The role of Sp1 and EZH2 in the regulation of LMX1A in cervical cancer cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 3206-3217

  Lin, Wen Chi ^a   Yan, Ming De ^b   Yu, Pei Ning ^a   Li, Hsin Jung ^a   Kuo, Chih Chi ^a   Hsu, Chia Lin ^a   Lin, Ya Wen ^a  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Cervical cancer; DNA methylation; EZH2; Histone modification; LMX1A; Sp1

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; HISTONE; LIM HOMEOBOX TRANSCRIPTION FACTOR 1ALPHA; MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR SP1; TRICHOSTATIN A; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CANCER CELL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ELECTROPHORESIS; FEMALE; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN METHYLATION; SITE DIRECTED MUTAGENESIS; UTERINE CERVIX CANCER;

EID: 84885414102     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.08.020     Document Type: Article

References (55)

1. Walboomers J.M., Jacobs M.V., Manos M.M., Bosch F.X., Kummer J.A., Shah K.V., Snijders P.J., Peto J., Meijer C.J., Munoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 1999, 189:12-19.
2. Moody C.A., Laimins L.A. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 2010, 10:550-560.
3. Feinberg A.P., Tycko B. The history of cancer epigenetics. Nat. Rev. Cancer 2004, 4:143-153.
4. Laird P.W. The power and the promise of DNA methylation markers. Nat. Rev. Cancer 2003, 3:253-266.
5. Woodman C.B., Collins S.I., Young L.S. The natural history of cervical HPV infection: unresolved issues. Nat. Rev. Cancer 2007, 7:11-22.
6. Nguyen D.X., Massague J. Genetic determinants of cancer metastasis. Nat. Rev. Genet. 2007, 8:341-352.
7. Popovic R., Licht J.D. Emerging epigenetic targets and therapies in cancer medicine. Cancer Discov. 2012, 2:405-413.
8. Rodriguez-Paredes M., Esteller M. Cancer epigenetics reaches mainstream oncology. Nat. Med. 2011, 17:330-339.
9. Sharma S., Kelly T.K., Jones P.A. Epigenetics in cancer. Carcinogenesis 2010, 31:27-36.
10. Simon J.A., Lange C.A. Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat. Res. 2008, 647:21-29.
11. Tsang D.P., Cheng A.S. Epigenetic regulation of signaling pathways in cancer: role of the histone methyltransferase EZH2. J. Gastroenterol. Hepatol. 2011, 26:19-27.
12. O'Meara M.M., Simon J.A. Inner workings and regulatory inputs that control Polycomb repressive complex 2. Chromosoma 2012, 121:221-234.
13. Varambally S., Dhanasekaran S.M., Zhou M., Barrette T.R., Kumar-Sinha C., Sanda M.G., Ghosh D., Pienta K.J., Sewalt R.G., Otte A.P., Rubin M.A., Chinnaiyan A.M. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002, 419:624-629.
14. Kleer C.G., Cao Q., Varambally S., Shen R., Ota I., Tomlins S.A., Ghosh D., Sewalt R.G., Otte A.P., Hayes D.F., Sabel M.S., Livant D., Weiss S.J., Rubin M.A., Chinnaiyan A.M. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:11606-11611.
15. Bachmann I.M., Halvorsen O.J., Collett K., Stefansson I.M., Straume O., Haukaas S.A., Salvesen H.B., Otte A.P., Akslen L.A. EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. J. Clin. Oncol. 2006, 24:268-273.
16. Fujii S., Ito K., Ito Y., Ochiai A. Enhancer of zeste homologue 2 (EZH2) down-regulates RUNX3 by increasing histone H3 methylation. J. Biol. Chem. 2008, 283:17324-17332.
17. Crea F., Fornaro L., Bocci G., Sun L., Farrar W.L., Falcone A., Danesi R. EZH2 inhibition: targeting the crossroad of tumor invasion and angiogenesis. Cancer Metastasis Rev. 2012, 31:753-761.
18. Ren G., Baritaki S., Marathe H., Feng J., Park S., Beach S., Bazeley P.S., Beshir A.B., Fenteany G., Mehra R., Daignault S., Al-Mulla F., Keller E., Bonavida B., de la Serna I., Yeung K.C. Polycomb protein EZH2 regulates tumor invasion via the transcriptional repression of the metastasis suppressor RKIP in breast and prostate cancer. Cancer Res. 2012, 72:3091-3104.
19. Vire E., Brenner C., Deplus R., Blanchon L., Fraga M., Didelot C., Morey L., Van Eynde A., Bernard D., Vanderwinden J.M., Bollen M., Esteller M., Di Croce L., de Launoit Y., Fuks F. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006, 439:871-874.
20. Acharyya S., Sharma S.M., Cheng A.S., Ladner K.J., He W., Kline W., Wang H., Ostrowski M.C., Huang T.H., Guttridge D.C. TNF inhibits Notch-1 in skeletal muscle cells by Ezh2 and DNA methylation mediated repression: implications in Duchenne muscular dystrophy. PLoS One 2010, 5:e12479.
21. Lai H.C., Lin Y.W., Huang T.H., Yan P., Huang R.L., Wang H.C., Liu J., Chan M.W., Chu T.Y., Sun C.A., Chang C.C., Yu M.H. Identification of novel DNA methylation markers in cervical cancer. Int. J. Cancer 2008, 123:161-167.
22. Lin Y.W., Chung M.T., Lai H.C., De Yan M., Shih Y.L., Chang C.C., Yu M.H. Methylation analysis of SFRP genes family in cervical adenocarcinoma. J. Cancer Res. Clin. Oncol. 2009, 135:1665-1674.
23. McLaughlin-Drubin M.E., Crum C.P., Munger K. Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2130-2135.
24. Su P.H., Lin Y.W., Huang R.L., Liao Y.P., Lee H.Y., Wang H.C., Chao T.K., Chen C.K., Chan M.W., Chu T.Y., Yu M.H., Lai H.C. Epigenetic silencing of PTPRR activates MAPK signaling, promotes metastasis and serves as a biomarker of invasive cervical cancer. Oncogene 2013, 32:15-26.
25. Au Yeung C.L., Tsang W.P., Tsang T.Y., Co N.N., Yau P.L., Kwok T.T. HPV-16 E6 upregulation of DNMT1 through repression of tumor suppressor p53. Oncol. Rep. 2010, 24:1599-1604.
26. Holland D., Hoppe-Seyler K., Schuller B., Lohrey C., Maroldt J., Durst M., Hoppe-Seyler F. Activation of the enhancer of zeste homologue 2 gene by the human papillomavirus E7 oncoprotein. Cancer Res. 2008, 68:9964-9972.
27. Fang J., Zhang M., Li Q. Enhancer of zeste homolog 2 expression is associated with tumor cell proliferation and invasion in cervical cancer. Am. J. Med. Sci. 2011, 342:198-204.
28. Herranz N., Pasini D., Diaz V.M., Franci C., Gutierrez A., Dave N., Escriva M., Hernandez-Munoz I., Di Croce L., Helin K., Garcia de Herreros A., Peiro S. Polycomb complex 2 is required for E-cadherin repression by the Snail1 transcription factor. Mol. Cell. Biol. 2008, 28:4772-4781.
29. Yoo K.H., Hennighausen L. EZH2 methyltransferase and H3K27 methylation in breast cancer. Int. J. Biol. Sci. 2012, 8:59-65.
30. Liu C.Y., Chao T.K., Su P.H., Lee H.Y., Shih Y.L., Su H.Y., Chu T.Y., Yu M.H., Lin Y.W., Lai H.C. Characterization of LMX-1A as a metastasis suppressor in cervical cancer. J. Pathol. 2009, 219:222-231.
31. Wang Y.T., Chuang J.Y., Shen M.R., Yang W.B., Chang W.C., Hung J.J. Sumoylation of specificity protein 1 augments its degradation by changing the localization and increasing the specificity protein 1 proteolytic process. J. Mol. Biol. 2008, 380:869-885.
32. Black A.R., Black J.D., Azizkhan-Clifford J. Sp1 and Krüppel-like factor family of transcription factors in cell growth regulation and cancer. J. Cell. Physiol. 2001, 188:143-160.
33. Suske G., Bruford E., Philipsen S. Mammalian SP/KLF transcription factors: bring in the family. Genomics 2005, 85:551-556.
34. Li L., Davie J.R. The role of Sp1 and Sp3 in normal and cancer cell biology. Ann. Anat. 2010, 192:275-283.
35. Lin R.K., Wu C.Y., Chang J.W., Juan L.J., Hsu H.S., Chen C.Y., Lu Y.Y., Tang Y.A., Yang Y.C., Yang P.C., Wang Y.C. Dysregulation of p53/Sp1 control leads to DNA methyltransferase-1 overexpression in lung cancer. Cancer Res. 2010, 70:5807-5817.
36. Zhang J., Zhu Z.G., Ji J., Yuan F., Yu Y.Y., Liu B.Y., Lin Y.Z. Transcription factor Sp1 expression in gastric cancer and its relationship to long-term prognosis. World J. Gastroenterol. 2005, 11:2213-2217.
37. Nam E.H., Lee Y., Park Y.K., Lee J.W., Kim S. ZEB2 upregulates integrin alpha5 expression through cooperation with Sp1 to induce invasion during epithelial-mesenchymal transition of human cancer cells. Carcinogenesis 2012, 33:563-571.
38. Cha T.L., Zhou B.P., Xia W., Wu Y., Yang C.C., Chen C.T., Ping B., Otte A.P., Hung M.C. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 2005, 310:306-310.
39. Blume S.W., Snyder R.C., Ray R., Thomas S., Koller C.A., Miller D.M. Mithramycin inhibits SP1 binding and selectively inhibits transcriptional activity of the dihydrofolate reductase gene in vitro and in vivo. J. Clin. Investig. 1991, 88:1613-1621.
40. Liu Y.N., Lee W.W., Wang C.Y., Chao T.H., Chen Y., Chen J.H. Regulatory mechanisms controlling human E-cadherin gene expression. Oncogene 2005, 24:8277-8290.
41. Hsu T.I., Wang M.C., Chen S.Y., Yeh Y.M., Su W.C., Chang W.C., Hung J.J. Sp1 expression regulates lung tumor progression. Oncogene 2012, 31:3973-3988.
42. McGarvey K.M., Greene E., Fahrner J.A., Jenuwein T., Baylin S.B. DNA methylation and complete transcriptional silencing of cancer genes persist after depletion of EZH2. Cancer Res. 2007, 67:5097-5102.
43. Kodach L.L., Jacobs R.J., Heijmans J., van Noesel C.J., Langers A.M., Verspaget H.W., Hommes D.W., Offerhaus G.J., Van Den Brink G.R., Hardwick J.C. The role of EZH2 and DNA methylation in the silencing of the tumour suppressor RUNX3 in colorectal cancer. Carcinogenesis 2010, 31:1567-1575.
44. Mitchell D.C., Stafford L.J., Li D., Bar-Eli M., Liu M. Transcriptional regulation of KiSS-1 gene expression in metastatic melanoma by specificity protein-1 and its coactivator DRIP-130. Oncogene 2007, 26:1739-1747.
45. Mulero-Navarro S., Carvajal-Gonzalez J.M., Herranz M., Ballestar E., Fraga M.F., Ropero S., Esteller M., Fernandez-Salguero P.M. The dioxin receptor is silenced by promoter hypermethylation in human acute lymphoblastic leukemia through inhibition of Sp1 binding. Carcinogenesis 2006, 27:1099-1104.
46. Mancini D.N., Singh S.M., Archer T.K., Rodenhiser D.I. Site-specific DNA methylation in the neurofibromatosis (NF1) promoter interferes with binding of CREB and SP1 transcription factors. Oncogene 1999, 18:4108-4119.
47. Choi J.Y., Lee S., Hwang S., Jo S.A., Kim M., Kim Y.J., Pang M.G., Jo I. Histone H3 lysine 27 and 9 hypermethylation within the Bad promoter region mediates 5-Aza-2'-deoxycytidine-induced Leydig cell apoptosis: implications of 5-Aza-2'-deoxycytidine toxicity to male reproduction. Apoptosis 2013, 18:99-109.
48. Zhang C., Li H., Zhou G., Zhang Q., Zhang T., Li J., Zhang J., Hou J., Liew C.T., Yin D. Transcriptional silencing of the TMS1/ASC tumour suppressor gene by an epigenetic mechanism in hepatocellular carcinoma cells. J. Pathol. 2007, 212:134-142.
49. McGarvey K.M., Fahrner J.A., Greene E., Martens J., Jenuwein T., Baylin S.B. Silenced tumor suppressor genes reactivated by DNA demethylation do not return to a fully euchromatic chromatin state. Cancer Res. 2006, 66:3541-3549.
50. Sun F., Chan E., Wu Z., Yang X., Marquez V.E., Yu Q. Combinatorial pharmacologic approaches target EZH2-mediated gene repression in breast cancer cells. Mol. Cancer Ther. 2009, 8:3191-3202.
51. Bracken A.P., Pasini D., Capra M., Prosperini E., Colli E., Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J. 2003, 22:5323-5335.
52. Gao J., Chen T., Liu J., Liu W., Hu G., Guo X., Yin B., Gong Y., Zhao J., Qiang B., Yuan J., Peng X. Loss of NECL1, a novel tumor suppressor, can be restored in glioma by HDAC inhibitor-Trichostatin A through Sp1 binding site. Glia 2009, 57:989-999.
53. Gregory R.C., Taxman D.J., Seshasayee D., Kensinger M.H., Bieker J.J., Wojchowski D.M. Functional interaction of GATA1 with erythroid Krüppel-like factor and Sp1 at defined erythroid promoters. Blood 1996, 87:1793-1801.
54. Watamoto K., Towatari M., Ozawa Y., Miyata Y., Okamoto M., Abe A., Naoe T., Saito H. Altered interaction of HDAC5 with GATA-1 during MEL cell differentiation. Oncogene 2003, 22:9176-9184.
55. Wong C.Y., Wuriyanghan H., Xie Y., Lin M.F., Abel P.W., Tu Y. Epigenetic regulation of phosphatidylinositol 3,4,5-triphosphate-dependent Rac exchanger 1 gene expression in prostate cancer cells. J. Biol. Chem. 2011, 286:25813-25822.