Integrated epigenetics of human breast cancer: Synoptic investigation of targeted genes, microRNAs and proteins upon demethylation treatment

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Radpour, Ramin ^a   Barekati, Zeinab ^a   Kohler, Corina ^a   Schumacher, Martin M ^b   Grussenmeyer, Thomas ^c   Jenoe, Paul ^d   Hartmann, Nicole ^b   Moes, Suzette ^d   Letzkus, Martin ^b   Bitzer, Johannes ^a   Lefkovits, Ivan ^c   Staedtler, Frank ^b   Zhong, Xiao Yan ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b NOVARTIS PHARMA AG   (Switzerland)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA METHYLTRANSFERASE 3A; EPIDERMAL GROWTH FACTOR RECEPTOR 2; MICRORNA; MICRORNA 24; MICRORNA 29B; ONCOPROTEIN; RNA; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIMETABOLITE; AZACITIDINE; DRUG DERIVATIVE; MESSENGER RNA; TUMOR MARKER;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CDKN2A ONCOGENE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY TEST; DEMETHYLATION; DNA METHYLATION; DNA MODIFICATION; DRUG TOLERANCE; EPIGENETICS; GENE EXPRESSION PROFILING; GENE REPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METASTASIS INHIBITION; ONCOGENE; PHARMACOGENETICS; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE; TWO DIMENSIONAL GEL ELECTROPHORESIS; BREAST TUMOR; CELL PROLIFERATION; DNA MICROARRAY; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; AZACITIDINE; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DNA METHYLATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TUMOR MARKERS, BIOLOGICAL;

EID: 80455156257     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027355     Document Type: Article

References (71)

1. Suzuki MM, Bird A, (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9: 465-476.
2. Bird A, (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21.
3. Laird PW, (2003) The power and the promise of DNA methylation markers. Nat Rev Cancer 3: 253-266.
4. Esquela-Kerscher A, Slack FJ, (2006) Oncomirs- microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269.
5. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
6. Fabbri M, Ivan M, Cimmino A, Negrini M, Calin GA, (2007) Regulatory mechanisms of microRNAs involvement in cancer. Expert Opin Biol Ther 7: 1009-1019.
7. Lujambio A, Ropero S, Ballestar E, Fraga MF, Cerrato C, et al. (2007) Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res 67: 1424-1429.
8. Kangaspeska S, Stride B, Metivier R, Polycarpou-Schwarz M, Ibberson D, et al. (2008) Transient cyclical methylation of promoter DNA. Nature 452: 112-115.
9. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, et al. (2008) Cyclical DNA methylation of a transcriptionally active promoter. Nature 452: 45-50.
10. Moggs JG, Goodman JI, Trosko JE, Roberts RA, (2004) Epigenetics and cancer: implications for drug discovery and safety assessment. Toxicol Appl Pharmacol 196: 422-430.
11. Yoo CB, Jones PA, (2006) Epigenetic therapy of cancer: past, present and future. Nat Rev Drug Discov 5: 37-50.
12. Suzuki MM, Bird A, (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9: 465-476.
13. Kantarjian H, Issa JP, Rosenfeld CS, Bennett JM, Albitar M, et al. (2006) Decitabine improves patient outcomes in myelodysplastic syndromes: results of a phase III randomized study. Cancer 106: 1794-1803.
14. Fenaux P, Mufti GJ, Hellstrom-Lindberg E, Santini V, Finelli C, et al. (2009) Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. Lancet Oncol 10: 223-232.
15. Issa JP, (2003) Decitabine. Curr Opin Oncol 15: 446-451.
16. Momparler RL, (2005) Epigenetic therapy of cancer with 5-aza-2′-deoxycytidine (decitabine). Semin Oncol 32: 443-451.
17. Chandrasekaran EV, Davidson EA, (1979) Glycosaminoglycans of normal and malignant cultured human mammary cells. Cancer research 39: 870-880.
18. Simstein R, Burow M, Parker A, Weldon C, Beckman B, (2003) Apoptosis, chemoresistance, and breast cancer: insights from the MCF-7 cell model system. Experimental biology and medicine 228: 995-1003.
19. Smith HS, (1979) In vitro properties of epithelial cell lines established from human carcinomas and nonmalignant tissue. Journal of the National Cancer Institute 62: 225-230.
20. Littlewood-Evans AJ, Bilbe G, Bowler WB, Farley D, Wlodarski B, et al. (1997) The osteoclast-associated protease cathepsin K is expressed in human breast carcinoma. Cancer research 57: 5386-5390.
21. Burfeind P, Chernicky CL, Rininsland F, Ilan J, (1996) Antisense RNA to the type I insulin-like growth factor receptor suppresses tumor growth and prevents invasion by rat prostate cancer cells in vivo. Proceedings of the National Academy of Sciences of the United States of America 93: 7263-7268.
22. Pollack MS, Heagney SD, Livingston PO, Fogh J, (1981) HLA-A, B, C and DR alloantigen expression on forty-six cultured human tumor cell lines. Journal of the National Cancer Institute 66: 1003-1012.
23. Berdichevsky F, Alford D, D'Souza B, Taylor-Papadimitriou J, (1994) Branching morphogenesis of human mammary epithelial cells in collagen gels. Journal of cell science 107 (Pt 12): 3557-3568.
24. Radpour R, Sikora M, Grussenmeyer T, Kohler C, Barekati Z, et al. (2009) Simultaneous Isolation of DNA, RNA, and Proteins for Genetic, Epigenetic, Transcriptomic, and Proteomic Analysis. J Proteome Res 8: 5264-5274.
25. Gatlin CL, Eng JK, Cross ST, Detter JC, Yates JR 3rd, (2000) Automated identification of amino acid sequence variations in proteins by HPLC/microspray tandem mass spectrometry. Anal Chem 72: 757-763.
26. Radpour R, Kohler C, Haghighi MM, Fan AX, Holzgreve W, et al. (2009) Methylation profiles of 22 candidate genes in breast cancer using high-throughput MALDI-TOF mass array. Oncogene 28: 2969-2978.
27. Han HJ, Russo J, Kohwi Y, Kohwi-Shigematsu T, (2008) SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 452: 187-193.
28. Dai M, Wang P, Boyd AD, Kostov G, Athey B, et al. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 33: e175.
29. Shi L, Campbell G, Jones WD, Campagne F, Wen Z, et al. (2010) The MicroArray Quality Control (MAQC)-II study of common practices for the development and validation of microarray-based predictive models. Nat Biotechnol 28: 827-838.
30. Plante I, Stewart MK, Barr K, Allan AL, Laird DW, (2010) Cx43 suppresses mammary tumor metastasis to the lung in a Cx43 mutant mouse model of human disease. Oncogene.
31. Fujita T, Ashikaga A, Shiba H, Uchida Y, Hirono C, et al. (2006) Regulation of IL-8 by Irsogladine maleate is involved in abolishment of Actinobacillus actinomycetemcomitans-induced reduction of gap-junctional intercellular communication. Cytokine 34: 271-277.
32. Li M, Qi SY, Wang Y, Feng SX, Zhang BZ, et al. (2005) Expression and clinical significance of vascular endothelial growth factor, cyclooxygenase-2, and Bcl-2 in borderline ovarian tumors. Arch Gynecol Obstet 272: 48-52.
33. Kishimoto T, (2005) Interleukin-6: from basic science to medicine-40 years in immunology. Annu Rev Immunol 23: 1-21.
34. Hong DS, Angelo LS, Kurzrock R, (2007) Interleukin-6 and its receptor in cancer: implications for Translational Therapeutics. Cancer 110: 1911-1928.
35. Schafer ZT, Brugge JS, (2007) IL-6 involvement in epithelial cancers. J Clin Invest 117: 3660-3663.
36. Radpour R, Barekati Z, Kohler C, Holzgreve W, Zhong XY, (2009) New trends in molecular biomarker discovery for breast cancer. Genet Test Mol Biomarkers 13: 565-571.
37. Mayo LD, Dixon JE, Durden DL, Tonks NK, Donner DB, (2002) PTEN protects p53 from Mdm2 and sensitizes cancer cells to chemotherapy. J Biol Chem 277: 5484-5489.
38. Zhou BP, Liao Y, Xia W, Zou Y, Spohn B, et al. (2001) HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat Cell Biol 3: 973-982.
39. Barekati Z, Radpour R, Kohler C, Zhang B, Toniolo P, et al. (2010) Methylation profile of TP53 regulatory pathway and mtDNA alterations in breast cancer patients lacking TP53 mutations. Hum Mol Genet 19: 2936-2946.
40. Rivenbark AG, Livasy CA, Boyd CE, Keppler D, Coleman WB, (2007) Methylation-dependent silencing of CST6 in primary human breast tumors and metastatic lesions. Exp Mol Pathol 83: 188-197.
41. Bachmeier BE, Mohrenz IV, Mirisola V, Schleicher E, Romeo F, et al. (2008) Curcumin downregulates the inflammatory cytokines CXCL1 and-2 in breast cancer cells via NFkappaB. Carcinogenesis 29: 779-789.
42. Croce CM, Calin GA, (2005) miRNAs, cancer, and stem cell division. Cell 122: 6-7.
43. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, et al. (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65: 7065-7070.
44. Tsuchiya Y, Nakajima M, Takagi S, Taniya T, Yokoi T, (2006) MicroRNA regulates the expression of human cytochrome P450 1B1. Cancer Res 66: 9090-9098.
45. Chan JA, Krichevsky AM, Kosik KS, (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65: 6029-6033.
46. Zhu S, Wu H, Wu F, Nie D, Sheng S, et al. (2008) MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18: 350-359.
47. Yan LX, Huang XF, Shao Q, Huang MY, Deng L, et al. (2008) MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA 14: 2348-2360.
48. Mertens-Talcott SU, Chintharlapalli S, Li X, Safe S, (2007) The oncogenic microRNA-27a targets genes that regulate specificity protein transcription factors and the G2-M checkpoint in MDA-MB-231 breast cancer cells. Cancer Res 67: 11001-11011.
49. Ma L, Teruya-Feldstein J, Weinberg RA, (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682-688. Epub 2007 Sep 2026.
50. Vogelstein B, Lane D, Levine AJ, (2000) Surfing the p53 network. Nature 408: 307-310.
51. Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, et al. (2008) Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem 283: 1026-1033.
52. Lu Z, Liu M, Stribinskis V, Klinge CM, Ramos KS, et al. (2008) MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene 27: 4373-4379.
53. Li J, Fu H, Xu C, Tie Y, Xing R, et al. (2010) miR-183 inhibits TGF-beta1-induced apoptosis by downregulation of PDCD4 expression in human hepatocellular carcinoma cells. BMC Cancer 10: 354.
54. Wu B, Chien EY, Mol CD, Fenalti G, Liu W, et al. (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330: 1066-1071.
55. Muller A, Homey B, Soto H, Ge N, Catron D, et al. (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410: 50-56.
56. Teicher BA, Fricker SP, (2010) CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res 16: 2927-2931.
57. Subramaniam DS, Isaacs C, (2005) Utilizing prognostic and predictive factors in breast cancer. Curr Treat Options Oncol 6: 147-159.
58. Rubin I, Yarden Y, (2001) The basic biology of HER2. Ann Oncol 12 (Suppl 1): S3-8.
59. Scott GK, Goga A, Bhaumik D, Berger CE, Sullivan CS, et al. (2007) Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem 282: 1479-1486.
60. Gumireddy K, Sun F, Klein-Szanto AJ, Gibbins JM, Gimotty PA, et al. (2007) In vivo selection for metastasis promoting genes in the mouse. Proc Natl Acad Sci U S A 104: 6696-6701.
61. Redmond KM, Wilson TR, Johnston PG, Longley DB, (2008) Resistance mechanisms to cancer chemotherapy. Front Biosci 13: 5138-5154.
62. Frank NY, Schatton T, Frank MH, (2010) The therapeutic promise of the cancer stem cell concept. J Clin Invest 120: 41-50.
63. Ma J, Dong C, Ji C, (2010) MicroRNA and drug resistance. Cancer Gene Ther 17: 523-531.
64. Ruas M, Peters G, (1998) The p16INK4a/CDKN2A tumor suppressor and its relatives. Biochim Biophys Acta 1378: F115-177.
65. Radpour R, Barekati Z, Kohler C, Lv Q, Bürki N, et al. (2011) Hypermethylation of Tumor Suppressor Genes Involved in Critical Regulatory Pathways for Developing a Blood-Based Test in Breast Cancer. PLoS One 6: e16080.
66. Musgrove EA, Lilischkis R, Cornish AL, Lee CS, Setlur V, et al. (1995) Expression of the cyclin-dependent kinase inhibitors p16INK4, p15INK4B and p21WAF1/CIP1 in human breast cancer. Int J Cancer 63: 584-591.
67. Lal A, Kim HH, Abdelmohsen K, Kuwano Y, Pullmann R Jr, et al. (2008) p16(INK4a) translation suppressed by miR-24. PLoS One 3: e1864.
68. Lin RK, Hsu HS, Chang JW, Chen CY, Chen JT, et al. (2007) Alteration of DNA methyltransferases contributes to 5′CpG methylation and poor prognosis in lung cancer. Lung Cancer 55: 205-213.
69. Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, et al. (2007) MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A 104: 15805-15810.
70. Garzon R, Liu S, Fabbri M, Liu Z, Heaphy CE, (2009) MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood 113: 6411-6418.
71. Savarese F, Davila A, Nechanitzky R, De La Rosa-Velazquez I, Pereira CF, et al. (2009) Satb1 and Satb2 regulate embryonic stem cell differentiation and Nanog expression. Genes Dev 23: 2625-2638.