Evaluation of protein expression and DNA methylation profiles detected by pyrosequencing in invasive breast cancer

Neoplasma

Volumn 60, Issue 6, 2013, Pages 635-646

  Zmetakova, I ^a   Danihel, L ^b,c   Smolkova, B ^a   Mego, M ^d   Kajabova, V ^a   Krivulcik, T ^a   Rusnak, I ^e   Rychly, B ^f   Danis, D ^f   Repiska, V ^b   Blasko, P ^g   Karaba, M ^h   Benca, J ^h   Pechan, J ^e,h   Fridrichova, I ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

^b UNIVERSITY HOSPITAL BRATISLAVA   (Slovakia)

^c Department of Forensic Medicine and Pathology   (Slovakia)

^d Physics and Informatics   (Slovakia)

^e SLOVAK MEDICAL UNIVERSITY   (Slovakia)

^f Cytopathos s r o   (Slovakia)

^g Department of Gynaecology   (Slovakia)

^h CANCER RESEARCH INSTITUTE   (Slovakia)

Author keywords

Breast cancer; DNA methylation; Invasivity and metastasising associated genes; Protein expression; Pyrosequencing analysis

Indexed keywords

ADULT; AGED; ARTICLE; BREAST CANCER; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA EXTRACTION; DNA METHYLATION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PYROSEQUENCING; VERY ELDERLY; BREAST TUMOR; CANCER GRADING; CANCER STAGING; CASE CONTROL STUDY; COLLOID CARCINOMA; COMPARATIVE STUDY; DNA SEQUENCE; ENZYME IMMUNOASSAY; EVALUATION; GENETICS; LUNG CARCINOMA; METABOLISM; MIDDLE AGED; PAGET NIPPLE DISEASE; PATHOLOGY; PROGNOSIS; TUMOR INVASION;

TUMOR MARKER;

ADENOCARCINOMA, MUCINOUS; ADULT; AGED; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, LOBULAR; CASE-CONTROL STUDIES; DNA METHYLATION; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROGNOSIS; SEQUENCE ANALYSIS, DNA; TUMOR MARKERS, BIOLOGICAL; YOUNG ADULT;

EID: 84884186376     PISSN: 00282685     EISSN: 13384317     Source Type: Journal    
DOI: 10.4149/neo_2013_082     Document Type: Article

References (57)

1. TRAPE AP, GONZALEZ-ANGULO AM Breast cancer and metastasis: on the way toward individualized therapy. Cancer Genomics Proteomics 2012; 9(5): 297-310
2. ESTELLER M Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 2007; 8(4): 286-298. http://dx.doi.org/10.1038/nrg2005
3. LEWIS CM, CLER LR, BU DW, ZOCHBAUER-MULLER S, MILCHGRUB S et al. Promoter hypermethylation in benign breast epithelium in relation to predicted breast cancer risk. Clin Cancer Res 2005; 11(1): 166-172.
4. ESTELLER M, CORN PG, BAYLIN SB, HERMAN JG A gene hypermethylation profile of human cancer. Cancer Res 2001; 61: 3225-3229.
5. PASQUALI L, BEDEIR A, RINGQUIST S, STYCHE A, BHARGAVA R et al. Quantification of CpG island methylation in progressive breast lesions from normal to invasive carcinoma. Cancer Lett 2007; 257(1): 136-144. http://dx.doi.org/10.1016/j.canlet.2007.07.010
6. FACKLER MJ, MC VEIGH M, MEHROTRA J, BLUM MA, LANGE J et al. Quantitative multiplex methylation-specific PCR assay for the detection of promoter hypermethylation in multiple genes in breast cancer. Cancer Res 2004; 64(13): 4442-4452. http://dx.doi.org/10.1158/0008-5472.CAN-03-3341
7. ZOCHBAUER-MULLER S, FONG KM, MAITRA A, LAM S, GERADTS J et al. 5' CpG island methylation of the FHIT gene is correlated with loss of gene expression in lung and breast cancer. Cancer Res 2001; 61(9): 3581-5.
8. MAO XY, CHEN H, WANG H, WEI J, LIU C et al. MTA1 expression correlates significantly with ER-alpha methylation in breast cancer. Tumour Biol 2012; 33(5): 1565-1572. http://dx.doi.org/10.1007/s13277-012-0410-7
9. ZHAO Y, ZHOU H, MA K, SUN J, FENG X et al. Abnormal methylation of seven genes and their associations with clinical characteristics in early stage non-small cell lung cancer. Oncol Lett 2013; 5(4): 1211-1218.
10. DEHAN P, CANON C, TROOSKENS G, REHLI M, MUNAUT C et al. Expression of type 2 orexin receptor in human endometrium and its epigenetic silencing in endometrial cancer. J Clin Endocrinol Metab 2013; 98(4): 1549-1557. http://dx.doi.org/10.1210/jc.2012-3263
11. HU XC, WONG IH, CHOW LW Tumor-derived aberrant methylation in plasma of invasive ductal breast cancer patients: clinical implications. Oncol Rep 2003; 10(6): 1811-1815.
12. MULLER HM, WIDSCHWENDTER A, FIEGL H, IVARSSON L, GOEBEL G et al. DNA methylation in serum of breast cancer patients: an independent prognostic marker. Cancer Res 2003; 63(22): 7641-7645.
13. DULAIMI E, HILLINCK J, IBANEZ DE CACERES I, ALSALEEM T, CAIRNS P Tumor suppressor gene promoter hypermethylation in serum of breast cancer patients. Clin Cancer Res 2004; 10(18 Pt 1): 6189-6193. http://dx.doi.org/10.1158/1078-0432.CCR-04-0597
14. FIEGL H, MILLINGER S, MUELLER-HOLZNER E, MARTH C, ENSINGER C et al. Circulating tumor-specific DNA: a marker for monitoring efficacy of adjuvant therapy in cancer patients. Cancer Res 2005; 65(4): 1141-1145. http://dx.doi.org/10.1158/0008-5472.CAN-04-2438
15. HOQUE MO, FENG Q, TOURE P, DEM A, CRITCHLOW CW et al. Detection of aberrant methylation of four genes in plasma DNA for the detection of breast cancer. J Clin Oncol 2006; 24(26): 4262-4269. http://dx.doi.org/10.1200/JCO.2005.01.3516
16. STURGEON SR, BALASUBRAMANIAN R, SCHAIRER C, MUSS HB, ZIEGLER RG et al. Detection of promoter methylation of tumor suppressor genes in serum DNA of breast cancer cases and benign breast disease controls. Epigenetics 2012; 7(11): 1258-1267. http://dx.doi.org/10.4161/epi.22220
17. MIKESKA T, BOCK C, DO H, DOBROVIC A DNA methylation biomarkers in cancer: progress towards clinical implementation. Expert Rev Mol Diagn 2012; 12(5): 473-487. http://dx.doi.org/10.1586/erm.12.45
18. FLANAGAN JM, MUNOZ-ALEGRE M, HENDERSON S, TANG T, SUN P et al. Gene-body hypermethylation of ATM in peripheral blood DNA of bilateral breast cancer patients. Hum Mol Genet 2009; 18(7): 1332-1342. http://dx.doi.org/10.1093/hmg/ddp033
19. WIDSCHWENDTER M, MENON U Circulating methylated DNA: a new generation of tumor markers. Clin Cancer Res 2006; 12(24): 7205-7208. http://dx.doi.org/10.1158/1078-0432.CCR-06-2531
20. LI L, CHOI JY, SUNG H, PARK SK, OZE I DNA methylation in peripheral blood: a potential biomarker for cancer molecular epidemiology. J Epidemiol 2012; 22(5): 384-394. http://dx.doi.org/10.2188/jea.JE20120003
21. CHO YH, SHEN J, GAMMON MD, ZHANG YJ, WANG Q et al. Prognostic significance of gene-specific promoter hypermethylation in breast cancer patients. Breast Cancer Res Treat 2012; 131(1): 197-205. http://dx.doi.org/10.1007/s10549-011-1712-y
22. GAUDET MM, CAMPAN M, FIGUEROA JD, YANG XR, LISSOWSKA J et al. DNA hypermethylation of ESR1 and PGR in breast cancer: pathologic and epidemiologic associations. Cancer Epidemiol Biomarkers Prev 2009; 18(11): 3036-3043. http://dx.doi.org/10.1158/1055-9965.EPI-09-0678
23. RAMOS EA, CAMARGO AA, BRAUN K, SLOWIK R, CAVALLI IJ et al. Simultaneous CXCL12 and ESR1 CpG island hypermethylation correlates with poor prognosis in sporadic breast cancer. BMC Cancer 2010; 10:23. http://dx.doi.org/10.1186/1471-2407-10-23
24. YUAN Y, MENDEZ R, SAHIN A, DAI JL Hypermethylation leads to silencing of the SYK gene in human breast cancer. Cancer Res 2001; 61(14): 5558-5561.
25. COSTA FF, VERBISCK NV SALIM AC, IERARDI DF, PIRES LC et al. Epigenetic silencing of the adhesion molecule ADAM23 is highly frequent in breast tumors. Oncogene 2004; 23: 1481-1488. http://dx.doi.org/10.1038/sj.onc.1207263
26. METGE BJ, FROST AR, KING JA, DYESS DL, WELCH DR et al. Epigenetic silencing contributes to the loss of BRMS1 expression in breast cancer. Clin Exp Metastasis 2008; 25(7): 753-63. http://dx.doi.org/10.1007/s10585-008-9187-x
27. REMMELE W, SCHICKETANZ KM Immunohistochemical determination of estrogen and progesterone receptor content in human breast cancer. Computer-assisted image analysis (QIC score) vs. subjective grading (IRS). Pathol Res Pract 1993; 189(8): 862-866. http://dx.doi.org/10.1016/S0344-0338(11)81095-2
28. KAJABOVA V, SMOLKOVA B, ZMETAKOVA I, SEBOVA K, KRIVULCIK T et al. RASSF1A promoter methylation levels positively correlate with oestrogen receptor expression in breast cancer patients. Trans Onc 2013; 6(3): 297-304.
29. CHO YH, YAZICI H, WU HC, TERRY MB, GONZALES K et al. Aberrant promoter hypermethylation and genomic hypomethylation in tumor, adjacent normal tissues and blood from breast cancer patients. Anticancer Res 2010; 30: 2489-2496.
30. BUHMEIDA A, MERDAD A, AL-MAGHRABI J, ALTHOBAITI F, ATA M et al. RASSF1A methylation is predictive of poor prognosis in female breast cancer in a background of overall low methylation frequency. Anticancer Res 2011; 31: 2975-2981.
31. XU J, SHETTY PB, FENG W, CHENAULT C, BAST RC JR at al. Methylation of HIN-1, RASSF1A, RIL and CDH13 in breast cancer is associated with clinical characteristics, but only RASSF1A methylation is associated with outcome. BMC Cancer 2012; 12: 243. http://dx.doi.org/10.1186/1471-2407-12-243
32. ZHOU W, JIANG Z, LIU N, XU F, WEN P et al. Downregulation of CXCL12 mRNA expression by promoter hypermethylation and its association with metastatic progression in human breast carcinomas. J Cancer Res Clin Oncol 2009; 135(1): 91-102. http://dx.doi.org/10.1007/s00432-008-0435-x
33. MIRISOLA V, ZUCCARINO A, BACHMEIER BE, SORMANI MP, FALTER J et al. CXCL12/SDF1 expression by breast cancers is an independent prognostic marker of disease-free and overall survival. Eur J Cancer 2009; 45(14): 2579-2587. http://dx.doi.org/10.1016/j.ejca.2009.06.026
34. RAMOS EA, GROCHOSKI M, BRAUN-PRADO K, SENISKI GG, CAVALLI IJ et al. Epigenetic changes of CXCR4 and its ligand CXCL12 as prognostic factors for sporadic breast cancer. PLoS One 2011; 6(12): e29461. http://dx.doi.org/10.1371/journal.pone.0029461
35. JIN Z, TAMURA G, TSUCHIYA T, SAKATA K, KASHIWABA M et al. Adenomatous polyposis coli (APC) gene promoter hypermethylation in primary breast cancers. Br J Cancer 2001; 85: 69-73. http://dx.doi.org/10.1054/bjoc.2001.1853
36. VIRMANI AK, RATHI A, SATHYANARAYANA UG, PADAR A, HUANG CX et al. Aberrant methylation of the adenomatous polyposis coli (APC) gene promoter 1A in breast and lung carcinomas. Clin Cancer Res 2001; 7: 1998-2004.
37. LIU Z, YANG L, CUI DX, LIU BL, ZHANG XB et al. Methylation status and protein expression of adenomatous polyposis coli (APC) gene in breast cancer. Ai Zheng 2007; 26: 586-590.
38. WENDT MK, COOPER AN, DWINELL MB. Epigenetic silencing of CXCL12 increases the metastatic potential of mammary carcinoma cells. Oncogene 2008; 27(10): 1461-1471. http://dx.doi.org/10.1038/sj.onc.1210751
39. KOBAYASHI T, TSUDA H, MORIYA T, YAMASAKI T, KIKUCHI R et al. Expression pattern of stromal cell-derived factor-1 chemokine in invasive breast cancer is correlated with estrogen receptor status and patient prognosis. Breast Cancer Res Treat 2010; 123(3): 733-745. http://dx.doi.org/10.1007/s10549-009-0672-y
40. GUIL S, ESTELLER M DNA methylomes, histone codes and miRNAs: tying it all together. Int J Biochem Cell Biol 2009; 41:87-95. http://dx.doi.org/10.1016/j.biocel.2008.09.005
41. HERVOUET E, CARTRON PF, JOUVENOT M, DELAGEMOURROUX R Epigenetic regulation of estrogen signaling in breast cancer. Epigenetics 2013; 8(3): 237-245. http://dx.doi.org/10.4161/epi.23790
42. MONTENEGRO MF, SÀEZ-AYALA M, PINERO-MADRONA A, CABEZAS-HERRERA J, RODRIGUEZ-LOPEZ JN Reactivation of the Tumour Suppressor RASSF1A in Breast Cancer by Simultaneous Targeting of DNA and E2F1 Methylation. PLoS ONE 2012; 7(12): e52231. http://dx.doi.org/10.1371/journal.pone.0052231
43. HAVIK AB, BRANDAL P, HONNE H, DAHLBACK HS, SCHEIE D et al. MGMT promoter methylation in gliomas-assessment by pyrosequencing and quantitative methylation-specific PCR. J Transl Med 2012; 10: 36. http://dx.doi.org/10.1186/1479-5876-10-36
44. MIKESKA T, BOCK C, EL-MAARRI O, HUBNER A, EHRENTRAUT D et al. Optimization of quantitative MGMT promoter methylation analysis using pyrosequencing and combined bisulfite restriction analysis. J Mol Diagn 2007; 9(3): 368-381. http://dx.doi.org/10.2353/jmoldx.2007.060167
45. VAN DER VAART M, PRETORIUS PJ Is the role of circulating DNA as a biomarker of cancer being prematurely overrated? Clin Biochem 2010; 43(1-2): 26-36. http://dx.doi.org/10.1016/j.clinbiochem.2009.08.027
46. JUNG K, FLEISCHHACKER M, RABIEN A Cell-free DNA in the blood as a solid tumor biomarker-a critical appraisal of the literature. Clin Chim Acta 2010; 411(21-22): 1611-1624. http://dx.doi.org/10.1016/j.cca.2010.07.032
47. KORSHUNOVA Y, MALONEY RK, LAKEY N, CITEK RW, BACHER B et al. Massively parallel bisulphite pyrosequencing reveals the molecular complexity of breast cancer-associated cytosine-methylation patterns obtained from tissue and serum DNA. Genome Res 2008;18(1): 19-29. http://dx.doi.org/10.1101/gr.6883307
48. ORDWAY JM, BUDIMAN MA, KORSHUNOVA Y, MALONEY RK, BEDELL JA et al. Identification of novel highfrequency DNA methylation changes in breast cancer. PLoS One. 2007; 2(12): e1314. http://dx.doi.org/10.1371/journal.pone.0001314
49. MATUSCHEK C, BOLKE E, LAMMERING G, GERBER PA, PEIPER M et al. Methylated APC and GSTP1 genes in serum DNA correlate with the presence of circulating blood tumor cells and are associated with a more aggressive and advanced breast cancer disease. Eur J Med Res 2010; 15: 277-286.
50. DIEHL F, LI M, DRESSMAN D, HE Y, SHEN D et al. Detection and quantification of mutations in the plasma of patients with colorectal tumors. Proc Natl Acad Sci U S A 2005; 102(45): 16368-16373. http://dx.doi.org/10.1073/pnas.0507904102
51. TERRY MB, DELGADO-CRUZATA L, VIN-RAVIN N, WU HC, SANTELLA RM DNA methylation in white blood cells: association with risk factors in epidemiologic studies. Epigenetics 2011; 6(7): 828-837. http://dx.doi.org/10.4161/epi.6.7.16500
52. WIDSCHWENDTER M, APOSTOLIDOU S, RAUM E, ROTHENBACHER D, FIEGL H et al. Epigenotyping in peripheral blood cell DNA and breast cancer risk: a proof of principle study. PLoS One. 2008; 3(7): e2656. http://dx.doi.org/10.1371/journal.pone.0002656
53. CHOI JY, JAMES SR, LINK PA, MC CANN SE, HONG CC et al. Association between global DNA hypomethylation in leukocytes and risk of breast cancer. Carcinogenesis 2009; 30: 1889-1897. http://dx.doi.org/10.1093/carcin/bgp143
54. MOORE LE, PFEIFFER RM, POSCABLO C, REAL FX, KOGEVINAS M et al. Genomic DNA hypomethylation as a biomarker for bladder cancer susceptibility in the Spanish Bladder Cancer Study: a case-control study. Lancet Oncol 2008; 9:359-366. http://dx.doi.org/10.1016/S1470-2045(08)70038-X
55. LIM U, FLOOD A, CHOI SW, ALBANES D, CROSS AJ et al. Genomic methylation of leukocyte DNA in relation to colorectal adenoma among asymptomatic women. Gastroenterology 2008; 134: 47-55. http://dx.doi.org/10.1053/j.gastro.2007.10.013
56. PEDERSEN KS, BAMET WR, OBERG AL, DE ANDRADE M, MATSUMOTO ME et al. Leukocyte DNA methylation signature differentiates pancreatic cancer patients from healthy controls. PLoS ONE 2011; 6: e18223. http://dx.doi.org/10.1371/journal.pone.0018223
57. TESCHENDORFF AE, MENON U, GENTRY-MAHARAJ A, RAMUS SJ, GAYTHER SA et al. An epigenetic signature in peripheral blood predicts active ovarian cancer. PLoS ONE. 2009; 4: e8274. http://dx.doi.org/10.1371/journal.pone.0008274