The effect of the histone deacetylase inhibitor M344 on BRCA1 expression in breast and ovarian cancer cells

Cancer Cell International

Volumn 11, Issue , 2011, Pages

  Weberpals, Johanne I ^a,b   O'Brien, Anna M ^b,c   Niknejad, Nima ^b   Garbuio, Kyla D ^b,c   Clark Knowles, Katherine V ^b   Dimitroulakos, Jim ^b,c  

^a UNIVERSITY OF OTTAWA   (Canada)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; CISPLATIN; HISTONE DEACETYLASE INHIBITOR; HISTONE H2AX; HISTONE H4; M 344; MESSENGER RNA; PLATINUM; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BREAST CANCER; CHROMATIN IMMUNOPRECIPITATION; CYTOTOXICITY; DNA DAMAGE; DOWN REGULATION; DRUG EFFECT; DRUG POTENTIATION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; OVARY CANCER; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 80051785180     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/1475-2867-11-29     Document Type: Article

References (61)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer Statistics, 2010. CA Cancer J Clin 2000, 60:277-300.
2. Hall JM, Lee MK, Newman B, Morrow JE, Anderson LA, Huey B, King MC. Linkage of early-onset familial breast cancer to chromosome 17q21. Science 1990, 250:1684-9. 10.1126/science.2270482, 2270482.
3. Miki Y, Swensen J, Shattuck-Eidens D, Futreal PA, Harshman K, Tavtigian S, Liu Q, Cochran C, Bennett LM, Ding W, et al. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 1994, 266:66-71. 10.1126/science.7545954, 7545954.
4. Thrall M, Gallion HH, Kryscio R, Kapali M, Armstrong DK, DeLoia JA. BRCA1 expression in a large series of sporadic ovarian carcinomas: a Gynecologic Oncology Group study. Int J Gynecol Cancer 2006, 16(Suppl 1):166-71.
5. Turner N, Tutt A, Ashworth A. Hallmarks of 'BRCAness' in sporadic cancers. Nat Rev Cancer 2004, 4:814-9. 10.1038/nrc1457, 15510162.
6. Quinn JE, Kennedy RD, Mullan PB, Gilmore PM, Carty M, Johnston PG, Harkin DP. BRCA1 functions as a differential modulator of chemotherapy-induced apoptosis. Cancer research 2003, 63:6221-8.
7. Weberpals J, Garbuio K, O'Brien A, Clark-Knowles K, Doucette S, Antoniouk O, Goss G, Dimitroulakos J. The DNA repair proteins BRCA1 and ERCC1 as predictive markers in sporadic ovarian cancer. Int J Cancer 2009, 124:806-15. 10.1002/ijc.23987, 19035454.
8. Lambie H, Miremadi A, Pinder SE, Bell JA, Wencyk P, Paish EC, Macmillan RD, Ellis IO. Prognostic significance of BRCA1 expression in sporadic breast carcinomas. J Pathol 2003, 200:207-13. 10.1002/path.1348, 12754741.
9. Taron M, Rosell R, Felip E, Mendez P, Souglakos J, Ronco MS, Queralt C, Majo J, Sanchez JM, Sanchez JJ, Maestre J. BRCA1 mRNA expression levels as an indicator of chemoresistance in lung cancer. Hum Mol Genet 2004, 13:2443-9. 10.1093/hmg/ddh260, 15317748.
10. Moynahan ME, Cui TY, Jasin M. Homology-directed dna repair, mitomycin-c resistance, and chromosome stability is restored with correction of a Brca1 mutation. Cancer research 2001, 61:4842-50.
11. Martinez-Iglesias O, Ruiz-Llorente L, Sanchez-Martinez R, Garcia L, Zambrano A, Aranda A. Histone deacetylase inhibitors: mechanism of action and therapeutic use in cancer. Clin Transl Oncol 2008, 10:395-8. 10.1007/s12094-008-0221-x, 18628067.
12. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 2006, 5:769-84. 10.1038/nrd2133, 16955068.
13. Marks PA, Jiang X. Histone deacetylase inhibitors in programmed cell death and cancer therapy. Cell Cycle 2005, 4:549-51. 10.4161/cc.4.4.1564, 15738652.
14. Khabele D, Son DS, Parl AK, Goldberg GL, Augenlicht LH, Mariadason JM, Rice VM. Drug-induced inactivation or gene silencing of class I histone deacetylases suppresses ovarian cancer cell growth: implications for therapy. Cancer Biol Ther 2007, 6:795-801. 10.4161/cbt.6.5.4007, 17387270.
15. Dietrich CS, Greenberg VL, DeSimone CP, Modesitt SC, van Nagell JR, Craven R, Zimmer SG. Suberoylanilide hydroxamic acid (SAHA) potentiates paclitaxel-induced apoptosis in ovarian cancer cell lines. Gynecol Oncol 2010, 116:126-30. 10.1016/j.ygyno.2009.09.039, 19875160.
16. Modesitt SC, Sill M, Hoffman JS, Bender DP. A phase II study of vorinostat in the treatment of persistent or recurrent epithelial ovarian or primary peritoneal carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol 2008, 109:182-6. 10.1016/j.ygyno.2008.01.009, 18295319.
17. Kim MS, Blake M, Baek JH, Kohlhagen G, Pommier Y, Carrier F. Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer research 2003, 63:7291-300.
18. Ozaki K, Kishikawa F, Tanaka M, Sakamoto T, Tanimura S, Kohno M. Histone deacetylase inhibitors enhance the chemosensitivity of tumor cells with cross-resistance to a wide range of DNA-damaging drugs. Cancer Sci 2008, 99:376-84. 10.1111/j.1349-7006.2007.00669.x, 18201278.
19. Ramalingam SS, Parise RA, Ramanathan RK, Lagattuta TF, Musguire LA, Stoller RG, Potter DM, Argiris AE, Zwiebel JA, Egorin MJ, Belani CP. Phase I and pharmacokinetic study of vorinostat, a histone deacetylase inhibitor, in combination with carboplatin and paclitaxel for advanced solid malignancies. Clin Cancer Res 2007, 13:3605-10. 10.1158/1078-0432.CCR-07-0162, 17510206.
20. Takai N, Ueda T, Nishida M, Nasu K, Narahara H. M344 is a novel synthesized histone deacetylase inhibitor that induces growth inhibition, cell cycle arrest, and apoptosis in human endometrial cancer and ovarian cancer cells. Gynecol Oncol 2006, 101:108-13. 10.1016/j.ygyno.2005.09.044, 16263156.
21. Olsen EA, Kim YH, Kuzel TM, Pacheco TR, Foss FM, Parker S, Frankel SR, Chen C, Ricker JL, Arduino JM, Duvic M. Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J Clin Oncol 2007, 25:3109-15. 10.1200/JCO.2006.10.2434, 17577020.
22. Ghosh S, Lu Y, Hu Y. A Role of CREB in BRCA1 Constitutive Promoter Activity and Aromatase Basal Expression. Int J Biomed Sci 2008, 4:260-5. 2703435, 19568323.
23. Henkels KM, Turchi JJ. Induction of apoptosis in cisplatin-sensitive and -resistant human ovarian cancer cell lines. Cancer research 1997, 57:4488-92.
24. Schilder RJ, Hall L, Monks A, Handel LM, Fornace AJ, Ozols RF, Fojo AT, Hamilton TC. Metallothionein gene expression and resistance to cisplatin in human ovarian cancer. Int J Cancer 1990, 45:416-22. 10.1002/ijc.2910450306, 2307530.
25. Tomlinson GE, Chen TT, Stastny VA, Virmani AK, Spillman MA, Tonk V, Blum JL, Schneider NR, Wistuba, Shay JW, Minna JD, Gazdar AF. Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer research 1998, 58:3237-42.
26. Kainu T, Kononen J, Johansson O, Olsson H, Borg A, Isola J. Detection of germline BRCA1 mutations in breast cancer patients by quantitative messenger RNA in situ hybridization. Cancer research 1996, 56:2912-5.
27. Rakha EA, El-Sheikh SE, Kandil MA, El-Sayed ME, Green AR, Ellis IO. Expression of BRCA1 protein in breast cancer and its prognostic significance. Hum Pathol 2008, 39:857-65. 10.1016/j.humpath.2007.10.011, 18400253.
28. Pilch DR, Sedelnikova OA, Redon C, Celeste A, Nussenzweig A, Bonner WM. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem Cell Biol 2003, 81:123-9. 10.1139/o03-042, 12897845.
29. Husain A, He G, Venkatraman ES, Spriggs DR. BRCA1 up-regulation is associated with repair-mediated resistance to cis-diamminedichloroplatinum(II). Cancer research 1998, 58:1120-3.
30. Burkitt K, Ljungman M. Phenylbutyrate interferes with the Fanconi anemia and BRCA pathway and sensitizes head and neck cancer cells to cisplatin. Mol Cancer 2008, 7:24. 10.1186/1476-4598-7-24, 2276233, 18325101.
31. Zhang Y, Carr T, Dimtchev A, Zaer N, Dritschilo A, Jung M. Attenuated DNA damage repair by trichostatin A through BRCA1 suppression. Radiat Res 2007, 168:115-24. 10.1667/RR0811.1, 17722998.
32. Kachhap SK, Rosmus N, Collis SJ, Kortenhorst MS, Wissing MD, Hedayati M, Shabbeer S, Mendonca J, Deangelis J, Marchionni L, Lin J, Hoti N, Nortier JW, DeWeese TL, Hammers H, Carducci MA. Downregulation of homologous recombination DNA repair genes by HDAC inhibition in prostate cancer is mediated through the E2F1 transcription factor. PloS one 5:e11208.
33. Konsoula Z, Cao H, Velena A, Jung M. Adamantanyl-histone deacetylase inhibitor H6CAHA exhibits favorable pharmacokinetics and augments prostate cancer radiation sensitivity. International journal of radiation oncology, biology, physics 79:1541-8.
34. Goh M, Chen F, Paulsen MT, Yeager AM, Dyer ES, Ljungman M. Phenylbutyrate attenuates the expression of Bcl-X(L), DNA-PK, caveolin-1, and VEGF in prostate cancer cells. Neoplasia 2001, 3:331-8. 10.1038/sj.neo.7900165, 1505863, 11571633.
35. Karagiannis TC, Harikrishnan KN, El-Osta A. The histone deacetylase inhibitor, Trichostatin A, enhances radiation sensitivity and accumulation of gammaH2A.X. Cancer Biol Ther 2005, 4:787-93.
36. Lee CK, Wang S, Huang X, Ryder J, Liu B. HDAC inhibition synergistically enhances alkylator-induced DNA damage responses and apoptosis in multiple myeloma cells. Cancer Lett 296:233-40.
37. Munshi A, Tanaka T, Hobbs ML, Tucker SL, Richon VM, Meyn RE. Vorinostat, a histone deacetylase inhibitor, enhances the response of human tumor cells to ionizing radiation through prolongation of gamma-H2AX foci. Molecular cancer therapeutics 2006, 5:1967-74. 10.1158/1535-7163.MCT-06-0022, 16928817.
38. Baschnagel A, Russo A, Burgan WE, Carter D, Beam K, Palmieri D, Steeg PS, Tofilon P, Camphausen K. Vorinostat enhances the radiosensitivity of a breast cancer brain metastatic cell line grown in vitro and as intracranial xenografts. Molecular cancer therapeutics 2009, 8:1589-95. 10.1158/1535-7163.MCT-09-0038, 19509253.
39. Chinnaiyan P, Vallabhaneni G, Armstrong E, Huang SM, Harari PM. Modulation of radiation response by histone deacetylase inhibition. International journal of radiation oncology, biology, physics 2005, 62:223-9. 10.1016/j.ijrobp.2004.12.088, 15850925.
40. Bochar DA, Wang L, Beniya H, Kinev A, Xue Y, Lane WS, Wang W, Kashanchi F, Shiekhattar R. BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell 2000, 102:257-65. 10.1016/S0092-8674(00)00030-1, 10943845.
41. Yarden RI, Brody LC. BRCA1 interacts with components of the histone deacetylase complex. Proc Natl Acad Sci USA 1999, 96:4983-8. 10.1073/pnas.96.9.4983, 21803, 10220405.
42. Yokota Y. Id and development. Oncogene 2001, 20:8290-8. 10.1038/sj.onc.1205090, 11840321.
43. Beger C, Pierce LN, Kruger M, Marcusson EG, Robbins JM, Welcsh P, Welch PJ, Welte K, King MC, Barber JR, Wong-Staal F. Identification of Id4 as a regulator of BRCA1 expression by using a ribozyme-library-based inverse genomics approach. Proc Natl Acad Sci USA 2001, 98:130-5. 10.1073/pnas.98.1.130, 14556, 11136250.
44. Roldan G, Delgado L, Muse IM. Tumoral expression of BRCA1, estrogen receptor alpha and ID4 protein in patients with sporadic breast cancer. Cancer Biol Ther 2006, 5:505-10. 10.4161/cbt.5.5.2597, 16582598.
45. Welcsh PL, Lee MK, Gonzalez-Hernandez RM, Black DJ, Mahadevappa M, Swisher EM, Warrington JA, King MC. BRCA1 transcriptionally regulates genes involved in breast tumorigenesis. Proc Natl Acad Sci USA 2002, 99:7560-5. 10.1073/pnas.062181799, 124283, 12032322.
46. Strait KA, Warnick CT, Ford CD, Dabbas B, Hammond EH, Ilstrup SJ. Histone deacetylase inhibitors induce G2-checkpoint arrest and apoptosis in cisplatinum-resistant ovarian cancer cells associated with overexpression of the Bcl-2-related protein Bad. Molecular cancer therapeutics 2005, 4:603-11. 10.1158/1535-7163.MCT-04-0107, 15827334.
47. Ueda T, Takai N, Nishida M, Nasu K, Narahara H. Apicidin, a novel histone deacetylase inhibitor, has profound anti-growth activity in human endometrial and ovarian cancer cells. Int J Mol Med 2007, 19:301-8.
48. Munster PN, Troso-Sandoval T, Rosen N, Rifkind R, Marks PA, Richon VM. The histone deacetylase inhibitor suberoylanilide hydroxamic acid induces differentiation of human breast cancer cells. Cancer research 2001, 61:8492-7.
49. Bali P, Pranpat M, Swaby R, Fiskus W, Yamaguchi H, Balasis M, Rocha K, Wang HG, Richon V, Bhalla K. Activity of suberoylanilide hydroxamic Acid against human breast cancer cells with amplification of her-2. Clin Cancer Res 2005, 11:6382-9. 10.1158/1078-0432.CCR-05-0344, 16144943.
50. Di LJ, Fernandez AG, De Siervi A, Longo DL, Gardner K. Transcriptional regulation of BRCA1 expression by a metabolic switch. Nature structural & molecular biology 17:1406-13.
51. Rikiishi H, Shinohara F, Sato T, Sato Y, Suzuki M, Echigo S. Chemosensitization of oral squamous cell carcinoma cells to cisplatin by histone deacetylase inhibitor, suberoylanilide hydroxamic acid. Int J Oncol 2007, 30:1181-8.
52. Chen CS, Wang YC, Yang HC, Huang PH, Kulp SK, Yang CC, Lu YS, Matsuyama S, Chen CY, Chen CS. Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation. Cancer research 2007, 67:5318-27. 10.1158/0008-5472.CAN-06-3996, 17545612.
53. Adimoolam S, Sirisawad M, Chen J, Thiemann P, Ford JM, Buggy JJ. HDAC inhibitor PCI-24781 decreases RAD51 expression and inhibits homologous recombination. Proc Natl Acad Sci USA 2007, 104:19482-7. 10.1073/pnas.0707828104, 2148315, 18042714.
54. Candelaria M, Gallardo-Rincon D, Arce C, Cetina L, Aguilar-Ponce JL, Arrieta O, Gonzalez-Fierro A, Chavez-Blanco A, de la Cruz-Hernandez E, Camargo MF, Trejo-Becerril C, Perez-Cardenas E, Perez-Plasencia C, Taja-Chayeb L, Wegman-Ostrosky T, Revilla-Vazquez A, Duenas-Gonzalez A. A phase II study of epigenetic therapy with hydralazine and magnesium valproate to overcome chemotherapy resistance in refractory solid tumors. Ann Oncol 2007, 18:1529-38. 10.1093/annonc/mdm204, 17761710.
55. Dizin E, Irminger-Finger I. Negative feedback loop of BRCA1-BARD1 ubiquitin ligase on estrogen receptor alpha stability and activity antagonized by cancer-associated isoform of BARD1. The international journal of biochemistry & cell biology 42:693-700.
56. Wu W, Sato K, Koike A, Nishikawa H, Koizumi H, Venkitaraman AR, Ohta T. HERC2 is an E3 ligase that targets BRCA1 for degradation. Cancer research 70:6384-92.
57. Choudhury AD, Xu H, Baer R. Ubiquitination and proteasomal degradation of the BRCA1 tumor suppressor is regulated during cell cycle progression. The Journal of biological chemistry 2004, 279:33909-18. 10.1074/jbc.M403646200, 15166217.
58. Lixia M, Zhijian C, Chao S, Chaojiang G, Congyi Z. Alternative splicing of breast cancer associated gene BRCA1 from breast cancer cell line. Journal of biochemistry and molecular biology 2007, 40:15-21. 10.5483/BMBRep.2007.40.1.015, 17244477.
59. Yoshikawa K, Honda K, Inamoto T, Shinohara H, Yamauchi A, Suga K, Okuyama T, Shimada T, Kodama H, Noguchi S, Gazdar AF, Yamaoka Y, Takahashi R. Reduction of BRCA1 protein expression in Japanese sporadic breast carcinomas and its frequent loss in BRCA1-associated cases. Clin Cancer Res 1999, 5:1249-61.
60. Wilson CA, Payton MN, Elliott GS, Buaas FW, Cajulis EE, Grosshans D, Ramos L, Reese DM, Slamon DJ, Calzone FJ. Differential subcellular localization, expression and biological toxicity of BRCA1 and the splice variant BRCA1-delta11b. Oncogene 1997, 14:1-16. 10.1038/sj.onc.1200924, 9010228.
61. Wang A, Schneider-Broussard R, Kumar AP, MacLeod MC, Johnson DG. Regulation of BRCA1 expression by the Rb-E2F pathway. The Journal of biological chemistry 2000, 275:4532-6. 10.1074/jbc.275.6.4532, 10660629.