Epigenetic silencing of DKK3 in medulloblastoma

International Journal of Molecular Sciences

Volumn 14, Issue 4, 2013, Pages 7492-7505

  Valdora, Francesca ^a   Banelli, Barbara ^a   Stigliani, Sara ^a   Pfister, Stefan M ^b,c   Moretti, Stefano ^d,e   Kool, Marcel ^b   Remke, Marc ^b,f   Bai, Alfa H C ^g   Brigati, Claudio ^a   Hielscher, Thomas ^b   Romani, Massimo ^a   Servidei, Tiziana ^h   Zollo, Massimo ⁱ   Cinalli, Giuseppe ^j   Oberthuer, André ^k   Tonini, Gian Paolo ^l   Coco, Simona ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^d Centre National de la Recherche Scientifique   (France)

^e UNIVERSITÉ PARIS DAUPHINE   (France)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

^g CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^h CATHOLIC UNIVERSITY   (Italy)

ⁱ CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^j SANTOBONO PAUSILIPON CHILDREN S HOSPITAL   (Italy)

^k UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^l UNIVERSITY OF PADOVA   (Italy)

more..

Author keywords

DKK family; DKK3 downregulation; Histone deacetylase; Medulloblastoma; TSA; Wnt antagonists

Indexed keywords

DICKKOPF 1 PROTEIN; DICKKOPF 3 PROTEIN; GLYCOPROTEIN; MESSENGER RNA; MICRORNA; TRICHOSTATIN A; UNCLASSIFIED DRUG; WNT PROTEIN; DKK3 PROTEIN, HUMAN; RNA; SIGNAL PEPTIDE; TUMOR PROTEIN;

ARTICLE; CHROMATIN CONDENSATION; COMPUTER MODEL; CONTROLLED STUDY; COPY NUMBER VARIATION; DICKKOPF 1 GENE; DICKKOPF 2 GENE; DICKKOPF 3 GENE; DICKKOPF 4 GENE; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LOCUS; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; GENETIC SCREENING; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MEDULLOBLASTOMA; NEGATIVE FEEDBACK; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; ADOLESCENT; ADULT; AGED; BIOSYNTHESIS; CHILD; CHROMATIN ASSEMBLY AND DISASSEMBLY; FEMALE; GENETIC DATABASE; GENETICS; INFANT; MALE; METABOLISM; METHYLATION; MIDDLE AGED; PATHOLOGY; PRESCHOOL CHILD; TUMOR CELL LINE;

ADOLESCENT; ADULT; AGED; CELL LINE, TUMOR; CHILD; CHILD, PRESCHOOL; CHROMATIN ASSEMBLY AND DISASSEMBLY; DATABASES, GENETIC; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; INFANT; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEDULLOBLASTOMA; METHYLATION; MIDDLE AGED; NEOPLASM PROTEINS; RNA, MESSENGER; RNA, NEOPLASM;

EID: 84875995033     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14047492     Document Type: Article

References (36)

1. Packer, R.J.; Cogen, P.; Vezina, G.; Rorke, L.B. Medulloblastoma: Clinical and biologic aspects. Neuro Oncol. 1999, 1, 232-250.
2. Kool, M.; Koster, J.; Bunt, J.; Hasselt, N.E.; Lakeman, A.; van Sluis, P.; Troost, D.; Meeteren, N.S.; Caron, H.N.; Cloos, J.; et al. Integrated genomics identifies five medulloblastoma subtypes with distinct genetic profiles, pathway signatures and clinicopathological features. PLoS One 2008, 3, 3088.
3. Northcott, P.A.; Korshunov, A.; Witt, H.; Hielscher, T.; Eberhart, C.G., Mack, S.; Bouffet, E.; Clifford, S.C.; Hawkins, C.E.; French, P.; et al. Medulloblastoma comprises four distinct molecular variants. J. Clin. Oncol. 2011, 10, 1408-1414.
4. Cho, Y.J.; Tsherniak, A.; Tamayo, P.; Santagata, S.; Ligon, A.; Greulich, H.; Berhoukim, R.; Amani, V.; Goumnerova, L.; Eberhart, C.G.; et al. Integrative genomic analysis of medulloblastoma identifies a molecular subgroup that drives poor clinical outcome. J. Clin. Oncol. 2011, 29, 1424-1430.
5. Remke, M.; Hielscher, T.; Korshunov, A.; Nothcott, P.A.; Bender, S.; Kool, M.; Westermann, F.; Benner, A.; Ryzhova, M.; Sturm, D.; et al. FSTL5 is a marker of poor prognosis in non-Wnt/non. SHH Medulloblastoma. J. Clin. Oncol. 2011, 29, 3852-3861.
6. Polkinghorn, W.R. Tarbel, N.J. Medulloblastoma: Tumorigenesis, current clinical paradigm, and efforts to improve risk stratification. Nat. Clin. Pract. Oncol. 2007, 4, 295-304.
7. Taylor, M.D.; Northcott, P.A.; Korshunov, A.; Remke, M.; Cho, Y.J.; Clifford, S.C.; Eberhart, C.G.; Parsons, D.W.; Rutkowski, S.; Gajjar, A.; et al. Molecular subgroups of medulloblastoma: The current consensus. Acta Neuropathol. 2012, 123, 465-472.
8. Kool, M.; Korshunov, A.; Remke, M.; Jones, D.T.; Schlanstein, M.; Northcott, P.A.; Cho, Y.J.; Koster, J.; Schouten-van Meeteren, A.; van Vuurden, D.; et al. Molecular subgroups of medulloblastoma: An international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, Group 3, and Group 4 medulloblastomas. Acta Neuropathol. 2012, 123, 473-484.
9. Marino, S. Medulloblastoma: Developmental mechanisms out of control. Trends Mol. Med. 2005, 11, 17-22.
10. Kawano, Y.; Kypta, R. Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 2003, 116, 2627-2634.
11. Katoh, M.; Katoh, M. WNT signaling pathway and stem cell signaling network. Clin. Cancer Res. 2007, 13, 4042-4045.
12. Kobayashi, K.; Ouchida, M.; Tsuji, T.; Hanafusa, H.; Miyazaki, M.; Namba, M.; Shimizu, N.; Shimizu, K. Reduced expression of the REIC/Dkk3 gene by promoter-hypermethylation in human tumor cells. Gene 2002, 2, 151-158.
13. Hsieh, S.Y.; Hsieh, P.S.; Chiu, C.-T.; Chen, W.Y. Dickkopf-3/REIC functions as a suppressor gene of tumor growth. Oncogene 2004, 2, 9183-9189.
14. Kuphal, S.; Lodermeyer, S.; Bataille, F.; Schuierer, M.; Hoang, B.H.; Bosserhoff, A.K. Expression of Dickkopf genes is strongly reduced in malignant Melanoma. Oncogene 2006, 25, 5027-5036.
15. Chung, M.T.; Lai, H.C.; Sytwu, H.K.; Yan, M.D.; Shih, Y.L.; Chang, C.C.; Yu, M.H.; Liu, H.S.; Chu, D.W.; Lin, Y.W. SFRP1 and SFRP2 suppress the transformation and invasion abilities of cervical cancer cells through Wnt signaling pathway. Ginecol. Oncol. 2009, 112, 646-653.
16. Sato, H.; Suzuki, H.; Toyotak, M.; Nojima, M.; Maruyama, R.; Sasaki, S.; Takagi, H.; Sogabe, Y.; Sasaki, Y.; Idogawa, M.; et al. Frequent epigenetic inactivation of DICKKOPF family genes in human gastrointestinal tumors. Carcinogenesis 2007, 28, 2459-2466.
17. Vibhakar, R.; Foltz, G.; Yoon, J.G.; Field, L.; Lee, H.; Ryu, G.Y.; Pierson, J.; Davidson, B.; Madan, A. Dickkopf-1 is an epigenetically silenced candidate tumor suppressor gene in medulloblastoma. Neuro Oncol. 2007, 4, 135-144.
18. Facchetti, F.; Previdi, S.; Ballarini, M.; Minucci, S.; Perego, P.; La Porta, C.A. Modulation of proand anti-apoptotic factors in human melanoma cells exposed to histone deacetylase inhibitors. Apoptosis 2004, 9, 573-582.
19. Yoshikawa, M.; Hishikawa, K.; Idei, M.; Fujita, T. Trichostatin a prevents TGF-beta1-induced apoptosis by inhibiting ERK activation in human renal tubular epithelial cells. Eur. J. Pharmacol. 2010, 642, 28-36.
20. Roth, R.B.; Hevezi, P.; Lee, J.; Willhite, D.; Lechner, S.M.; Foster, A.C.; Zlotnik, A. Gene expression analyses reveal molecular relationships among 20 regions of the human CNS. Neurogenetics 2006, 7, 67-80.
21. Northcott, P.A.; Shih, D.J.; Peacock, J.; Garzia, L.; Morrissy, A.S.; Zichner, T.; Stütz, A.M.; Korshunov, A.; Reimand, J.; Schumacher, S.E.; et al. Subgroup-specific structural variation across 1000 medulloblastoma genomes. Nature 2012, 488, 49-56.
22. Haug, B.H.; Henriksen, J.R.; Buechner, J.; Geerts, D.; Tømte, E.; Kogner, P.; Martinsson, T.; Flægstad, T.; Sveinbjørnsson, B.; Einvik, C. MYCN-regulated miRNA-92 inhibits secretion of the tumor suppressor DICKKOPF-3 (DKK3) in neuroblastoma. Carcinogenesis 2011, 32, 1005-1012.
23. Aldosari, N.; Bigner, S.H.; Burger, P.C.; Becker, L.; Kepner, J.L.; Friedman, H.S.; McLendon, R.E. MYCC and MYCN oncogene amplification in medulloblastoma. A fluorescence in situ hybridization study on paraffin sections from the Children's Oncology Group. Arch. Pathol. Lab. Med. 2002, 126, 540-544.
24. Kongkham, P.N.; Northcott, P.A.; Croul, S.E.; Smith, C.A.; Taylor, M.D.; Rutka, J.T. The SFRP family of WNT inhibitors function as novel tumor suppressor genes epigenetically silenced in medulloblastoma. Oncogene 2010, 29, 3017-3024.
25. Häcker, S.; Dittrich, A.; Mohr, A.; Schweitzer, T.; Rutkowski, S.; Krauss, J.; Debatin, K.M.; Fulda, S. Histone deacetylase inhibitors cooperate with IFN-gamma to restore caspase-8 expression and overcome TRAIL resistance in cancers with silencing of caspase-8. Oncogene 2009, 28, 3097-3110.
26. Yang, B.; Du, Z.; Gao, Y.T.; Lou, C.; Zhang, S.G.; Bai, T.; Wang, Y.J.; Song, W.Q. Methylation of Dickkopf-3 as a prognostic factor in cirrhosis-related hepatocellular carcinoma. World J. Gastroenterol. 2010, 16, 755-763.
27. Roman-Gomez, J.; Jimenez-Velasco, A.; Agirre, X.; Castillejo, J.A.; Navarro, G.; Barrios, M.; Andreu, E.J.; 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.
28. Veeck, J.; Bektas, N.; Hartmann, A.; Kristiansen, G.; Heindrichs, U.; Knuchel, R.; Dahl, E. Wnt signalling in human breast cancer: Expression of the putative Wnt inhibitor Dickkopf-3 (DKK3) is frequently suppressed by promoter hypermethylation in mammary tumours. Breast Cancer Res. 2008, 10, R82.
29. Cameron, E.E.; Bachman, K.E.; Myöhänen, S.; Herman, J.G.; Baylin, S.B. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet. 1999, 21, 103-107.
30. Brigati, C.; Banelli, B.; Casciano, I.; di Vinci, A.; Matis, S.; Cutrona, G.; Forlani, A.; Allemanni, G.; Romani, M. Epigenetic mechanisms regulate ΔNP73 promoter function in human tonsil B cells. Mol. Immunol. 2011, 48, 408-414.
31. Coco, S.; Valdora, F.; Bonassi, S.; Scaruffi, P.; Stigliani, S.; Oberthuer, A.; Berthold, F.; Adolfo, I.; Servidei, T.; Riccardi, R.; et al. Chromosome 9q and 16q loss identified by genome-wide pooled analysis are associated with tumor aggressiveness in patients with classic medulloblastoma. J. Integr. Biol. 2011, 15, 273-280.
32. Pfister, S.M.; Remke, M.; Benner, A.; Mendrzyk, F.; Toedt, G.; Felsberg, J.; Wittmann, A.; Devens, F.; Gerber, N.U.; Joos, S.; et al. Outcome prediction in pediatric medulloblastoma based on DNA copy-number aberrations of chromosomes 6q and 17q and the MYC and MYCN loci. J. Clin. Oncol. 2009, 27, 1627-1636.
33. Banelli, B.; Bonassi, S.; Casciano, I.; Mazzocco, K.; di Vinci, A.; Scaruffi, P.; Brigati, C.; Allemanni, G.; Borzì, L.; Tonini, G.P.; et al. Outcome prediction and risk assessment by quantitative pyrosequencing methylation analysis of the SFN gene advanced stage, high-risk, neuroblastic tumor patients. Int. J. Cancer. 2010, 126, 656-668.
34. Del Grosso, F.; Coco, S.; Scaruffi, P.; Stigliani, S.; Valdora, F.; Benelli, R.; Salvi, S.; Boccardo, S.; Truini, M.; Croce, M.; et al. Role of CXCL13-CXCR5 crosstalk between malignant neuroblastoma cells and Schwannian stromal cells in neuroblastic tumors. Mol. Cancer Res. 2011, 9, 815-823.
35. Giangaspero, F.; Eberhart, C.; Haapasalo, H.; Pietsch, T.; Wiestler, O.D.; Ellison, D.W. Medulloblastoma. In WHO Classification of Tumours of the Central Nervous System; Louis, D.N., Ohgaki, H., Wiestler, O.D., Cavenee, W.K., Eds.; IARC Press: Lyon, France, 2007.
36. Chang, C.H.; Housepian, E.M.; Herbert, C., Jr. An operative staging system and a megavoltage radiotherapeutic technic for cerebellar medulloblastomas. Radiology 1969, 93, 13561-1359.