Hypermethylation-mediated reduction of WWOX expression in intraductal papillary mucinous neoplasms of the pancreas

British Journal of Cancer

Volumn 100, Issue 9, 2009, Pages 1438-1443

  Nakayama, S ^a   Semba, S ^a   Maeda, N ^a   Matsushita, M ^a   Kuroda, Y ^a   Yokozaki, H ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Hypermethylation; Intraductal papillary mucinous neoplasm of the pancreas; SMAD4; WW domain containing oxidoreductase

Indexed keywords

KI 67 ANTIGEN; OXIDOREDUCTASE; SMAD4 PROTEIN; DNA; SINGLE STRANDED DNA; TUMOR SUPPRESSOR PROTEIN; WWOX PROTEIN, HUMAN;

ADULT; AGED; APOPTOSIS; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTRADUCTAL PAPILLARY MUCINOUS TUMOR; LABELING INDEX; MALE; METHYLATION; PANCREAS ADENOMA; PANCREAS CARCINOMA; PANCREAS DUCT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE; WW DOMAIN CONTAINING OXIDOREDUCTASE GENE; COLLOID CARCINOMA; DNA METHYLATION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETICS; PANCREAS TUMOR; PAPILLARY CARCINOMA; PATHOLOGY; TUMOR CELL LINE;

ADENOCARCINOMA, MUCINOUS; AGED; CARCINOMA, PAPILLARY; CELL LINE, TUMOR; DNA METHYLATION; DNA, NEOPLASM; DNA, SINGLE-STRANDED; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; OXIDOREDUCTASES; PANCREATIC NEOPLASMS; POLYMERASE CHAIN REACTION; SUPPRESSION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 65549119551     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6604986     Document Type: Article

References (31)

1. Aqeilan RI, Palamarchuk A, Weigel RJ, Herrero JJ, Pekařsky Y, Croce CM (2004b) Physical and functional interactions between the Wwox tumor suppressor protein and the AP-2y transcription factor. Cancer Res 64: 8256-8261
2. Aqeilan RI, Pekařsky Y, Herrero JJ, Palamarchuk A, Letofsky J, Druck T, Trapasso F, Han SY, Melino G, Huebner K, Croce CM (2004a) Functional association between Wwox tumor suppressor protein and p73, a p53 homolog. Proc Natl Acad Sei USA 101: 401-406
3. Aqeilan RI, Trapasso F, Hussain S, Costinean S, Marshall D, Pekařsky Y, Hagan JP, Zanesi N, Kaou M, Stein GS, Lian JB, Croce CM (2007) Targeted deletion of Wwox reveals a tumor suppressor function. Proc Natl Acad Sei USA 104: 3949-3954
4. Driouch K, Prydz H, Monese R, Johansen H, Lidereau R, Frengen E (2002) Alternative transcripts of the candidate tumor suppressor gene, WWOX, are expressed at high levels in human breast tumors. Oncogene 21: 1832-1840
5. Fabbri M, Iliopoulos D, Trapasso F, Aqeilan RI, Cimmino A, Zanesi N, Yendamuri S, Han SY, Amadori D, Huebner K, Croce CM (2005) WWOX gene restoration prevents lung cancer growth in vitro and in vivo. Proc NatlAcadSci USA 102: 15611-15616
6. Fukushige S, Furukawa T, Satoh K, Sunamura M, Kobari M, Koizumi M, Horii A (1998) Loss of chromosome 18q is an early event in pancreatic duct tumorigenesis. Cancer Res 58: 4222-4226
7. Hahn SA, Schutte M, Hoque AT, Moskaluk CA, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH, Kern SE (1996) DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271: 350-353
8. Hruban RH, Goggins M, Parsons J, Kern SE (2000) Progression model for pancreatic cancer. Clin Cancer Res 6: 2969-2972
9. Hruban RH, Takaori K, Klimstra DS, Adsay NV, Albores-Saavedra J, Biankin AV, Biankin SA, Compton C, Fukushima N, Furukawa T, Goggins M, Kato Y, Klöppel G, Longnecker DS, Lüttges J, Maitra A, Offerhaus GJ, Shimizu M, Yonezawa S (2004) An illustrated consensus on the classification of pancreatic intraepithelial neoplasia and intraductal papillary mucinous neoplasms. Am J Surg Pathol 28: 977-987
10. Iliopoulos D, Guler G, Han SY, Druck T, Ottey M, McCorkell KA, Huebner K (2006) Roles of FHIT and WWOX fragile genes in cancer. Cancer Lett 232: 27-36
11. Iliopoulos D, Guler G, Han SY, Johnston D, Druck T, McCorkell KA, Palazzo J, McCue PA, Baffa R, Huebner K (2005) Fragile genes as biomarkers: epigenetic control of WWOX and FHIT in lung, breast and bladder cancer. Oncogene 24: 1625-1633
12. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, Ji H, Potash JB, Sabunciyan S, Feinberg AP (2009) The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 41: 178-186
13. Japan Pancreas Society (2003) Classification of Pancreatic Carcinoma. 2nd edn, Kanehara: Tokyo
14. Kawarada Y, Miura N, Sugiyama T (1998) Antibody against single-stranded DNA useful for detecting apoptotic cells recognizes hexadeoxynucleotides with various base sequences. J Biochem 123: 492-498
15. Kuroki T, Trapasso F, Shiraishi T, Alder H, Mimori K, Mori M, Croce CM (2002) Genetic alterations of the tumor suppressor gene WWOX in esophageal squamous cell carcinoma. Cancer Res 62: 2258-2260
16. Kuroki T, Yendamuri S, Trapasso F, Matsuyama A, Aqeilan RI, Alder H, Rattan S, Cesari R, Nolli ML, Williams NN, Mori M, Kanematsu T, Croce CM (2004) The tumor suppressor gene WWOX at FRA16D is involved in pancreatic carcinogenesis. Clin Cancer Res 10: 2459-2465
17. Morèn A, Hellman U, Inada Y, Imamura T, Heldin CH, Moustakas A (2003) Differential ubiquitination defines the functional status of the tumor suppressor Smad4. J Biol Chem 278: 33571 -33582
18. Morèn A, Imamura T, Miyazono K, Heldin CH, Moustakas A (2005) Degradation of the tumor suppressor Smad4 by WW and HECT domain ubiquitin ligases. J Biol Chem 280: 22115-22123
19. Nakayama S, Semba S, Maeda N, Aqeilan RI, Huebner K, Yokozaki H (2008) Role of the WWOX gene, encompassing fragüe region FRA16D, in suppression of pancreatic carcinoma cells. Cancer Sei 99: 1370-1376
20. Paige AJ, Taylor C, Taylor C, Hillier SG, Farrington S, Scott D, Porteous DJ, Smyth JF, Gabra H, Watson JE (2001) WWOX: a candidate tumor suppressor gene involved in multiple tumor types. Proc Natl Acad Sei USA 98: 11417-11422
21. Qin HR, Iliopoulos D, Semba S, Fabbri M, Druck T, Volinia S, Croce CM, Morrison CD, Klein RD, Huebner K (2006) A role for the WWOX gene in prostate cancer. Cancer Res 66: 6477-6481
22. Schönleben F, Qiu W, Bruckman KC, Ciau NT, Li X, Lauerman MH, Frucht H, Chabot JA, Allendorf JD, Remotti HE, Su GH (2007) BRAF and KRAS gene mutations in intraductal papillary mucinous neoplasia/carcinoma (IPMN/IPMC) of the pancreas. Cancer Lett 249: 242-248
23. Schönleben F, Qiu W, Ciau NT, Ho DJ, Li X, Allendorf JD, Remotti HE, Su GH (2006) PI3CA mutations in intraductal papillary mucinous neoplasm/ carcinoma of the pancreas. Clin Cancer Res 12: 3851-3855
24. Semba S, Moriya T, Kimura W, Yamakawa M (2003) Phosphorylated Akt/ PKB controls cell growth and apoptosis in intraductal papillarymucinous tumor and invasive ductal adenocarcinoma of the pancreas. Pancreas 26: 250-257
25. Sessa F, Solcia E, Capella C, Bonato M, Scarpa A, Zamboni G, Pellegata NS, Ranzani GN, Rickaert F, Klöppel G (1994) Intraductal papillarymucinous tumours represent a distinct group of pancreatic neoplasms: an investigation of tumour cell differentiation and K-ras, p53 and c-erbB2 abnormalities in 26 patients. Virchows Arch 425: 357-367
26. Sohn TA, Yeo CJ, Cameron JL, Iacobuzio-Donahue CA, Hruban RH, Lillemoe KD (2001) Intraductal papillary mucinous neoplasms of the pancreas: an increasingly recognized clinicopathologic entity. Ann Surg 234:313-321
27. Takahashi H, Oda T, Hasebe T, Aoyagi Y, Kinoshita T, Konishi M, Nakagohri T, Inoue K, Takahashi S, Kawahira H, Monden M, Ochiai A (2004) Biologically different subgroups of invasive ductal carcinoma of the pancreas: Dpc4 status according to the ratio of intraductal carcinoma components. Clin Cancer Res 10: 3772-3779
28. Watanabe I, Toyoda M, Okuda J, Tenjo T, Tanaka K, Yamamoto T, Kawasaki H, Sugiyama T, Kawarada Y, Tanigawa N (1999) Detection of apoptotic cells in human colorectal cancer by two different in situ methods: antibody against single-stranded DNA and terminal deoxynucleotidyl transferase-mediated dUTP-biotin nick end-labeling (TUNEL) methods. Jpn J Cancer Res 90: 188-193
29. Wilentz RE, Su GH, Dai JL, Sparks AB, Argani P, Sohn TA, Yeo CJ, Kern S (2000) Immunohistochemical labeling for dpc4 mirrors genetic status in pancreatic adenocarcinomas: a new marker of DPC4 inactivation. Am J Pathol 156: 37-43
30. Yamao K, Ohashi K, Nakamura T, Suzuki T, Shimizu Y, Nakamura Y, Horibe Y, Yanagisawa A, Nakao A, Nimuara Y, Naito Y, Hayakawa T (2000) The prognosis of intraductal papillary mucinous tumors of the pancreas. Hepatogastroenterology 47: 1129-1134
31. Z'graggen K, Rivera JA, Compton CC, Pins M, Werner J, Fernandez-del Castillo C, Rattner DW, Lewandrowski KB, Rustgi AK, Warshaw AL (1997) Prevalence of activating K-ras mutations in the evolutionary stages of neoplasia in intraductal papillary mucinous tumors of the pancreas. Ann Surg 226: 491 -498