Cytotoxic effects of Jay Amin hydroxamic acid (JAHA), a ferrocene-based class i histone deacetylase inhibitor, on triple-negative MDA-MB231 breast cancer cells

Chemical Research in Toxicology

Volumn 25, Issue 11, 2012, Pages 2608-2616

  Librizzi, Mariangela ^a   Longo, Alessandra ^a   Chiarelli, Roberto ^a   Amin, Jahanghir ^b   Spencer, John ^c   Luparello, Claudio ^a  

^a UNIVERSITY OF PALERMO   (Italy)

^b UNIVERSITY OF GREENWICH   (United Kingdom)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; HISTONE DEACETYLASE INHIBITOR; JAY AMIN HYDROXAMIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BIOASSAY; BREAST CANCER; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL VIABILITY; COMPETITIVE INHIBITION; CONTROLLED STUDY; CYTOTOXICITY; FLOW CYTOMETRY; IC 50; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; FERROUS COMPOUNDS; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MOLECULAR STRUCTURE; REACTIVE OXYGEN SPECIES; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 84869453615     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx300376h     Document Type: Article

References (54)

1. Spencer, et al. (2011) ACS Med. Chem. Lett. 2, 358 - 362
2. Bell, O., Tiwari, V. K., Thomä, N. H., and Schübeler, D. (2011) Determinants and dynamics of genome accessibility Nat. Rev. Genet. 12, 554-564
3. Majdzadeh, N., Morrison, B. E., and D'Mello, S. R. (2008) Class IIA HDACs in the regulation of neurodegeneration Front. Biosci. 13, 1072-1082
4. Grabiec, A. M., Tak, P. P., and Reedquist, K. A. (2011) Function of histone deacetylase inhibitors in inflammation Crit. Rev. Immunol. 31, 233-263
5. Hagelkruys, A., Sawicka, A., Rennmayr, M., and Seiser, C. (2011) The biology of HDAC in cancer: the nuclear and epigenetic components Handb. Exp. Pharmacol. 206, 13-37
6. Manteuffel-Cymborowska, M. (1999) Nuclear receptors, their coactivators and modulation of transcription Acta Biochim. Pol. 46, 77-89
7. Green, C. D. and Han, J. D. (2011) Epigenetic regulation by nuclear receptors Epigenomics 3, 59-72
8. Glozak, M. A., Sengupta, N., Zhang, X., and Seto, E. (2005) Acetylation and deacetylation of non-histone proteins Gene 363, 15-23
9. de Ruijter, A. J., van Gennip, A. H., Caron, H. N., Kemp, S., and van Kuilenburg, A. B. (2003) Histone deacetylases (HDACs): Characterization of the classical HDAC family Biochem. J. 370 (Part 3) 737-749
10. Dickinson, M., Johnstone, R. W., and Prince, H. M. (2010) Histone deacetylase inhibitors: Potential targets responsible for their anti-cancer effect Invest. New Drugs 28 (Suppl. 1) S3-S20
11. Kim, H. J. and Bae, S. C. (2011) Histone deacetylase inhibitors: Molecular mechanisms of action and clinical trials as anti-cancer drugs Am. J. Transl. Res. 3, 166-179
12. Mann, B. S., Johnson, J. R., Cohen, M. H., Justice, R., and Pazdur, R. (2007) FDA approval summary: Vorinostat for treatment of advanced primary cutaneous T-cell lymphoma Oncologist 12, 1247-1252
13. Spencer, J., Amin, J., Wang, M., Packham, G., Alwi, S. S., Tizzard, G. J., Coles, S. J., Paranal, R. M., Bradner, J. E., and Heightman, T. D. (2011) Synthesis and biological evaluation of JAHAs: ferrocene-based histone deacetylase inhibitors ACS Med. Chem. Lett. 2, 358-362
14. Kassam, F., Enright, K., Dent, R., Dranitsaris, G., Myers, J., Flynn, C., Fralick, M., Kumar, R., and Clemons, M. (2009) Survival outcomes for patients with metastatic triple-negative breast cancer: Implications for clinical practice and trial design Clin. Breast Cancer 9, 29-33
15. Gartel, A. L., Feliciano, C., and Tyner, A. L. (2003) A new method for determining the status of p53 in tumor cell lines of different origin Oncol. Res. 13, 405-408
16. Luparello, C., David, F., Campisi, G., and Sirchia, R. (2003) T47-D cells and type V collagen: A model for the study of apoptotic gene expression by breast cancer cells Biol. Chem. 384, 965-975
17. Luparello, C., Sirchia, R., and Lo Sasso, B. (2008) Midregion PTHrP regulates Rip1 and caspase expression in MDA-MB231 breast cancer cells Breast Cancer Res. Treat. 111, 461-474
18. Cannino, G., Ferruggia, E., Luparello, C., and Rinaldi, A. M. (2008) Effects of cadmium chloride on some mitochondria-related activity and gene expression of human MDA-MB231 breast tumor cells J. Inorg. Biochem. 102, 1668-1676
19. Cossarizza, A. and Salvioli, S. (2001) Flow cytometric analysis of mitochondrial membrane potential using JC-1 Curr. Protoc. Cytom. 14.1-14.7
20. Jiang, H., White, E. J., Conrad, C., Gomez-Manzano, C., and Fueyo, J. (2009) Autophagy pathways in glioblastoma Methods Enzymol. 453, 273-286
21. Chen, Y., Azad, M. B., and Gibson, S. B. (2010) Methods for detecting autophagy and determining autophagy-induced cell death Can. J. Physiol. Pharmacol. 88, 285-295
22. Chiarelli, R., Agnello, M., and Roccheri, M. C. (2011) Sea urchin embryos as a model system for studying autophagy induced by cadmium stress Autophagy 7, 1028-1034
23. Armstrong, L. J. and Gorski, S. M. (2010) Breast cancer and autophagy. In Breast Cancer: Causes, Diagnosis and Treatment (Romero, M. E. and Dashek, L. M., Eds.) pp 53-88, Nova Science Publishers Inc., New York.
24. Chang, S. B., Miron, P., Miron, A., and Iglehart, J. D. (2007) Rapamycin inhibits proliferation of estrogen-receptor-positive breast cancer cells J. Surg. Res. 138, 37-44
25. Yamamoto, S., Tanaka, K., Sakimura, R., Okada, T., Nakamura, T., Li, Y., Takasaki, M., Nakabeppu, Y., and Iwamoto, Y. (2008) Suberoylanilide hydroxamic acid (SAHA) induces apoptosis or autophagy-associated cell death in chondrosarcoma cell lines Anticancer Res. 28, 1585-1591
26. Mizushima, N. and Yoshimori, T. (2007) How to interpret LC3 immunoblotting Autophagy 3, 542-545
27. Yang, Y. P., Liang, Z. Q., Gu, Z. L., and Qin, Z. H. (2005) Molecular mechanism and regulation of autophagy Acta Pharmacol. Sin. 26, 1421-1434
28. Gluz, O., Liedtke, C., Gottschalk, N., Pusztai, L., Nitz, U., and Harbeck, N. (2009) Triple-negative breast cancer-current status and future directions Ann. Oncol. 20, 1913-1927
29. Huang, L. and Pardee, A. B. (2000) Suberoylanilide hydroxamic acid as a potential therapeutic agent for human breast cancer treatment Mol. Med. 6, 849-866
30. Xu, W. S., Perez, G., Ngo, L., Gui, C. Y., and Marks, P. A. (2005) Induction of polyploidy by histone deacetylase inhibitor: a pathway for antitumor effects Cancer Res. 65, 7832-7839
31. Dai, Y., Rahmani, M., Dent, P., and Grant, S. (2005) Blockade of histone deacetylase inhibitor-induced RelA/p65 acetylation and NF-kappaB activation potentiates apoptosis in leukemia cells through a process mediated by oxidative damage, XIAP downregulation, and c-Jun N-terminal kinase 1 activation Mol. Cell. Biol. 25, 5429-5444
32. Portanova, P., Russo, T., Pellerito, O., Calvaruso, G., Giuliano, M., Vento, R., and Tesoriere, G. (2008) The role of oxidative stress in apoptosis induced by the histone deacetylase inhibitor suberoylanilide hydroxamic acid in human colon adenocarcinoma HT-29 cells Int. J. Oncol. 33, 325-331
33. Li, J., Liu, R., Lei, Y., Wang, K., Lau, Q. C., Xie, N., Zhou, S., Nie, C., Chen, L., Wei, Y., and Huang, C. (2010) Proteomic analysis revealed association of aberrant ROS signaling with suberoylanilide hydroxamic acid-induced autophagy in Jurkat T-leukemia cells Autophagy 6, 711-724
34. Yamamoto, A., Tagawa, Y., Yoshimori, T., Moriyama, Y., Masaki, R., and Tashiro, Y. (1998) Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells Cell Struct. Funct. 23, 33-42
35. Liu, Y. L., Yang, P. M., Shun, C. T., Wu, M. S., Weng, J. R., and Chen, C. C. (2010) Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma Autophagy 6, 1057-1065
36. Gammoh, N., Lam, D., Puente, C., Ganley, I., Marks, P. A., and Jiang, X. (2010) Role of autophagy in histone deacetylase inhibitor-induced apoptotic and nonapoptotic cell death Proc. Natl. Acad. Sci. U.S.A. 109, 6561-6565
37. Ueda, T., Takai, N., Nishida, M., Nasu, K., and Narahara, H. (2007) Apicidin, a novel histone deacetylase inhibitor, has profound anti-growth activity in human endometrial and ovarian cancer cells Int. J. Mol. Med. 19, 301-308
38. Ahn, M. Y., Jung, J. H., Na, Y. J., and Kim, H. S. (2008) A natural histone deacetylase inhibitor, Psammaplin A, induces cell cycle arrest and apoptosis in human endometrial cancer cells Gynecol. Oncol. 108, 27-33
39. Noh, E. J., Lim, D. S., Jeong, G., and Lee, J. S. (2009) An HDAC inhibitor, trichostatin A, induces a delay at G2/M transition, slippage of spindle checkpoint, and cell death in a transcription-dependent manner Biochem. Biophys. Res. Commun. 378, 326-331
40. Knutson, A. K., Welsh, J., Taylor, T., Roy, S., Wang, W. L., and Tenniswood, M. (2012) Comparative effects of histone deacetylase inhibitors on p53 target gene expression, cell cycle and apoptosis in MCF-7 breast cancer cells Oncol. Rep. 27, 849-853
41. Andreyev, A. Y., Kushnareva, Y. E., and Starkov, A. A. (2005) Mitochondrial metabolism of reactive oxygen species Biochemistry (Moscow) 70, 200-214
42. Abramov, A. Y., Scorziello, A., and Duchen, M. R. (2007) Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation J. Neurosci. 27, 1129-1138
43. Rogalska, A., Koceva-Chyła, A., and Jóźwiak, Z. (2008) Aclarubicin-induced ROS generation and collapse of mitochondrial membrane potential in human cancer cell lines Chem.-Biol. Interact. 176, 58-70
44. Chen, Y., Zheng, Y., and Foster, D. A. (2003) Phospholipase D confers rapamycin resistance in human breast cancer cells Oncogene 22, 3937-3942
45. Apel, A., Herr, I., Schwarz, H., Rodemann, H. P., and Mayer, A. (2008) Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy Cancer Res. 68, 1485-1494
46. Choi, C. H., Jung, Y. K., and Oh, S. H. (2010) Autophagy induction by capsaicin in malignant human breast cells is modulated by p38 and extracellular signal-regulated mitogen-activated protein kinases and retards cell death by suppressing endoplasmic reticulum stress-mediated apoptosis Mol. Pharmacol. 78, 114-125
47. Kanematsu, S., Uehara, N., Miki, H., Yoshizawa, K., Kawanaka, A., Yuri, T., and Tsubura, A. (2010) Autophagy inhibition enhances sulforaphane-induced apoptosis in human breast cancer cells Anticancer Res. 30, 3381-3390
48. Moreau, K., Ravikumar, B., Puri, C., and Rubinsztein, D. C. (2012) Arf6 promotes autophagosome formation via effects on phosphatidylinositol 4,5-bisphosphate and phospholipase D J. Cell Biol. 196, 483-496
49. Okamoto, K. (2011) Mitochondria breathe for autophagy EMBO J. 30, 2095-2096
50. Kathiria, A. S., Butcher, L. D., Feagins, L. A., Souza, R. F., Boland, C. R., and Theiss, A. L. (2012) Prohibitin 1 modulates mitochondrial stress-related autophagy in human colonic epithelial cells PLoS One 7 (2) e31231 10.1371/journal.pone.0031231
51. Karantza-Wadsworth, V., Patel, S., Kravchuk, O., Chen, G., Mathew, R., Jin, S., and White, E. (2007) Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis Genes Dev. 21, 1621-1635
52. Rao, R., Balusu, R., Fiskus, W., Mudunuru, U., Venkannagari, S., Chauhan, L., Smith, J. E., Hembruff, S. L., Ha, K., Atadja, P., and Bhalla, K. N. (2012) Combination of pan-histone deacetylase inhibitor and autophagy inhibitor exerts superior efficacy against triple-negative human breast cancer cells Mol. Cancer Ther. 11, 973-983
53. Osella, D., Homa Mahboobi, H., Colangelo, D., Cavigiolio, G., Vessieres, A., and Jaouen, G. (2005) FACS analysis of oxidative stress induced on tumour cells by SERMs Inorg. Chim. Acta 358, 1993-1998
54. Spencer, J., Amin, J., Boddiboyena, R., Packham, G., Cavell, B. E., Syed Alwi, S. S., Paranal, R. M., Heightman, T. D., Wang, M., Marsden, B., Coxhead, P., Guille, M., Tizzard, G. J., Coles, S. J., and Bradner, J. E. (2012) Click JAHAs: Conformationally restricted ferrocene-based histone deacetylase inhibitors Med. Chem. Commun. 3, 61-64