Frequent loss of endothelin-3 (EDN3) expression due to epigenetic inactivation in human breast cancer

Breast Cancer Research

Volumn 11, Issue 3, 2009, Pages

  Wiesmann, Frank ^a   Veeck, Jürgen ^b   Galm, Oliver ^a   Hartmann, Arndt ^c   Esteller, Manel ^b   Knüchel, Ruth ^a   Dahl, Edgar ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ENDOTHELIN 1; ENDOTHELIN 2; ENDOTHELIN 3; MESSENGER RNA; TRICHOSTATIN A;

ADULT; ADVERSE OUTCOME; ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; BREAST EPITHELIUM; CANCER TISSUE; CONTROLLED STUDY; CPG ISLAND; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MAJOR CLINICAL STUDY; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN METHYLATION; REAL TIME POLYMERASE CHAIN REACTION; TISSUE MICROARRAY; TREATMENT OUTCOME; BIOSYNTHESIS; BREAST TUMOR; CANCER INVASION; CELL DIFFERENTIATION; CELL MOTION; CELL PROLIFERATION; CELL SURVIVAL; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

BREAST NEOPLASMS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; ENDOTHELIN-1; ENDOTHELIN-2; ENDOTHELIN-3; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM INVASIVENESS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

EID: 74049135484     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2319     Document Type: Article

References (53)

1. Grimshaw MJ. Endothelins and hypoxia-inducible factor in cancer. Endocr Relat Cancer 2007, 14:233-244. 10.1677/ERC-07-0057, 17639040.
2. Levin ER. Endothelins. N Engl J Med 1995, 333:356-363. 10.1056/NEJM199508103330607, 7609754.
3. Masaki T. The endothelin family: an overview. J Cardiovasc Pharmacol 2000, 35:S3-S5. 10976772.
4. Grimshaw MJ, Hagemann T, Ayhan A, Gillet CE, Binder C, Balkwill FR. A role for endothelin-2 and its receptors in breast tumor cell invasion. Cancer Res 2004, 64:2461-2468. 10.1158/0008-5472.CAN-03-1069, 15059899.
5. Smollich M, Wulfing P. The endothelin axis: a novel target for pharmacotherapy of female malignancies. Curr Vasc Pharmacol 2007, 5:239-248. 10.2174/157016107781024082, 17627567.
6. Pollock DM, Keith TL, Highsmith RF. Endothelin receptors and calcium signaling. FASEB J 1995, 9:1196-1204.
7. Bagnato A, Catt KJ. Endothelin as autocrine regulators of tumor cell growth. Trends Endocrinol Metab 1998, 9:378-383. 10.1016/S1043-2760(98)00094-0, 18406309.
8. Bagnato A, Spinella F, Rosano L. Emerging role of the endothelin axis in ovarian tumour progression. Endocr Relat Cancer 2005, 12:761-772. 10.1677/erc.1.01077, 16322321.
9. Pla P, Larue L. Involvement of endothelin receptors in normal and pathological development of neural crest cells. Int J Dev Biol 2003, 47:315-325.
10. Alanen K, Deng DX, Chakrabarti S. Augmented expression of endothelin-1, endothelin-3 and the endothelin-B receptor in breast carcinoma. Histopathology 2000, 36:161-167. 10.1046/j.1365-2559.2000.00795.x, 10672062.
11. Berry P, Burchill S. Endothelins may modulate invasion and proliferation of Ewing's sarcoma and neuroblastoma. Clin Sci (Lond) 2002, 103(Suppl 48):322S-326S. 12193114.
12. Grimshaw MJ. Endothelins in breast tumour cell invasion. Cancer Lett 2005, 222:129-138. 10.1016/j.canlet.2004.08.029, 15863261.
13. Bagnato A, Natali PG. Endothelin receptors as novel targets in tumor therapy. J Transl Med 2004, 2:16. 436068, 15165288, 10.1186/1479-5876-2-16.
14. Spinella F, Rosano L, Di Castro V, Natali PG, Bagnato A. Endothelin-1 induces vascular endothelial growth factor by increasing hypoxia-inducible factor-1alpha in ovarian carcinoma cells. J Biol Chem 2002, 277:27850-27855. 10.1074/jbc.M202421200, 12023962.
15. Nelson JB, Chan-Tack K, Hedican SP, Magnuson SR, Opgenorth TJ, Bova GS, Simons JW. Endothelin-1 production and decreased endothelin B receptor expression in advanced prostate cancer. Cancer Res 1996, 56:663-668.
16. Hagemann T, Binder C, Binder L, Pukrop T, Trümper L, Grimshaw MJ. Expression of endothelins and their receptors promotes an invasive phenotype of breast tumor cells but is insufficient to induce invasion in benign cells. DNA Cell Biol 2005, 24:766-776. 10.1089/dna.2005.24.766, 16274297.
17. Mitaka C, Hirata Y, Ichikawa K, Yokoyama K, Emori T. Effects of TNF-alpha on hemodynamic changes and circulating endothelium-derived vasoactive factors in dogs. Am J Physiol 1994, 267:H1530-H1536. 7943398.
18. Thomson E, Kumarathasan P, Vincent R. Pulmonary expression of preproET-1 and preproET-3 mRNAs is altered re ciprocally in rats after inhalation of air pollutants. Exp Biol Med (Maywood) 2006, 231:979-984.
19. TNM Classification of Malignant Tumours 2002, New York: Wiley-Liss, Sobin LH, Wittekind C, 6.
20. Elston EW, Ellis IO. Method for grading breast cancer. J Clin Pathol 1993, 46:189-190. 501162, 8459046, 10.1136/jcp.46.2.189-b.
21. Bubendorf L, Nocito A, Moch H, Sauter G. Tissue microarray (TMA) technology: miniaturized pathology archives for high-throughput in situ studies. J Pathol 2001, 195:72-79. 10.1002/path.893, 11568893.
22. Veeck J, Niederacher D, An H, Klopocki E, Wiesmann F, Betz B, Galm O, Camara O, Dürst M, Kristiansen G, Huszka C, Knüchel R, Dahl E. Aberrant methylation of the Wnt antagonist SFRP1 in breast cancer is associated with unfavourable prognosis. Oncogene 2006, 25:3479-3488. 10.1038/sj.onc.1209386, 16449975.
23. Fink L, Seeger W, Ermert L, Hänze J, Stahl U, Grimminger F, Kummer W, Bohle RM. Real-time quantitative RT-PCR after laser-assisted cell picking. Nat Med 1998, 4:1329-1333. 10.1038/3327, 9809560.
24. Remmele W, Stegner HE. Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathologe 1987, 8:138-140.
25. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002, 18:1427-1431. 10.1093/bioinformatics/18.11.1427, 12424112.
26. Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996, 93:9821-9826. 38513, 8790415, 10.1073/pnas.93.18.9821.
27. Dahl E, Sadr-Nabavi A, Klopocki E, Betz B, Grube S, Kreutzfeld R, Himmelfarb M, Gelling S, Klaman I, Hinzmann B, Kristiansen G, Grützmann R, Kuner R, Petschke B, Rhiem K, Wiechen K, Sers C, Wiestler O, Schneider A, Höfler H, Nährig J, Dietel M, Schäfer R, Rosenthal A, Schmutzler R, Dürst M, Meindl A, Niederacher D. Systematic identification and molecular characterization of genes differentially expressed in breast and ovarian cancer. J Pathol 2005, 205:21-28. 15586368 .
28. Dahl E, Kristiansen G, Gottlob K, Klaman I, Ebner E, Hinzmann B, Hermann K, Pilarsky C, Dürst M, Klinkhammer-Schalke M, Blaszyk H, Knuechel R, Hartmann A, Rosenthal A, Wild PJ. Molecular profiling of laser-microdissected matched tumor and normal breast tissue identifies karyopherin alpha2 as a potential novel prognostic marker in breast cancer. Clin Cancer Res 2006, 12:3950-3960. 10.1158/1078-0432.CCR-05-2090, 16818692.
29. Wallace BA, Janes RW, Bassolino DA, Krystek SR. A comparison of X-ray and NMR structures for human endothelin-1. Protein Sci 1995, 4:75-83. 2142965, 7773179.
30. Esteller M. Epigenetic gene silencing in cancer: the DNA hypermethylome. Hum Mol Genet 2007, 16(Spec No 1):R50-59. 10.1093/hmg/ddm018, 17613547.
31. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, Chen WD, Pretlow TP, Yang B, Akiyama Y, Van Engeland M, Toyota M, Tokino T, Hinoda Y, Imai K, Herman JG, Baylin SB. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 2004, 36:417-422. 10.1038/ng1330, 15034581.
32. Donninger H, Bonome T, Radonovich M, Pise-Masison CA, Brady J, Shih JH, Barrett JC, Birrer MJ. Whole genome expression profiling of advance stage papillary serous ovarian cancer reveals activated pathways. Oncogene 2004, 23:8065-8077. 10.1038/sj.onc.1207959, 15361855.
33. Kopetz ES, Nelson JB, Carducci MA. Endothelin-1 as a target for therapeutic intervention. Invest New Drugs 2002, 20:173-182. 10.1023/A:1015630513908, 12099577.
34. Wulfing P, Diallo R, Kersting C, Wülfing C, Poremba C, Rody A, Greb RR, Böcker W, Kiesel L. Expression of endothelin-1, endothelin-A, and endothelin-B receptor in human breast cancer and correlation with long-term follow-up. Clin Cancer Res 2003, 9:4125-4131. 14519635.
35. Klopocki E, Kristiansen G, Wild PJ, Klaman I, Castanos-Velez E, Singer G, Stöhr R, Simon R, Sauter G, Leibiger H, Essers L, Weber B, Hermann K, Rosenthal A, Hartmann A, Dahl E. Loss of SFRP1 is associated with breast cancer progression and poor prognosis in early stage tumors. Int J Oncol 2004, 25:641-649.
36. Veeck J, Chorovicer M, Naami A, Breuer E, Zafrakas M, Bektas N, Dürst M, Kristiansen G, Wild PJ, Hartmann A, Knuechel R, Dahl E. The extracellular matrix protein ITIH5 is a novel prognostic marker in invasive node-negative breast cancer and its aberrant expression is caused by promoter hypermethylation. Oncogene 2008, 27:865-875. 10.1038/sj.onc.1210669, 17653090.
37. Chen SC, Lin CY, Chen YH, Fang HY, Cheng CY, Chang CW, Chen RA, Tai HL, Lee CH, Chou MC, Lin TS, Hsu LS. Aberrant promoter methylation of EDNRB in lung cancer in Taiwan. Oncol Rep 2006, 15:167-172.
38. Pao MM, Tsutsumi M, Liang G, Uzvolgyi E, Gonzales FA, Jones PA. The endothelin receptor B (EDNRB) promoter displays heterogeneous, site specific methylation patterns in normal and tumor cells. Hum Mol Genet 2001, 10:903-910. 10.1093/hmg/10.9.903, 11309363.
39. De Marzo AM, Isaacs WB, Nelson WG. Hypermethylation of CpG islands in primary and metastatic human prostate cancer. Cancer Res 2004, 64:1975-1986. 10.1158/0008-5472.CAN-03-3972, 15026333.
40. Friedrich MG, Weisenberger DJ, Cheng JC, Chandrasoma S, Siegmund KD, Gonzalgo ML, Toma MI, Huland H, Yoo C, Tsai YC, Nichols PW, Bochner BH, Jones PA, Liang G. Detection of methylated apoptosis-associated genes in urine sediments of bladder cancer patients. Clin Cancer Res 2004, 10:7457-7465. 10.1158/1078-0432.CCR-04-0930, 15569975.
41. Pflug BR, Zheng H, Udan MS, D'Antonio JM, Marshall FF, Brooks JD, Nelson JB. Endothelin-1 promotes cell survival in renal cell carcinoma through the ET(A) receptor. Cancer Lett 2007, 246:139-148. 10.1016/j.canlet.2006.02.007, 16581180.
42. Hsu LS, Lee HC, Chau GY, Yin PH, Chi CW, Lui WY. Aberrant methylation of EDNRB and p16 genes in hepatocellular carcinoma (HCC) in Taiwan. Oncol Rep 2006, 15:507-511.
43. Zhao BJ, Sun DG, Zhang M, Tan SN, Ma X. Identification of aberrant promoter methylation of EDNRB gene in esophageal squamous cell carcinoma. Dis Esophagus 2009, 22:55-61. 10.1111/j.1442-2050.2008.00848.x, 18564167.
44. Lo KW, Tsang YS, Kwong J, To KF, Teo PM, Huang DP. Promoter hypermethylation of the EDNRB gene in nasopharyngeal carcinoma. Int J Cancer 2002, 98:651-655. 10.1002/ijc.10271, 11920632.
45. Hsiao PC, Liu MC, Chen LM, Tsai CY, Wang YT, Chen J, Hsu LS. Promoter methylation of p16 and EDNRB gene in leukemia patients in Taiwan. Chin J Physiol 2008, 51:27-31.
46. Sun de J, Liu Y, Lu DC, Kim W, Lee JH, Maynard J, Deisseroth A. Endothelin-3 growth factor levels decreased in cervical cancer compared with normal cervical epithelial cells. Hum Pathol 2007, 38:1047-1056. 10.1016/j.humpath.2006.12.015, 17445867.
47. Dréau D, Karaa A, Culberson C, Wyan H, McKillop IH, Clemens MG. Bosentan inhibits tumor vascularization and bone metastasis in an immunocompetent skin-fold chamber model of breast carcinoma cell metastasis. Clin Exp Metastasis 2006, 23:41-53. 10.1007/s10585-006-9016-z, 16826430.
48. Nelson J, Bagnato A, Battistini B, Nisen P. The endothelin axis: emerging role in cancer. Nat Rev Cancer 2003, 3:110-116. 10.1038/nrc990, 12563310.
49. Rosanò L, Di Castro V, Spinella F, Nicotra MR, Natali PG, Bagnato A. ZD4054, a specific antagonist of the endothelin A receptor, inhibits tumor growth and enhances paclitaxel activity in human ovarian carcinoma in vitro and in vivo. Mol Cancer Ther 2007, 6:2003-2011. 10.1158/1535-7163.MCT-07-0151, 17620430.
50. Bagnato A, Cirilli A, Salani D, Simeone P, Muller A, Nicotra MR, Natali PG, Venuti A. Growth inhibition of cervix carcinoma cells in vivo by endothelin A receptor blockade. Cancer Res 2002, 62:6381-6384.
51. Akhavan A, McHugh KH, Guruli G, Bies RR, Zamboni WC, Strychor SA, Nelson JB, Pflug BR. Endothelin receptor A blockade enhances taxane effects in prostate cancer. Neoplasia 2006, 8:725-732. 1584296, 16984730, 10.1593/neo.06388.
52. Jazaeri AA, Awtrey CS, Chandramouli GV, Chuang YE, Khan J, Sotiriou C, Aprelikova O, Yee CJ, Zorn KK, Birrer MJ, Barrett JC, Boyd J. Gene expression profiles associated with response to chemotherapy in epithelial ovarian cancers. Clin Cancer Res 2005, 11:6300-6310. 10.1158/1078-0432.CCR-04-2682, 16144934.
53. Ortega Mateo A, De Artiñano AA. Highlights on endothelins: a review. Pharmacol Res 1997, 36:339-351. 10.1006/phrs.1997.0246, 9441724.