Van-Gogh-like 2 antagonises the canonical WNT pathway and is methylated in colorectal cancers

British Journal of Cancer

Volumn 108, Issue 8, 2013, Pages 1750-1756

  Piazzi, G ^a,b,c   Selgrad, M ^a,d   Garcia, M ^a   Ceccarelli, C ^b   Fini, L ^a,e   Bianchi, P ^e   Laghi, L ^e   D'Angelo, L ^b   Paterini, P ^d   Malfertheiner, P ^d   Chieco, P ^b   Boland, C R ^a   Bazzoli, F ^c   Ricciardiello, L ^a,b,c  

^a BAYLOR RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

^e HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; B RAF KINASE; BETA CATENIN; DNA; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG; VAN GOGH LIKE 2 PROTEIN;

AGED; ARTICLE; ASCENDING COLON; CANCER INHIBITION; CELL PROLIFERATION; CLONOGENESIS; COLONY FORMATION; COLORECTAL CANCER; CONTROLLED STUDY; ENZYME ACTIVATION; EPIGENETICS; FEMALE; GENE OVEREXPRESSION; GENETIC REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN METHYLATION; WNT SIGNALING PATHWAY;

AGED; AZACITIDINE; BETA CATENIN; CACO-2 CELLS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DNA METHYLATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HCT116 CELLS; HT29 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MICROSATELLITE INSTABILITY; MUTATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS B-RAF; RNA, MESSENGER; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84877031028     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.142     Document Type: Article

References (38)

1. Aguilera O, Fraga MF, Ballestar E, Paz MF, Herranz M, Espada J, Garcia JM, Munoz A, Esteller M, Gonzalez-Sancho JM (2006) Epigenetic inactivation of the Wnt antagonist DICKKOPF-1 (DKK-1) gene in human colorectal cancer. Oncogene 25(29): 4116-4121.
2. Barrow JR (2006) Wnt/PCP signaling: a veritable polar star in establishing patterns of polarity in embryonic tissues. Semin Cell Dev Biol 17(2): 185-193.
3. Baylin SB, Ohm JE (2006) Epigenetic gene silencing in cancer-a mechanism for early oncogenic pathway addiction Nat Rev Cancer 6(2): 107-116.
4. Boland CR, Goel A (2010) Microsatellite instability in colorectal cancer. Gastroenterology 138(6): 2073-2087 e3.
5. Boland CR, Thibodeau SN, Hamilton SR, Sidransky D, Eshleman JR, Burt RW, Meltzer SJ, Rodriguez-Bigas MA, Fodde R, Ranzani GN, Srivastava S (1998) A National cancer institute workshop on microsatellite instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res 58(22): 5248-5257.
6. Cantrell VA, Jessen JR (2010) The planar cell polarity protein Van Gogh-Like 2 regulates tumor cell migration and matrix metalloproteinase- dependent invasion. Cancer Lett 287(1): 54-61.
7. Gao B, Song H, Bishop K, Elliot G, Garrett L, English MA, Andre P, Robinson J, Sood R, Minami Y, Economides AN, Yang Y (2011) Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev Cell 20(2): 163-176.
8. Grady WM, Carethers JM (2008) Genomic and epigenetic instability in colorectal cancer pathogenesis. Gastroenterology 135(4): 1079-1099.
9. Greenacre M (1984) Theory and Applications of Correspondence Analysis. London: Academic Press.
10. Hiltunen MO, Alhonen L, Koistinaho J, Myohanen S, Paakkonen M, Marin S, Kosma VM, Janne J (1997) Hypermethylation of the APC (adenomatous polyposis coli) gene promoter region in human colorectal carcinoma. Int J Cancer 70(6): 644-648.
11. Iliescu A, Gravel M, Horth C, Apuzzo S, Gros P (2011) Transmembrane topology of mammalian planar cell polarity protein Vangl1. Biochemistry 50(12): 2274-2282.
12. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, Goldman H, Jessup JM, Kolodner R (1997) Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res 57(5): 808-811.
13. Kibar Z, Salem S, Bosoi CM, Pauwels E, De Marco P, Merello E, Bassuk AG, Capra V, Gros P (2011) Contribution of VANGL2 mutations to isolated neural tube defects. Clin Genet 80(1): 76-82.
14. Kibar Z, Vogan KJ, Groulx N, Justice MJ, Underhill DA, Gros P (2001) Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat Genet 28(3): 251-255.
15. Laghi L, Bianchi P, Malesci A (2008) Differences and evolution of the methods for the assessment of microsatellite instability. Oncogene 27(49): 6313-6321.
16. Lara E, Calvanese V, Huidobro C, Fernandez AF, Moncada-Pazos A, Obaya AJ, Aguilera O, Gonzalez-Sancho JM, Sanchez L, Astudillo A, Munoz A, Lopez-Otin C, Esteller M, Fraga MF (2010) Epigenetic repression of ROR2 has a Wnt-mediated, pro-tumourigenic role in colon cancer. Mol Cancer 9: 170.
17. Lei YP, Zhang T, Li H, Wu BL, Jin L, Wang HY (2010) VANGL2 mutations in human cranial neural-tube defects. N Engl J Med 362(23): 2232-2235.
18. Li S, Esterberg R, Lachance V, Ren D, Radde-Gallwitz K, Chi F, Parent JL, Fritz A, Chen P (2011) Rack1 is required for Vangl2 membrane localization and planar cell polarity signaling while attenuating canonical Wnt activity. Proc Natl Acad Sci USA 108(6): 2264-2269.
19. Lindqvist M, Horn Z, Bryja V, Schulte G, Papachristou P, Ajima R, Dyberg C, Arenas E, Yamaguchi TP, Lagercrantz H, Ringstedt T (2010) Vang-like protein 2 and Rac1 interact to regulate adherens junctions. J Cell Sci 123(Pt 3): 472-483.
20. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810.
21. Oishi I, Suzuki H, Onishi N, Takada R, Kani S, Ohkawara B, Koshida I, Suzuki K, Yamada G, Schwabe GC, Mundlos S, Shibuya H, Takada S, Minami Y (2003) The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8(7): 645-654.
22. Pino MS, Chung DC (2010) The chromosomal instability pathway in colon cancer. Gastroenterology 138(6): 2059-2072.
23. Rawson JB, Mrkonjic M, Daftary D, Dicks E, Buchanan DD, Younghusband HB, Parfrey PS, Young JP, Pollett A, Green RC, Gallinger S, McLaughlin JR, Knight JA, Bapat B (2011) Promoter methylation of Wnt5a is associated with microsatellite instability and BRAF V600E mutation in two large populations of colorectal cancer patients. Br J Cancer 104(12): 1906-1912.
24. Reya T, Clevers H (2005) Wnt signalling in stem cells and cancer. Nature 434(7035): 843-850.
25. Ricciardiello L, Ceccarelli C, Angiolini G, Pariali M, Chieco P, Paterini P, Biasco G, Martinelli GN, Roda E, Bazzoli F (2005) High thymidylate synthase expression in colorectal cancer with microsatellite instability: implications for chemotherapeutic strategies. Clin Cancer Res 11(11): 4234-4240.
26. Segditsas S, Tomlinson I (2006) Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene 25(57): 7531-7537.
27. Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA Cancer J Clin 62(1): 10-29.
28. Sinicrope FA, Sargent DJ (2012) Molecular pathways: microsatellite instability in colorectal cancer: prognostic, predictive, and therapeutic implications. Clin Cancer Res 18(6): 1506-1512.
29. 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, Hinoda Y, Imai K, Herman JG, Baylin SB (2004) Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 36(4): 417-422.
30. Taniguchi H, Yamamoto H, Hirata T, Miyamoto N, Oki M, Nosho K, Adachi Y, Endo T, Imai K, Shinomura Y (2005) Frequent epigenetic inactivation of Wnt inhibitory factor-1 in human gastrointestinal cancers. Oncogene 24(53): 7946-7952.
31. Taylor J, Abramova N, Charlton J, Adler PN (1998) Van Gogh: a new Drosophila tissue polarity gene. Genetics 150(1): 199-210.
32. Torban E, Wang HJ, Groulx N, Gros P (2004) Independent mutations in mouse Vangl2 that cause neural tube defects in looptail mice impair interaction with members of the Dishevelled family. J Biol Chem 279(50): 52703-52713.
33. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP (1999) CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 96(15): 8681-8686.
34. Veeman MT, Axelrod JD, Moon RT (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5(3): 367-377.
35. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, Kang GH, Widschwendter M, Weener D, Buchanan D, Koh H, Simms L, Barker M, Leggett B, Levine J, Kim M, French AJ, Thibodeau SN, Jass J, Haile R, Laird PW (2006) CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 38(7): 787-793.
36. Williams BB, Cantrell VA, Mundell NA, Bennett AC, Quick RE, Jessen JR (2012) VANGL2 regulates membrane trafficking of MMP14 to control cell polarity and migration. J Cell Sci 125(Pt 9): 2141-2147.
37. Wolff T, Rubin GM (1998) Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125(6): 1149-1159.
38. Ying J, Li H, Yu J, Ng KM, Poon FF, Wong SC, Chan AT, Sung JJ, Tao Q (2008) WNT5A exhibits tumor-suppressive activity through antagonizing the Wnt/beta-catenin signaling, and is frequently methylated in colorectal cancer. Clin Cancer Res 14(1): 55-61.