DNA methylation of polycomb group target genes in cores taken from breast cancer centre and periphery

Breast Cancer Research and Treatment

Volumn 120, Issue 2, 2010, Pages 345-355

  Fourkala, Evangelia Ourania ^a   Hauser Kronberger, Cornelia ^b   Apostolidou, Sophia ^a   Burneil, Matthew ^a   Jones, Allison ^a   Grall, Johannes ^b   Reitsamer, Roland ^b   Fiegl, Heidi ^c   Jacobs, Ian ^a   Menon, Usha ^a   Widschwendter, Martin ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b PARACELSUS MEDICAL UNIVERSITY   (Austria)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Breast cancer; Dna methylation; Intra tumour heterogeneity

Indexed keywords

MESSENGER RNA; NEUROGENIC DIFFERENTIATION FACTOR;

ACCURACY; ADULT; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CONTROLLED STUDY; DIAGNOSTIC VALUE; DNA METHYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; PREDICTION; PRIORITY JOURNAL; RECEIVER OPERATING CHARACTERISTIC;

AREA UNDER CURVE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BREAST NEOPLASMS; DNA METHYLATION; FEMALE; HUMANS; MIDDLE AGED; NEOPLASM STAGING; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; ROC CURVE; TUMOR MARKERS, BIOLOGICAL;

EID: 77950692374     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-009-0384-3     Document Type: Article

References (53)

1. 1. Feuer EJ, Wun LM, Boring CC et al (1993) The lifetime risk of developing breast cancer. J Natl Cancer Inst 85:892-897. doi: 10.1093/jnci/85.11.892 (Pubitemid 23157129)
2. Kok M, Linn SC, Van Laar RK, Jansen MP, van den Berg TM, Delahaye LJ, Glas AM, Peterse JL, Hauptmann M, Foekens JA, Klijn JG, Wessels LF, Van't Veer LJ, Berns EM (2009) Comparison of gene expression profiles predicting progression in breast cancer patients treated with tamoxifen. Breast Cancer Res Treat 113:275-283. doi:10.1007/s10549-008-9939-y
3. Lu X, Lu X, Wang ZC, Iglehart JD, Zhang X, Richardson AL (2008) Predicting features of breast cancer with gene expression patterns. Breast Cancer Res Treat 108:191-201. doi: 10.1007/ s10549-007-9596-9606
4. Yang SX, Steinberg SM, Nguyen D, Wu TD, Modrusan Z, Swain SM (2008) Gene expression profile and angiogenic marker correlates with response to neoadjuvant bevacizumab followed by bevacizumab plus chemotherapy in breast cancer. Clin Cancer Res 14:5893-5899. doi: 10.1158/1078-0432.CCR-Cr7-4762
5. 5. Chanrion M, Negre V, Fontaine H, Salvetat N, Bibeau F, Mac Grogan G, Mauriac L, Katsaros D, Molina F, Theillet C, Darbon JM (2008) A gene expression signature that can predict the recurrence of tamoxifen-treated primary breast cancer. Clin Cancer Res 14:1744-1752. doi: 10.1158/1078-0432.CCR-07-1833 (Pubitemid 351469459)
6. 6. Michiels S, Koscielny S, Hill C (2005) Prediction of cancer outcome with microarrays: a multiple random validation strategy. Lancet 365:488-492. doi: 10.101.6/S0140-6736(05) 17866-0 (Pubitemid 40215731)
7. Heppner GH (1984) Tumor heterogeneity. Cancer Res 44:2259-2265
8. 8. Khalique L, Ayhan A, Weale ME, Jacobs IJ, Ramus SJ, Gayther SA (2007) Genetic intra-tumor heterogeneity in epithelial ovarian cancer and its implications for molecular diagnosis of tumors. J Pathol 211:286-295. doi:10,1002/path.2112 (Pubitemid 46172704)
9. Losi L, Baisse B, Bouzourene H, Benhattar J (2005) Evolution of intra-tumoral genetic heterogeneity during colorectal cancer progression. Carcinogenesis 26:9.16-922. doi:10.1093/carcin/bgi044
10. Lyng MB, Laenkholm AV, Pallisgraad N et al (2007) Intra-tumor genetic heterogeneity in advanced carcinomas as determined by fine needle aspiration and TaqMan low density array. Cell Oncol 29:361-372
11. Ruiz-Cerda JL, Hernandez M, Sempere A, O'Connor JE, Kimler BF, Jimenez-Cruz F (1999) Intra-tumoral heterogeneity of DNA content in renal cell carcinoma and its prognostic significance. Cancer 86:664-671. doi: 10.1002/(SICI) 1097-0142(19990815) 86:4<664::AID-CNCR16>3.0.CO;2-E
12. van der Poel HG, Oosterhof GO, Schaafsma HE, Debruyne FM, Schalken JA (1997) Intra-tumoral nuclear morphologic heterogeneity in prostate cancer. Urology 49:652-657. doi: 10.1016/ S0090-4295(96)00557-562
13. 13. Lyng H, Beigi M, Svendsrud DH, Brustugun OT, Stokke T, Kristensen GB, Sundfor K, Skjonsberg A, De Angelis PM (2004) Intra-tumor chromosomal heterogeneity in advanced carcinomas of the uterine cervix. Int J Cancer 111:358-366, doi: 10.1002/ ijc.20258 (Pubitemid 38998815)
14. 14. Aubele M, Mattis A, Zitzelsberger H, Walch A, Kremer M, Hutzler P, Hotter H, Werner M (1999) Intra-tumoral heterogeneity in breast carcinoma revealed by laser-microdissection and comparative genomic hybridization. Cancer Genet Cytogenet 110:94-102. doi:10.1016/S0165-4608(98)00205-2 (Pubitemid 29181514)
15. 15. Zhu G, Reynolds L, Crnogorac-Jurcevic T, Gillett CE, Dublin EA, Marshall JF, Barnes D, D'Arrigo C, Van Trappen PO, Lemoine NR, Hart IR (2003) Combination of microdissection and microarray analysis to identify gene expression changes between differentially located tumor cells in breast cancer. Oncogene 22:3742-3748. doi:10.1038/sj.onc.1206428 (Pubitemid 36760736)
16. Nakamura T, Kuwai T, Kitadai Y, Sasaki T, Fan D, Coombes KR, Kim SJ, Fidler IJ (2007) Zonal heterogeneity for gene expression in human pancreatic carcinoma. Cancer Res 67:7597-7604. doi: 10.1158/0008-5472.CAN-07-0874
17. Sigalotti L, Coral S, Nardi G, Spessotto A, Cortini E, Cattarossi I, Colizzi F, Altomonte M, Maio M (2002) Promoter methylation controls the expression of MAGE2, 3 and 4 genes in human cutaneous melanoma. J Immunother 25:16-26. doi: 10.1097/ 00002371-200201000-200300002
18. Kuniyasu H, Troncoso P, Johnston D, Bucana CD, Tahara E, Fidler IJ, Pettaway CA (2000) Relative expression of type IV collagenase, E-cadherin, and vascular endothelial growth factor/ vascular permeability factor in prostatectomy specimens distinguishes organ-confined from pathologically advanced prostate cancers. Clin Cancer Res 6:2295-2308
19. 19. Jarque F, Lluch A, Vera FJ, Pascual A, Vizcarra E, Alberola V, Garcia-Conde J (1990) Intra-tumoral variation of estrogen and progesterone receptors in breast cancer: relationship with histopathological characteristics of the tumor. Oncology 47:9-13 (Pubitemid 20027731)
20. 20. Davis BW, Zava DT, Locher GW, Goldhirsch A, Hartmann WH ( 1984) Receptor heterogeneity of human breast cancer as measured by multiple intratumoral assays of estrogen and progesterone receptor. Eur J Cancer Clin Oncol 20:375-382. doi: 10.1016/02775379(84)90084-1 (Pubitemid 14157815)
21. 21. van Notten JP, Armstrong JB, Caryle SS, Goodchild NL, Thornton IG, Brigden ML, Coy P, Fletcher C (1988) Estrogen receptor distribution in the peripheral, intermediate and central regions of breast cancer. Eur J Cancer Clin Oncol 24:1885-1889. doi: 10.1016/0277-5379(88)90102-2 (Pubitemid 19022380)
22. Baylin SB, Ohm JE (2006) Epigenetic gene silencing in cancer a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 6:107-116. doi: 1.0.1.038/nrc1799
23. Feinberg AP, Tycko B (2004) The history of cancer epigenetics. Nat Rev Cancer 4:143-153. doi:1.0.1.038/nrc1279
24. Widschwendter M, Jones PA (2002) DNA methylation and breast carcinogenesis. Oncogene 21:5462-5482. doi:10.1038/sj.onc.1205606
25. 25. Ordway JM, Budiman MA, Korshunova Y, Maloney RK, Bedell JA, Citek RW, Bacher B, Peterson S, Rohlfing T, Hall J, Brown R, Lakey N, Doerge RW, Martienssen RA, Leon J, McPherson JD, Jeddeloh JA (2007) Identification of novel high-frequency DNA methylation changes in breast cancer. PLoS ONE 2:e1314. doi: 10.1371/journal.pone.0001314 (Pubitemid 351766831)
26. 26. Widschwendter M, Siegmund KD, Muller HM, Fiegl H, Marth C, Muller-Holzner E, Jones PA, Laird PW (2004) Association of breast cancer DNA methylation profiles with hormone receptor status and response to tamoxifen, Cancer Res 64:3807-3813. doi: 10.1158/0008-5472.CAN-03-3852 (Pubitemid 38697289)
27. Fiegl H, Jones A, Hauser-Kronberger C, Hutarew G, Reitsamer R, Jones RL, Dowsett M, Mueller-Holzner E, Windbichler G, Daxenbichler G, Goebel G, Ensinger C, Jacobs I, Widschwendter M (2008) Methylated NEUROD1 promoter is a marker for chemosensitivity in breast cancer, Clin Cancer Res 14:3494-3502, doi: 10.1158/1078-0432.CCR-07-4557
28. Pakneshan P, Têtu B, Rabbani SA (2004) Demethylation of urokinase promoter as a prognostic marker in patients with breast carcinoma. Clin Cancer Res 10:3035-3041.doi: 10.1158/1078-0432.CCR-03-0545
29. 29. Chung W, Kwabi-Addo B, Ittmann M, Jelinek J, Shen L, Yu Y, Issa JP (2008) Identification of novel tumor markers in prostate, colon and breast cancer by unbiased methylation profiling. PLoS ONE 30:e2079. doi: 10.1371/journal.pone.0002079 (Pubitemid 352025019)
30. 30. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, Weisenberger DJ, Campan M, Young J, Jacobs I, Laird PW (2007) Epigenetic stem cell signature in cancer. Nat Genet 39:157-158. doi: 10.1038/ng1941 (Pubitemid 46184343)
31. 31. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, Mohammad HP, Chen W, Daniel VC, Yu W, Berman DM, Jenuwein T, Pruitt K, Sharkis SJ, Watkins DN, Herman JG, Baylin SB (2007) A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 39:237-242. doi:10.1038/ng1972 (Pubitemid 46184356)
32. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, Eden E, Yakhini Z, Ben Shushan E, Reubinoff BE, Bergman Y, Simon I, Cedar H (2007) Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 39:232-236. doi: 10.1038/ng 1950
33. Eads CA, Danenberg KD, Kawakami K, Saltz LB, Blake C, Shibata D, Danenberg PV, Laird PW (2000) MethyLight: a highthroughput assay to measure. Nucleic Acids Res 28:E32. doi:10.1093/nar/28.8.e32
34. 34. Widschwendter M, Berger J, Hermann M, Müller HM, Amberger A, Zeschnigk M., Widschwendter A, B Abendstein, Zeimet AG, Daxenbichler G, Marth C (2000) Methylation and silencing of the retinoic acid receptor-beta2 gene in breast cancer. J Natl Cancer Inst 92:826-832. doi: 10.1093/jnci/92.10.826 (Pubitemid 30368039)
35. 35. Muller HM, Fiegl H, Goebel G, Hubalek MM, Widschwendter A, Muller-Holzner E, Marth C, Widschwendter M (2003) MeCP2 and MBD2 expression in human neoplastic and non-neoplastic breast tissue and its association with oestrogen receptor status. Br J Cancer 89:1934-1939. doi: 10.1038/sj.bjc.6601392 (Pubitemid 37533273)
36. Bieche I, Franc B, Vidaud D, Vidaud M, Lidereau R (2001) Analyses of MYC, ERBB2, and CCND1 genes in benign and malignant thyroid follicular cell tumors by real-time polymerase chain reaction. Thyroid 11:147-152. doi: 10.1089/105072501. 300042802
37. Harbeck N, Nimmrich I, Hartmann A, Ross JS, Cufer T, Grutzmann R, Kristiansen G, Paradiso A, Hartmann O, Margossian A, Martens J, Schwope I, Lukas A, Muller V, Milde-Langosch K, Nahrig J, Foekens J, Maier S, Schmitt M, Lesche, R Multicenter Study (2008) Using paraffin-embedded tumor tissue testing PITX2 DNA methylation as a marker for outcome prediction in tamoxifen-treated, node-negative breast cancer patients. J Clin Oncol 28:5036-5042. doi: 10.1200/JCO.2007.14.1697
38. 38. Sigalotti L, Fratta E, Coral S, Tanzarella S, Danielli R, Colizzi F, Fonsatti E, Traversari C, Altomonte M, Maio M (2004) Intratumor heterogeneity of cancer/testis antigens expression in human cutaneous melanoma is methylation-regulated and functionally reverted by 5-aza-2′-deoxycytidine. Cancer Res 64: 9167-9171. doi: 10.11.58/0008-5472.CAN-04-1.442 (Pubitemid 39665532)
39. 39. Rastetter M, Schagdarsurengin U, Lahtz C, Fiedler E, Marsch WC, Dammann R, Helmbold P (2007) Frequent intra-tumoral heterogeneity of promoter hypermethylation in malignant melanoma. Histol Histopathol 22:1005-1015 (Pubitemid 47034166)
40. Woloszynska-Read A, Mhawech-Fauceglia P, Yu J, Odunsi K, Karpf AR (2008) Intertumor and intratumor NY-ESO-1 expression heterogeneity is associated with promoter-specific and global DNA methylation status in ovarian cancer. Clin Cancer Res 14:3283-3290. doi: 10.1158/1078-0432.CCR-07-5279
41. Ebert MP, Mooney SH, Tonnes-Priddy L, Lograsso J, Hoffmann J, Chen J, Rocken C, Schulz HU, Malfertheiner P, Lofton-Day C (2005) Hypermethylation of the TPEF/HPP1 gene in primary and metastatic colorectal cancers. Neoplasia 7:771-778. doi: 10.1593/ neo.05235
42. Liang G, Robertson KD, Talmadge C, Sumagi J, Jones PA (2000) The gene for a novel transmembrane protein containing epidermal growth factor and follistatin domains is frequently hypermethylated in human tumor cells. Cancer Res 60:4907-4912
43. 43. Shibata DM, Sato F, Mori Y, Perry K, Yin J, Wang S, Xu Y, Olaru A, Selaru F, Spring K, Young J, Abraham JM, Meltzer SJ (2002) Hypermethylation of HPP1 is associated with hMLH1 hypermethylation in gastric adenocarcinomas. Cancer Res 62: 5637-5640 (Pubitemid 35204713)
44. Goo YA, Goodlett DR, Pascal LE, Worthington KD, Vessella RL, True LD, Liu AY (2005) Stromal mesenchyme cell genes of the human prostate and bladder. BMC Urol 5:17. doi: 10.1186/ 1471-2490-5-17
45. Lind GE, Kleivi K, Meling GI, Teixeira MR, Thiis-Evensen E, Rognum TO, Lothe RA (2006) ADAMTS1, CRABP1, and NR3C1 identified as epigenetically deregulated genes in colorectal tumorigenesis. Cell Oncol 28:259-272
46. 46. Wu Q, Lothe RA, Ahlquist T, Silins I, Trope CG, Micci F, Nesland JM, Suo Z, Lind GE (2007) DNA methylation profiling of ovarian carcinomas and their in vitro models HOXA9, HOXB5, SCGB3A1 as novel targets. Mol Cancer 6:45-55. doi: 10.1186/1476-4598-6-45 (Pubitemid 47381869)
47. 47. Piotrowski A, Benetkiewicz M., Menzel U, de Ståhl TD, Mantripragada K, Grigelionis G, Buckley PG, Jankowski M, Hoffman J, Bała D, Srutek E, Laskowski R, Zegarski W, Dumanski JP (2006) Microarray-based survey of CpG islands identifies concurrent hyper- and hypomethylation patterns in tissues derived from patients with breast cancer. Genes Chromosomes Cancer 45:656-667. doi: 10.1002/gcc.20331 (Pubitemid 43727153)
48. 48. Pearson JC, Lemons D, McGinnis W (2006) Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6:893-904. doi: 10.1038/nrg1726 (Pubitemid 41782157)
49. 49. Caré A, Silvavi A, Meccia E, Mattia G, Stoppacciaro A, Parmiani G, Peschle C, Colombo MP (1996) HOXB7 constitutively activates basic fibroblast growth factor in melanomas. Mol Cell Biol 16:4842-4851 (Pubitemid 26272139)
50. Chen H, Sukumar S (2003) HOX genes: emerging stars in cancer. Cancer Biol Ther 2:524-525
51. Novak P, Jensen T, Oshiro MM, Wozniak RJ, Nouzova M, Watts GS, Klimecki WT, Kim C, Futscher BW (2006) Epigenetic inactivation of the HOXA gene cluster in breast cancer. Cancer Res 66:10664-10670. doi:.10.11.58/0008-5472.CAN-06-2761
52. 52. Fieg1 H, Windbichler G, Mueller-Holzner E, Goebel G, Lechner M, Jacobs IJ, Widschwendter M (2008) HOXA11 DNA methylation - a novel prognostic biomarker in ovarian cancer. Int J Cancer 123:725-729. doi:10.1002/ijc.23563 (Pubitemid 351898435)
53. 53. Wu JM, Fackler MJ, Halushka MK, Molavi DW, Taylor ME, Teo WW, Griffin C, Fetting J, Davidson NE, De Marzo AM, Hicks JL, Chitale D, Ladanyi M, Sukumar S, Argani P (2008) Heterogeneity of breast cancer metastases: comparison of therapeutic target expression and promoter methylation between primary tumors and their multifocal metastases. Clin Cancer Res 7:1938 1946. doi:10.1158/1078-0432.CCR-07-4082 (Pubitemid 351551102)