Silencing of wnt5a during colon cancer metastasis involves histone modifications

Epigenetics

Volumn 7, Issue 6, 2012, Pages 551-558

  Li, Qian ^a   Chen, Hong ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Cell adhesion; HDAC inhibitor; Sw480; SW620; WNT signaling; catenin

Indexed keywords

ACETYLATED HISTONE H3; ACETYLATED HISTONE H4; AZACITIDINE; BETA CATENIN; BUTYRIC ACID; DIMETHYL HISTONE H3 LYSINE 4; HISTONE H3; HISTONE H4; MESSENGER RNA; TRICHOSTATIN A; TRIMETHYL HISTONE H3 LYSINE 27; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ARTICLE; CANCER CELL; CELL ADHESION; CELL FUNCTION; COLON CANCER; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; HISTONE MODIFICATION; HUMAN; HUMAN CELL; METASTASIS; PROMOTER REGION; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; WNT SIGNALING PATHWAY;

EID: 84861937510     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.20050     Document Type: Article

References (41)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics. CA Cancer J Clin 2010; 60:277-300. PMID:20610543; http://dx.doi.org/10.3322/caac.20073.
2. Segal NH, Saltz LB. Evolving treatment of advanced colon cancer. Annu Rev Med 2009; 60:207-19. PMID:19630571; http://dx.doi.org/10.1146/annurev.med.60.041807.132435.
3. Sheldahl LC, Park M, Malbon CC, Moon RT. Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a G-protein-dependent manner. Curr Biol 1999; 9:695-8. PMID:10395542; http://dx.doi.org/10.1016/S0960-9822(99)80310-8.
4. 2+ signaling by Wnt-5A. Dev Biol 1997; 182:114-20. PMID:9073455; http://dx.doi.org/10.1006/dbio.1996.8463.
5. Umbhauer M, Djiane A, Goisset C, Penzo-Méndez A, Riou JF, Boucaut JC, et al. The C-terminal cytoplasmic Lys-thr-X-X-X-Trp motif in frizzled receptors mediates Wnt/beta-catenin signalling. EMBO J 2000; 19:4944-54. PMID:10990458; http://dx.doi.org/10.1093/emboj/19.18.4944.
6. He X, Saint-Jeannet JP, Wang Y, Nathans J, Dawid I, Varmus H. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 1997; 275:1652-4. PMID:9054360; http://dx.doi.org/10.1126/science.275.5306.1652.
7. Olson DJ, Gibo DM. Antisense wnt-5a mimics wnt-1-mediated C57MG mammary epithelial cell transformation. Exp Cell Res 1998; 241:134-41. PMID:9633521; http://dx.doi.org/10.1006/excr.1998.4030.
8. Yamamoto H, Oue N, Sato A, Hasegawa Y, Yamamoto H, Matsubara A, et al. Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 2010; 29:2036-46. PMID:20101234; http://dx.doi.org/10.1038/onc.2009.496.
9. Da Forno PD, Pringle JH, Hutchinson P, Osborn J, Huang Q, Potter L, et al. WNT5A expression increases during melanoma progression and correlates with outcome. Clin Cancer Res 2008; 14:5825-32. PMID:18794093; http://dx.doi.org/10.1158/1078-0432.CCR-07-5104.
10. Ying J, Li H, Yu J, Ng KM, Poon FF, Wong SC, et al. WNT5A exhibits tumor-suppressive activity through antagonizing the Wnt/beta-catenin signaling, and is frequently methylated in colorectal cancer. Clin Cancer Res 2008; 14:55-61. PMID:18172252; http://dx.doi.org/10.1158/1078-0432.CCR-07-1644.
11. Kremenevskaja N, von Wasielewski R, Rao AS, Schöfl C, Andersson T, Brabant G. Wnt-5a has tumor suppressor activity in thyroid carcinoma. Oncogene 2005; 24:2144-54. PMID:15735754; http://dx.doi. org/10.1038/sj.onc.1208370.
12. Medrek C, Landberg G, Andersson T, Leandersson K. Wnt-5a-CKIalpha signaling promotes beta-catenin/Ecadherin complex formation and intercellular adhesion in human breast epithelial cells. J Biol Chem 2009; 284:10968-79. PMID:19244247; http://dx.doi.org/10.1074/jbc.M804923200.
13. Roman-Gomez J, Jimenez-Velasco A, Cordeu L, Vilas-Zornoza A, San Jose-Eneriz E, Garate L, et al. WNT5A, a putative tumour suppressor of lymphoid malignancies, is inactivated by aberrant methylation in acute lymphoblastic leukaemia. Eur J Cancer 2007; 43:2736-46. PMID:18032022; http://dx.doi.org/10.1016/j.ejca.2007.10.004.
14. Dejmek J, Dejmek A, Säfholm A, Sjölander A, Andersson T. Wnt-5a protein expression in primary dukes B colon cancers identifies a subgroup of patients with good prognosis. Cancer Res 2005; 65:9142-6. PMID:16230369; http://dx.doi.org/10.1158/0008- 5472.CAN-05-1710.
15. Witze ES, Litman ES, Argast GM, Moon RT, Ahn NG. Wnt5a control of cell polarity and directional movement by polarized redistribution of adhesion receptors. Science 2008; 320:365-9. PMID:18420933; http://dx.doi.org/10.1126/science.1151250.
16. Matsumoto S, Fumoto K, Okamoto T, Kaibuchi K, Kikuchi A. Binding of APC and dishevelled mediates Wnt5a-regulated focal adhesion dynamics in migrating cells. EMBO J 2010; 29:1192-204. PMID:20224554; http://dx.doi.org/10.1038/emboj.2010.26.
17. Jensen TJ, Wozniak RJ, Eblin KE, Wnek SM, Gandolfi AJ, Futscher BW. Epigenetic mediated transcriptional activation of WNT5A participates in arsenical-associated malignant transformation. Toxicol Appl Pharmacol 2009; 235:39-46. PMID:19061910; http://dx.doi.org/10.1016/j.taap.2008.10.013.
18. Leibovitz A, Stinson JC, McCombs WB, 3rd, McCoy CE, Mazur KC, Mabry ND. Classification of human colorectal adenocarcinoma cell lines. Cancer Res 1976; 36:4562-9. PMID:1000501.
19. Hewitt RE, McMarlin A, Kleiner D, Wersto R, Martin P, Tsokos MJ, et al. Validation of a model of colon cancer progression. J Pathol 2000; 192:446-54. PMID:11113861; http://dx.doi.org/10.1002/1096- 9896(2000)9999:9999::AID-PATH7753.0.CO;2- K.
20. Hewitt RE, Brown KE, Corcoran M, Stetler-Stevenson WG. Increased expression of tissue inhibitor of metalloproteinases type 1 (TIMP-1) in a more tumourigenic colon cancer cell line. J Pathol 2000; 192:455-9. PMID:11113862; http://dx.doi.org/10.1002/1096- 9896(2000)9999:9999::AID-PATH7773.0.CO;2- E.
21. Li Q, Chen H. Transcriptional silencing of N-Myc downstream-regulated gene 1 (NDRG1) in metastatic colon cancer cell line SW620. Clin Exp Metastasis 2011; 28:127-35. PMID:21184144; http://dx.doi.org/10.1007/s10585-010-9366-4.
22. Rodenhiser DI. Epigenetic contributions to cancer metastasis. Clin Exp Metastasis 2009; 26:5-18. PMID:18386135; http://dx.doi.org/10.1007/s10585-008-9166-2.
23. Chik F, Szyf M, Rabbani SA. Role of epigenetics in cancer initiation and progression. Adv Exp Med Biol 2011; 720:91-104. PMID:21901621; http://dx.doi.org/10.1007/978-1-4614-0254-1_8.
24. Li Q, Chen H. Epigenetic modifications of metastasis suppressor genes in colon cancer metastasis. Epigenetics 2011; 6:849-52. PMID:21758003; http://dx.doi.org/10.4161/epi.6.7.16314.
25. von Burstin J, Eser S, Paul MC, Seidler B, Brandl M, Messer M, et al. E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/ HDAC1/HDAC2 repressor complex. Gastroenterology 2009; 137:361-71. PMID:19362090; http://dx.doi. org/10.1053/j.gastro.2009.04.004.
26. Su HY, Lai HC, Lin YW, Liu CY, Chen CK, Chou YC, et al. Epigenetic silencing of SFRP5 is related to malignant phenotype and chemoresistance of ovarian cancer through Wnt signaling pathway. Int J Cancer 2010; 127:555-67. PMID:19957335; http://dx.doi.org/10.1002/ijc.25083.
27. Kawakami K, Yamamura S, Hirata H, Ueno K, Saini S, Majid S, et al. Secreted frizzled-related protein- 5 is epigenetically downregulated and functions as a tumor suppressor in kidney cancer. Int J Cancer 2011; 128:541-50. PMID:20340127; http://dx.doi.org/10.1002/ijc.25357.
28. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007; 129:823-37. PMID:17512414; http://dx.doi.org/10.1016/j.cell.2007.05.009.
29. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006; 441:349-53. PMID:16625203; http://dx.doi.org/10.1038/nature04733.
30. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet 2008; 40:741-50. PMID:18488029; http://dx.doi.org/10.1038/ng.159.
31. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007; 39:232-6. PMID:17200670; http://dx.doi.org/10.1038/ng1950.
32. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001; 410:120-4. PMID:11242054; http://dx.doi.org/10.1038/35065138.
33. Prigent C, Dimitrov S. Phosphorylation of serine 10 in histone H3, what for? J Cell Sci 2003; 116:3677-85. PMID:12917355; http://dx.doi.org/10.1242/ jcs.00735.
34. Nowak SJ, Corces VG. Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet 2004; 20:214-20. PMID:15041176; http://dx.doi.org/10.1016/j.tig.2004.02.007.
35. Kim HJ, Bae SC. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am J Transl Res 2011; 3:166-79. PMID:21416059.
36. Mossman D, Scott RJ. Long term transcriptional reactivation of epigenetically silenced genes in colorectal cancer cells requires DNA hypomethylation and histone acetylation. PLoS One 2011; 6:23127. PMID:21829702; http://dx.doi.org/10.1371/journal.pone.0023127.
37. Kikuchi A, Yamamoto H, Sato A, Matsumoto S. Wnt5a: its signalling, functions and implication in diseases. Acta Physiol (Oxf) 2012; 204:17-33. PMID:21518267; http://dx.doi.org/10.1111/j.1748-16.2011.02294.x.
38. Li J, Ying J, Fan Y, Wu L, Ying Y, Chan AT, et al. WNT5A antagonizes WNT/β-catenin signaling and is frequently silenced by promoter CpG methylation in esophageal squamous cell carcinoma. Cancer Biol Ther 2010; 10:617-24. PMID:20603606; http://dx.doi.org/10.4161/cbt.10.6.12609.
39. Wang Z, Chen H. Genistein increases gene expression by demethylation of WNT5a promoter in colon cancer cell line SW1116. Anticancer Res 2010; 30:4537-45. PMID:21115903.
40. Roman-Gomez J, Jimenez-Velasco A, Cordeu L, Vilas-Zornoza A, San Jose-Eneriz E, Garate L, et al. WNT5A, a putative tumour suppressor of lymphoid malignancies, is inactivated by aberrant methylation in acute lymphoblastic leukaemia. Eur J Cancer 2007; 43:2736-46. PMID:18032022; http://dx.doi.org/10.1016/j.ejca.2007.10.004.
41. Chen H, Pan YX, Dudenhausen EE, Kilberg MS. Amino acid deprivation induces the transcription rate of the human asparagine synthetase gene through a timed program of expression and promoter binding of nutrient-responsive basic region/leucine zipper transcription factors as well as localized histone acetylation. J Biol Chem 2004; 279:50829-39. PMID:15385533; http://dx.doi.org/10.1074/jbc.M409173200.