hMLH1 promoter methylation and silencing in primary endometrial cancers are associated with specific alterations in MBDs occupancy and histone modifications

Gynecologic Oncology

Volumn 103, Issue 1, 2006, Pages 321-328

  Xiong, Yuning ^a   Dowdy, Sean C ^a,b   Eberhardt, Norman L ^a   Podratz, Karl C ^a,b   Jiang, Shi Wen ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO CLINIC CANCER CENTER   (United States)

Author keywords

DNA methylation; Endometrial cancer; Epigenetic; hMLH1; MBD

Indexed keywords

HISTONE; HISTONE H3; HISTONE H4; MESSENGER RNA; METHYL CPG BINDING PROTEIN; METHYL CPG BINDING PROTEIN 1; METHYL CPG BINDING PROTEIN 2; METHYL CPG BINDING PROTEIN 3; METHYL CPG BINDING PROTEIN 4; PROTEIN MLH1; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; DNA METHYLATION; ENDOMETRIUM CANCER; FEMALE; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN MODIFICATION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CARRIER PROTEINS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; DNA-BINDING PROTEINS; ENDOMETRIAL NEOPLASMS; FEMALE; GENE SILENCING; HISTONES; HUMANS; METHYL-CPG-BINDING PROTEIN 2; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); RNA, MESSENGER;

EID: 33748569883     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2006.03.045     Document Type: Article

References (40)

1. Cederquist K., Emanuelsson M., Goransson I., Holinski-Feder E., Muller-Koch Y., Golovleva I., et al. Mutation analysis of the MLH1, MSH2 and MSH6 genes in patients with double primary cancers of the colorectum and the endometrium: a population-based study in northern Sweden. Int J Cancer 109 (2004) 370-376
2. Hirasawa A., Aoki D., Inoue J., Imoto I., Susumu N., Sugano K., et al. Unfavorable prognostic factors associated with high frequency of microsatellite instability and comparative genomic hybridization analysis in endometrial cancer. Clin Cancer Res 9 (2003) 5675-5682
3. Esteller M., Levine R., Baylin S.B., Ellenson L.H., and Herman J.G. MLH1 promoter hypermethylation is associated with the microsatellite instability phenotype in sporadic endometrial carcinomas. Oncogene 17 (1998) 2413-2417
4. Gurin C.C., Federici M.G., Kang L., and Boyd J. Causes and consequences of microsatellite instability in endometrial carcinoma. Cancer Res 59 (1999) 462-466
5. Banno K., Susumu N., Hirao T., Yanokura M., Hirasawa A., Aoki D., et al. Identification of germline MSH2 gene mutations in endometrial cancer not fulfilling the new clinical criteria for hereditary nonpolyposis colorectal cancer. Cancer Genet Cytogenet 146 (2003) 58-65
6. Atkin N.B. Microsatellite instability. Cytogenet 92 (2001) 177-181
7. Quaresima B., Faniello M.C., Baudi F., Cuda G., Grandinetti C., Tassone P., et al. Transcriptional regulation of the mismatch repair gene hMLH1. Gene 275 (2001) 261-265
8. Warnick C.T., Dabbas B., Ilstrup S.J., Ford C.D., and Strait K.A. Cell type-dependent regulation of hMLH1 promoter activity is influenced by the presence of multiple redundant elements. Mol Cancer Res 1 (2003) 610-618
9. Strazzullo M., Cossu A., Baldinu P., Colombino M., Satta M.P., Tanda F., et al. High-resolution methylation analysis of the hMLH1 promoter in sporadic endometrial and colorectal carcinomas. Cancer 98 (2003) 1540-1546
10. Simpkins S.B., Bocker T., Swisher E.M., Mutch D.G., Gersell D.J., Kovatich A.J., et al. MLH1 promoter methylation and gene silencing is the primary cause of microsatellite instability in sporadic endometrial cancers. Hum Mol Genet 8 (1999) 661-666
11. Russo M.T., Blasi M.F., Chiera F., Fortini P., Degan P., Macpherson P., et al. The oxidized deoxynucleoside triphosphate pool is a significant contributor to genetic instability in mismatch repair-deficient cells. Mol Cell Biol 24 (2004) 465-474
12. Herman J.G., Umar A., Polyak K., Graff J.R., Ahuja N., Issa J.P., et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci U S A 95 (1998) 6870-6875
13. Nakagawa H., Nuovo G.J., Zervos E.E., Martin Jr. E.W., Salovaara R., Aaltonen L.A., et al. Age-related hypermethylation of the 5′ region of MLH1 in normal colonic mucosa is associated with microsatellite-unstable colorectal cancer development. Cancer Res 61 (2001) 6991-6995
14. Esteller M., Catasus L., Matias-Guiu X., Mutter G.L., Prat J., Baylin S.B., et al. hMLH1 promoter hypermethylation is an early event in human endometrial tumorigenesis. Am J Pathol 155 (1999) 1767-1772
15. Horowitz N., Pinto K., Mutch D.G., Herzog T.J., Rader J.S., Gibb R., et al. Microsatellite instability, MLH1 promoter methylation, and loss of mismatch repair in endometrial cancer and concomitant atypical hyperplasia. Gynecol Oncol 86 (2002) 62-68
16. Jin F., Dowdy S.C., Xiong Y., Eberhardt N.L., Podratz K.C., and Jiang S.W. Up-regulation of DNA methyltransferase 3B expression in endometrial cancers. Gynecol Oncol 96 (2005) 531-538
17. Ng H.H., Zhang Y., Hendrich B., Johnson C.A., Turner B.M., Erdjument-Bromage H., et al. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat Genet 23 (1999) 58-61
18. Sekimata M., Takahashi A., Murakami-Sekimata A., and Homma Y. Involvement of a novel zinc finger protein, MIZF, in transcriptional repression by interacting with a methyl-CpG-binding protein, MBD2. J Biol Chem 276 (2001) 42632-42638
19. Suzuki M., Yamada T., Kihara-Negishi F., Sakurai T., and Oikawa T. Direct association between PU.1 and MeCP2 that recruits mSin3A-HDAC complex for PU.1-mediated transcriptional repression. Oncogene 22 (2003) 8688-8698
20. Somech R., Izraeli S., and A JS. Histone deacetylase inhibitors-A new tool to treat cancer. Cancer Treat Rev 30 (2004) 461-472
21. Hebbes T.R., Clayton A.L., Thorne A.W., and Crane-Robinson C. Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain. EMBO J 13 (1994) 1823-1830
22. Fahrner J.A., Eguchi S., Herman J.G., and Baylin S.B. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res 62 (2002) 7213-7218
23. Kondo Y., Shen L., and Issa J.P. Critical role of histone methylation in tumor suppressor gene silencing in colorectal cancer. Mol Cell Biol 23 (2003) 206-215
24. Tanaka Y., Kurumizaka H., and Yokoyama S. CpG methylation of the CENP-B box reduces human CENP-B binding. FEBS J 272 (2005) 282-289
25. Zhu W.G., Srinivasan K., Dai Z., Duan W., Druhan L.J., Ding H., et al. Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21(Cip1) promoter. Mol Cell Biol 23 (2003) 4056-4065
26. Chang Y.S., Wang L., Suh Y.A., Mao L., Karpen S.J., Khuri F.R., et al. Mechanisms underlying lack of insulin-like growth factor-binding protein-3 expression in non-small-cell lung cancer. Oncogene 23 (2004) 6569-6580
27. Hung H.L., and High K.A. Liver-enriched transcription factor HNF-4 and ubiquitous factor NF-Y are critical for expression of blood coagulation factor X. J Biol Chem 271 (1996) 2323-2331
28. Dugast C., and Weber M.J. NF-Y binding is required for transactivation of neuronal aromatic l-amino acid decarboxylase gene promoter by the POU-domain protein Brn-2. Brain Res Mol Brain Res 89 (2001) 58-70
29. Deng G., Chen A., Hong J., Chae H.S., and Kim Y.S. Methylation of CpG in a small region of the hMLH1 promoter invariably correlates with the absence of gene expression. Cancer Res 59 (1999) 2029-2033
30. Fuks F., Hurd P.J., Wolf D., Nan X., Bird A.P., and Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 278 (2003) 4035-4040
31. Fraga M.F., Ballestar E., Montoya G., Taysavang P., Wade P.A., and Esteller M. The affinity of different MBD proteins for a specific methylated locus depends on their intrinsic binding properties. Nucleic Acids Res 31 (2003) 1765-1774
32. Magdinier F., and Wolffe A.P. Selective association of the methyl-CpG binding protein MBD2 with the silent p14/p16 locus in human neoplasia. Proc Natl Acad Sci U S A 98 (2001) 4990-4995
33. Lin X., and Nelson W.G. Methyl-CpG-binding domain protein-2 mediates transcriptional repression associated with hypermethylated GSTP1 CpG islands in MCF-7 breast cancer cells. Cancer Res 63 (2003) 498-504
34. Sakai H., Urano T., Ookata K., Kim M.H., Hirai Y., Saito M., et al. MBD3 and HDAC1, two components of the NuRD complex, are localized at Aurora-A-positive centrosomes in M phase. J Biol Chem 277 (2002) 48714-48723
35. Tamaru H., and Selker E.U. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414 (2001) 277-283
36. Lehnertz B., Ueda Y., Derijck A.A., Braunschweig U., Perez-Burgos L., Kubicek S., et al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13 (2003) 1192-1200
37. Muller-Tidow C., Kugler K., Diederichs S., Klumpen S., Moller M., Vogt U., et al. Loss of expression of HDAC-recruiting methyl-CpG-binding domain proteins in human cancer. Br J Cancer 85 (2001) 1168-1174
38. Gonzalgo M.L., Hayashida T., Bender C.M., Pao M.M., Tsai Y.C., Gonzales F.A., et al. The role of DNA methylation in expression of the p19/p16 locus in human bladder cancer cell lines. Cancer Res 58 (1998) 1245-1252
39. Graziano F., Arduini F., Ruzzo A., Mandolesi A., Bearzi I., Silva R., et al. Combined analysis of E-cadherin gene (CDH1) promoter hypermethylation and E-cadherin protein expression in patients with gastric cancer: implications for treatment with demethylating drugs. Ann Oncol 15 (2004) 489-492
40. Gilbert J., Gore S.D., Herman J.G., and Carducci M.A. The clinical application of targeting cancer through histone acetylation and hypomethylation. Clin Cancer Res 10 (2004) 4589-4596