysis of DKK1 and in vivo evidence of predominant p53-independent DKK1 function in gliomas. Acta Neuropathol 2005;109:314-320 (Pubitemid 41166601)
34. Preusser M, Charles JR, Felsberg J, Reifenberger G, Hamou MF, Diserens AC, Stupp R, Gorlia T, Marosi C, Heinzl H, Hainfellner JA, Hegi M. Anti-O6- methylguanine-methyltransferase (MGMT) immunohistochemistry in glioblastoma multiforme: observer variability and lack of association with patient survival impede its use as clinical biomarker. Brain Pathol 2008;18:520-532
35. Shou J, Ali-Osman F, Multani AS, Pathak S, Fedi P, Srivenugopal KS. Human Dkk-1, a gene encoding a Wnt antagonist, responds to DNA damage and its overexpression sensitizes brain tumor cells to apoptosis following alkylation damage of DNA. Oncogene 2002;21:878-889 (Pubitemid 34146301)
36. Wang J, Shou J, Chen X. Dickkopf-1, an inhibitor of the Wnt signaling pathway, is induced by p53. Oncogene 2000;19:1843-1848 (Pubitemid 30200990)
37. Veeck J, Niederacher D, An H, Klopocki E, Wiesmann F, Betz B, Galm O, Camara O, Durst M, Kristiansen G, Huszka C, Knuchel R, et al. Aberrant methylation of the Wnt antagonist SFRP1 in breast cancer is associated with unfavourable prognosis. Oncogene 2006;25:3479-3488
38. Esteller M. Epigenetic gene silencing in cancer: the DNA hypermethylome. Hum Mol Genet 2007;16 (Spec No 1):R50-R59. (Pubitemid 47241842)
39. Kunitz A, Wolter M, van den BJ, Felsberg J, Tews B, Hahn M, Benner A, Sabel M, Lichter P, Reifenberger G, von Deimling A, Hartmann C. DNA hypermethylation and aberrant expression of the EMP3 gene at 19q13.3 in human gliomas. Brain Pathol 2007;17:363-370 (Pubitemid 47537593)
40. Tepel M, Roerig P, Wolter M, Gutmann DH, Perry A, Reifenberger G, Riemenschneider MJ. Frequent promoter hypermethylation and transcriptional downregulation of the NDRG2 gene at 14q11.2 in primary glioblastoma. Int J Cancer 2008;123:2080-2086
41. Mulero-Navarro S, Esteller M. Epigenetic biomarkers for human cancer: the time is now. Crit Rev Oncol Hematol 2008;68:1-11.
42. Yang X, Phillips DL, Ferguson AT, Nelson WG, Herman JG, Davidson NE. Synergistic activation of functional estrogen receptor (ER)-alpha by DNA methyltransferase and histone deacetylase inhibition in human ER-alpha-negative breast cancer cells. Cancer Res 2001;61:7025-7029 (Pubitemid 32946489)
43. Baylin SB and Ohm JE. Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 2006;6:107-116
44. Yu JM, Jun ES, Jung JS, Suh SY, Han JY, Kim JY, Kim KW, Jung JS. Role of Wnt5a in the proliferation of human glioblastoma cells. Cancer Lett 2007;257:172-181 (Pubitemid 47538822)
45. Mizobuchi Y, Matsuzaki K, Kuwayama K, Kitazato K, Mure H, Kageji T, Nagahiro S. REIC/Dkk-3 induces cell death in human malignant glioma. Neuro Oncol 2008;10:244-253