Trend of Histone Deacetylase Inhibitors in Cancer Therapy: Isoform Selectivity or Multitargeted Strategy

Medicinal Research Reviews

Volumn 35, Issue 1, 2015, Pages 63-84

  Zhang, Lei ^a   Han, Yantao ^a   Jiang, Qixiao ^a   Wang, Chunbo ^a   Chen, Xuehong ^a   Li, Xiaoguang ^b   Xu, Fuming ^b   Jiang, Yuqi ^b   Wang, Qiang ^c   Xu, Wenfang ^b  

^a QINGDAO UNIVERSITY   (China)

^b SHANDONG UNIVERSITY   (China)

^c SOUTH CENTRAL UNIVERSITY FOR NATIONALITIES   (China)

Author keywords

Bifunctional molecule; Histone deacetylase; Inhibitors; Multitargeted; Selectivity

Indexed keywords

ANTINEOPLASTIC AGENT; HISTONE DEACETYLASE INHIBITOR; ISOPROTEIN;

DRUG EFFECTS; HUMAN; NEOPLASMS;

ANTINEOPLASTIC AGENTS; HISTONE DEACETYLASE INHIBITORS; HUMANS; NEOPLASMS; PROTEIN ISOFORMS;

EID: 84914815183     PISSN: 01986325     EISSN: 10981128     Source Type: Journal    
DOI: 10.1002/med.21320     Document Type: Article

References (141)

1. Bernstein BE, Tong JK, Schreiber SL. Genomewide studies of histone deacetylase function in yeast. Proc Natl Acad Sci USA 2000;97(25):13708-13713.
2. De Ruijter AJM, Van Gennip AH, Caron HN, Kemp S, Van Kuilenburg ABP. Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochem J 2003;370:737-749.
3. Foglietti C, Filocamo G, Cundari E, De Rinaldis E, Lahm A, Cortese R, Steinkuhler C. Dissecting the biological functions of Drosophila histone deacetylases by RNA interference and transcriptional profiling. J Biol Chem 2006;281(26):17968-17976.
4. North BJ, Verdin E. Sirtuins: Sir2-related NAD-dependent protein deacetylases. Genome Biol 2004;5(5):224.
5. Gronroos E, Hellman U, Heldin CH, Ericsson J. Control of Smad7 stability by competition between acetylation and ubiquitination. Mol Cell 2002;10(3):483-493.
6. Giandomenico V, Simonsson M, Gronroos E, Ericsson J. Coactivator-dependent acetylation stabilizes members of the SREBP family of transcription factors. Mol Cell Biol 2003;23(7):2587-2599.
7. Jin YH, Jeon EJ, Li QL, Lee YH, Choi JK, Kim WJ, Lee KY, Bae SC. Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. J Biol Chem 2004;279(28):29409-29417.
8. Ververis K, Hiong A, Karagiannis TC, Licciardi PV. Histone deacetylase inhibitors (HDACIs): Multitargeted anticancer agents. Biologics Tar Ther 2013;7:47-60.
9. Polo SE, Almouzni G. Histone metabolic pathways and chromatin assembly factors as proliferation markers. Cancer Lett 2005;220(1):1-9.
10. Pruitt K, Zinn RL, Ohm JE, McGarvey KM, Kang SH, Watkins DN, Herman JG, Baylin SB. Inhibition of SIRT1 reactivates silenced cancer genes without loss of promoter DNA hypermethylation. PLoS Genet 2006;2(3):e40.
11. Bode AM, Dong ZG. Post-translational modification of p53 in tumorigenesis. Nat Rev Cancer 2004;4(10):793-805.
12. Chen LF, Greene WC. Shaping the nuclear action of NF-kappa B. Nat Rev Mol Cell Bio 2004;5(5):392-401.
13. Kovacs JJ, Murphy PJM, Gaillard S, Zhao XA, Wu JT, Nicchitta CV, Yoshida M, Toft DO, Pratt WB, Yao TP. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 2005;18(5):601-607.
14. Soragni E, Xu C, Cooper A, Plasterer HL, Rusche JR, Gottesfeld JM. Evaluation of histone deacetylase inhibitors as therapeutics for neurodegenerative diseases. Methods Mol Biol 2011;793:495-508.
15. Mai A, Rotili D, Valente S, Kazantsev AG. Histone deacetylase inhibitors and neurodegenerative disorders: Holding the promise. Curr Pharm Design 2009;15(34):3940-3957.
16. Roger T, Lugrin J, Le Roy D, Goy G, Mombelli M, Koessler T, Ding XC, Chanson AL, Reymond MK, Miconnet I, Schrenzel J, Francois P, Calandra T. Histone deacetylase inhibitors impair innate immune responses to Toll-like receptor agonists and to infection. Blood 2011;117(4):1205-1217.
17. Valenzuela-Fernandez A, Alvarez S, Gordon-Alonso M, Barrero M, Ursa A, Cabrero JR, Fernandez G, Naranjo-Suarez S, Yanez-Mo M, Serrador JM, Munoz-Fernandez MA, Sanchez-Madrid F. Histone deacetylase 6 regulates human immunodeficiency virus type 1 infection. Mol Biol Cell 2005;16(11):5445-5454.
18. Saiyed ZM, Gandhi N, Agudelo M, Napuri J, Samikkannu T, Reddy PV, Khatavkar P, Yndart A, Saxena SK, Nair MP. HIV-1 Tat upregulates expression of histone deacetylase-2 (HDAC2) in human neurons: Implication for HIV-associated neurocognitive disorder (HAND). Neurochem Int 2011;58(6):656-664.
19. Margolis DM. Histone deacetylase inhibitors and HIV latency. Curr Opin HIV AIDS 2011;6(1):25-29.
20. Ylisastigui L, Archin NM, Lehrman G, Bosch RJ, Margolis DM. Coaxing HIV-1 from resting CD4 T cells: Histone deacetylase inhibition allows latent viral expression. Aids 2004;18(8):1101-1108.
21. Gallo P, Latronico MV, Gallo P, Grimaldi S, Borgia F, Todaro M, Jones P, Gallinari P, De Francesco R, Ciliberto G, Steinkuhler C, Esposito G, Condorelli G. Inhibition of class I histone deacetylase with an apicidin derivative prevents cardiac hypertrophy and failure. Cardiovasc Res 2008;80(3):416-424.
22. Kook H, Lepore JJ, Gitler AD, Lu MM, Wing-Man Yung W, Mackay J, Zhou R, Ferrari V, Gruber P, Epstein JA. Cardiac hypertrophy and histone deacetylase-dependent transcriptional repression mediated by the atypical homeodomain protein Hop. J Clin Invest 2003;112(6):863-871.
23. Marks PA, Rifkind RA, Richon VM, Breslow R, Miller T, Kelly WK. Histone deacetylases and cancer: Causes and therapies. Nat Rev Cancer 2001;1(3):194-202.
24. Gu W, Roeder RG. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 1997;90(4):595-606.
25. Ito A, Kawaguchi Y, Lai CH, Kovacs JJ, Higashimoto Y, Appella E, Yao TP. MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J 2002;21(22):6236-6245.
26. Luo J, Li M, Tang Y, Laszkowska M, Roeder RG, Gu W. Acetylation of p53 augments its site-specific DNA binding both in vitro and in vivo. Proc Natl Acad Sci USA 2004;101(8):2259-2264.
27. Thevenet L, Mejean C, Moniot B, Bonneaud N, Galeotti N, Aldrian-Herrada G, Poulat F, Berta P, Benkirane M, Boizet-Bonhoure B. Regulation of human SRY subcellular distribution by its acetylation/deacetylation. EMBO J 2004;23(16):3336-3345.
28. Yuan ZL, Guan YJ, Chatterjee D, Chin YE. Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 2005;307(5707):269-273.
29. Wang R, Cherukuri P, Luo J. Activation of Stat3 sequence-specific DNA binding and transcription by p300/CREB-binding protein-mediated acetylation. J Biol Chem 2005;280(12):11528-11534.
30. Boyes J, Byfield P, Nakatani Y, Ogryzko V. Regulation of activity of the transcription factor GATA-1 by acetylation. Nature 1998;396(6711):594-598.
31. Hayakawa F, Towatari M, Ozawa Y, Tomita A, Privalsky ML, Saito H. Functional regulation of GATA-2 by acetylation. J Leukocyte Biol 2004;75(3):529-540.
32. Martinez-Balbas MA, Bauer UM, Nielsen SJ, Brehm A, Kouzarides T. Regulation of E2F1 activity by acetylation. EMBO J 2000;19(4):662-671.
33. Marzio G, Wagener C, Gutierrez MI, Cartwright P, Helin K, Giacca M. E2F family members are differentially regulated by reversible acetylation. J Biol Chem 2000;275(15):10887-10892.
34. Sartorelli V, Puri PL, Hamamori Y, Ogryzko V, Chung G, Nakatani Y, Wang JY, Kedes L. Acetylation of MyoD directed by PCAF is necessary for the execution of the muscle program. Mol Cell 1999;4(5):725-734.
35. Yao YL, Yang WM, Seto E. Regulation of transcription factor YY1 by acetylation and deacetylation. Mol Cell Biol 2001;21(17):5979-5991.
36. Munshi N, Merika M, Yie J, Senger K, Chen G, Thanos D. Acetylation of HMG I(Y) by CBP turns off IFN beta expression by disrupting the enhanceosome. Mol Cell 1998;2(4):457-467.
37. Munshi N, Agalioti T, Lomvardas S, Merika M, Chen G, Thanos D. Coordination of a transcriptional switch by HMGI(Y) acetylation. Science 2001;293(5532):1133-1136.
38. Luhrs H, Hock R, Schauber J, Weihrauch M, Harrer M, Melcher R, Scheppach W, Bustin M, Menzel T. Modulation of HMG-N2 binding to chromatin by butyrate-induced acetylation in human colon adenocarcinoma cells. Int J Cancer 2002;97(5):567-573.
39. Kiernan R, Bres V, Ng RW, Coudart MP, El Messaoudi S, Sardet C, Jin DY, Emiliani S, Benkirane M. Post-activation turn-off of NF-kappa B-dependent transcription is regulated by acetylation of p65. J Biol Chem 2003;278(4):2758-2766.
40. Fu M, Wang C, Reutens AT, Wang J, Angeletti RH, Siconolfi-Baez L, Ogryzko V, Avantaggiati ML, Pestell RG. p300 and p300/cAMP-response element-binding protein-associated factor acetylate the androgen receptor at sites governing hormone-dependent transactivation. J Biol Chem 2000;275(27):20853-20860.
41. Gaughan L, Logan IR, Cook S, Neal DE, Robson CN. Tip60 and histone deacetylase 1 regulate androgen receptor activity through changes to the acetylation status of the receptor. J Biol Chem 2002;277(29):25904-25913.
42. Gaughan L, Logan IR, Neal DE, Robson CN. Regulation of androgen receptor and histone deacetylase 1 by Mdm2-mediated ubiquitylation. Nucleic Acids Res 2005;33(1):13-26.
43. Fu M, Wang C, Wang J, Zhang X, Sakamaki T, Yeung YG, Chang C, Hopp T, Fuqua SA, Jaffray E, Hay RT, Palvimo JJ, Janne OA, Pestell RG. Androgen receptor acetylation governs trans activation and MEKK1-induced apoptosis without affecting in vitro sumoylation and trans-repression function. Mol Cell Biol 2002;22(10):3373-3388.
44. Wang C, Fu M, Angeletti RH, Siconolfi-Baez L, Reutens AT, Albanese C, Lisanti MP, Katzenellenbogen BS, Kato S, Hopp T, Fuqua SA, Lopez GN, Kushner PJ, Pestell RG. Direct acetylation of the estrogen receptor alpha hinge region by p300 regulates transactivation and hormone sensitivity. J Biol Chem 2001;276(21):18375-18383.
45. Kawai H, Li H, Avraham S, Jiang S, Avraham HK. Overexpression of histone deacetylase HDAC1 modulates breast cancer progression by negative regulation of estrogen receptor alpha. Int J Cancer 2003;107(3):353-358.
46. Yamagata T, Mitani K, Oda H, Suzuki T, Honda H, Asai T, Maki K, Nakamoto T, Hirai H. Acetylation of GATA-3 affects T-cell survival and homing to secondary lymphoid organs. EMBO J 2000;19(17):4676-4687.
47. Zhang W, Bieker JJ. Acetylation and modulation of erythroid Kruppel-like factor (EKLF) activity by interaction with histone acetyltransferases. Proc Natl Acad Sci USA 1998;95(17):9855-9860.
48. Jin YH, Jeon EJ, Li QL, Lee YH, Choi JK, Kim WJ, Lee KY, Bae SC. Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. J Biol Chem 2004;279(28):29409-29417.
49. Jeong JW, Bae MK, Ahn MY, Kim SH, Sohn TK, Bae MH, Yoo MA, Song EJ, Lee KJ, Kim KW. Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation. Cell 2002;111(5):709-720.
50. Patel JH, Du Y, Ard PG, Phillips C, Carella B, Chen CJ, Rakowski C, Chatterjee C, Lieberman PM, Lane WS, Blobel GA, McMahon SB. The c-MYC oncoprotein is a substrate of the acetyltransferases hGCN5/PCAF and TIP60. Mol Cell Biol 2004;24(24):10826-10834.
51. Gronroos E, Hellman U, Heldin CH, Ericsson J. Control of Smad7 stability by competition between acetylation and ubiquitination. Mol Cell 2002;10(3):483-493.
52. Zhang W, Kadam S, Emerson BM, Bieker JJ. Site-specific acetylation by p300 or CREB binding protein regulates erythroid Kruppel-like factor transcriptional activity via its interaction with the SWI-SNF complex. Mol Cell Biol 2001;21(7):2413-2422.
53. Bannister AJ, Miska EA, Gorlich D, Kouzarides T. Acetylation of importin-alpha nuclear import factors by CBP/p300. Curr Biol 2000;10(8):467-470.
54. Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 2001;293(5535):1653-1657.
55. Cohen HY, Lavu S, Bitterman KJ, Hekking B, Imahiyerobo TA, Miller C, Frye R, Ploegh H, Kessler BM, Sinclair DA. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol Cell 2004;13(5):627-638.
56. Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT, Nicchitta CV, Yoshida M, Toft DO, Pratt WB, Yao TP. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 2005;18(5):601-607.
57. Thiagalingam SAM, Cheng K-H, Lee HJ, Mineva N, Thiagalingam A, Ponte JF. Histone deacetylases: Unique players in shaping the epigenetic histone code. Ann NY Acad Sci 2003;983(1):84-100.
58. Marks PA, Richon VM, Rifkind RA. Histone deacetylase inhibitors: Inducers of differentiation or apoptosis of transformed cells. J Nat Cancer Inst 2000;92(15):1210-1216.
59. Richon VM, Emiliani S, Verdin E, Webb Y, Breslow R, Rifkind RA, Marks PA. A class of hybrid polar inducers of transformed cell differentiation inhibits histone deacetylases. Proc Natl Acad Sci USA 1998;95(6):3003-3007.
60. Ueda H, Nakajima H, Hori Y, Fujita T, Nishimura M, Goto T, Okuhara M. Fr901228, a novel antitumor bicyclic depsipeptide produced by chromobacterium-violaceum No-968. 1. Taxonomy, fermentation, isolation, physicochemical and biological properties, and antitumor-activity. J Antibiot 1994;47(3):301-310.
61. Saito A, Yamashita T, Mariko Y, Nosaka Y, Tsuchiya K, Ando T, Suzuki T, Tsuruo T, Nakanishi O. A synthetic inhibitor of histone deacetylase, MS-27-275, with marked in vivo antitumor activity against human tumors. Proc Natl Acad Sci USA 1999;96(8):4592-4597.
62. Furumai R, Matsuyama A, Kobashi N, Lee KH, Nishiyama M, Nakajima H, Tanaka A, Komatsu Y, Nishino N, Yoshida M, Horinouchi S. FK228 (depsipeptide) as a natural prodrug that inhibits class I histone deacetylases. Cancer Res 2002;62(17):4916-4921.
63. Furumai R, Komatsu Y, Nishino N, Khochbin S, Yoshida M, Horinouchi S. Potent histone deacetylase inhibitors built from trichostatin A and cyclic tetrapeptide antibiotics including trapoxin. Proc Natl Acad Sci USA 2001;98(1):87-92.
64. Yurek-George A, Cecil AR, Mo AH, Wen S, Rogers H, Habens F, Maeda S, Yoshida M, Packham G, Ganesan A. The first biologically active synthetic analogues of FK228, the depsipeptide histone deacetylase inhibitor. J Med Chem 2007;50(23):5720-5726.
65. Wong JC, Hong R, Schreiber SL. Structural biasing elements for in-cell histone deacetylase paralog selectivity. J Am Chem Soc 2003;125(19):5586-5587.
66. Beckers T, Burkhardt C, Wieland H, Gimmnich P, Ciossek T, Maier T, Sanders K. Distinct pharmacological properties of second generation HDAC inhibitors with the benzamide or hydroxamate head group. Int J Cancer 2007;121(5):1138-1148.
67. Hu E, Dul E, Sung CM, Chen Z, Kirkpatrick R, Zhang GF, Johanson K, Liu R, Lago A, Hofmann G, Macarron R, de los Frailes M, Perez P, Krawiec J, Winkler J, Jaye M. Identification of novel isoform-selective inhibitors within class I histone deacetylases. J Pharm Exp Ther 2003;307(2):720-728.
68. Moffat D, Patel S, Day F, Belfield A, Donald A, Rowlands M, Wibawa J, Brotherton D, Stimson L, Clark V, Owen J, Bawden L, Box G, Bone E, Mortenson P, Hardcastle A, van Meurs S, Eccles S, Raynaud F, Aherne W. Discovery of 2-(6-{[(6-fluoroquinolin-2-yl)methyl]amino}bicyclo[3.1.0]hex-3-yl)-N-hydroxypyrim idine-5-carboxamide (CHR-3996), a class I selective orally active histone deacetylase inhibitor. J Med Chem 2010;53(24):8663-8678.
69. Krennhrubec K, Marshall BL, Hedglin M, Verdin E, Ulrich SM. Design and evaluation of "Linkerless" hydroxamic acids as selective HDAC8 inhibitors. Bioorg Med Chem Lett 2007;17(10):2874-2878.
70. Balasubramanian S, Ramos J, Luo W, Sirisawad M, Verner E, Buggy JJ. A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas. Leukemia 2008;22(5):1026-1034.
71. Suzuki T, Ota Y, Ri M, Bando M, Gotoh A, Itoh Y, Tsumoto H, Tatum PR, Mizukami T, Nakagawa H, Iida S, Ueda R, Shirahige K, Miyata N. Rapid discovery of highly potent and selective inhibitors of histone deacetylase 8 using click chemistry to generate candidate libraries. J Med Chem 2012;55(22):9562-9575.
72. Ononye SN, VanHeyst MD, Oblak EZ, Zhou W, Ammar M, Anderson AC, Wright DL. Tropolones as lead-like natural products: The development of potent and selective histone deacetylase inhibitors. ACS Med Chem Lett 2013;4(8):757-761.
73. Suzuki T, Kasuya Y, Itoh Y, Ota Y, Zhan P, Asamitsu K, Nakagawa H, Okamoto T, Miyata N. Identification of highly selective and potent histone deacetylase 3 inhibitors using click chemistry-based combinatorial fragment assembly. PloS One 2013;8(7):e68669.
74. Haggarty SJ, Koeller KM, Wong JC, Butcher RA, Schreiber SL. Multidimensional chemical genetic analysis of diversity-oriented synthesis-derived deacetylase inhibitors using cell-based assays. Chem Biol 2003;10(5):383-396.
75. Estiu G, Greenberg E, Harrison CB, Kwiatkowski NP, Mazitschek R, Bradner JE, Wiest O. Structural origin of selectivity in class II-selective histone deacetylase inhibitors. J Med Chem 2008;51(10):2898-2906.
76. Butler KV, Kalin J, Brochier C, Vistoli G, Langley B, Kozikowski AP. Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J Am Chem Soc 2010;132(31):10842-10846.
77. Bergman JA, Woan K, Perez-Villarroel P, Villagra A, Sotomayor EM, Kozikowski AP. Selective histone deacetylase 6 inhibitors bearing substituted urea linkers inhibit melanoma cell growth. J Med Chem 2012;55(22):9891-9899.
78. Yu CW, Chang PT, Hsin LW, Chern JW. Quinazolin-4-one derivatives as selective histone deacetylase-6 inhibitors for the treatment of Alzheimer's disease. J Med Chem 2013;56(17):6775-6791.
79. Olson DE, Wagner FF, Kaya T, Gale JP, Aidoud N, Davoine EL, Lazzaro F, Weiwer M, Zhang YL, Holson EB. Discovery of the first histone deacetylase 6/8 dual inhibitors. J Med Chem 2013;56(11):4816-4820.
80. DeVita VT, Jr., Chu E. A history of cancer chemotherapy. Cancer Res 2008;68(21):8643-8653.
81. Chabner BA, Roberts TG, Jr. Timeline: Chemotherapy and the war on cancer. Nat Rev Cancer 2005;5(1):65-72.
82. Bieler A, Mantwill K, Dravits T, Bernshausen A, Glockzin G, Kohler-Vargas N, Lage H, Gansbacher B, Holm PS. Novel three-pronged strategy to enhance cancer cell killing in glioblastoma cell lines: Histone deacetylase inhibitor, chemotherapy, and oncolytic adenovirus dl520. Hum Gene Ther 2006;17(1):55-70.
83. Lopez G, Liu J, Ren W, Wei W, Wang S, Lahat G, Zhu QS, Bornmann WG, McConkey DJ, Pollock RE, Lev DC. Combining PCI-24781, a novel histone deacetylase inhibitor, with chemotherapy for the treatment of soft tissue sarcoma. Clin Cancer Res 2009;15(10):3472-3483.
84. Sampson ER, Amin V, Schwarz EM, O'Keefe RJ, Rosier RN. The histone deacetylase inhibitor vorinostat selectively sensitizes fibrosarcoma cells to chemotherapy. J Orthop Res 2011;29(4):623-632.
85. Sanchez E, Shen J, Steinberg J, Li M, Wang C, Bonavida B, Chen H, Li ZW, Berenson JR. The histone deacetylase inhibitor LBH589 enhances the anti-myeloma effects of chemotherapy in vitro and in vivo. Leukemia Res 2011;35(3):373-379.
86. Yang C, Choy E, Hornicek FJ, Wood KB, Schwab JH, Liu X, Mankin H, Duan Z. Histone deacetylase inhibitor PCI-24781 enhances chemotherapy-induced apoptosis in multidrug-resistant sarcoma cell lines. Anticancer Res 2011;31(4):1115-1123.
87. Brabec V, Kasparkova J. Molecular aspects of resistance to antitumor platinum drugs. Drug Resist Update 2002;5(3-4):147-161.
88. Desoize B, Madoulet C. Particular aspects of platinum compounds used at present in cancer treatment. Crit Rev Oncol Hematol 2002;42(3):317-325.
89. Kasparkova J, Novakova O, Vrana O, Intini F, Natile G, Brabec V. Molecular aspects of antitumor effects of a new platinum(IV) drug. Mol Pharm 2006;70(5):1708-1719.
90. Griffith D, Morgan MP, Marmion CJ. A novel anti-cancer bifunctional platinum drug candidate with dual DNA binding and histone deacetylase inhibitory activity. Chem Commun 2009;(44):6735-6737.
91. Griffith DM, Duff B, Suponitsky KY, Kavanagh K, Morgan MP, Egan D, Marmion CJ. Novel trans-platinum complexes of the histone deacetylase inhibitor valproic acid; synthesis, in vitro cytotoxicity and mutagenicity. J Inorg Biochem 2011;105(6):793-799.
92. Yang J, Sun X, Mao W, Sui M, Tang J, Shen Y. Conjugate of Pt(IV)-histone deacetylase inhibitor as a prodrug for cancer chemotherapy. Mol Pharm 2012;9(10):2793-2800.
93. Hedstrom L. IMP dehydrogenase: Structure, mechanism, and inhibition. Chem Rev 2009;109(7):2903-2928.
94. Bairagya HR, Mukhopadhyay BP, Sekar K. An insight to the dynamics of conserved water molecular triad in IMPDH II (human): Recognition of cofactor and substrate to catalytic Arg 322. J Biomol Struct Dynam 2009;27(2):149-158.
95. He Y, Mou Z, Li W, Liu B, Fu T, Zhao S, Xiang D, Wu Y. Identification of IMPDH2 as a tumor-associated antigen in colorectal cancer using immunoproteomics analysis. Int J Colorectal Dis 2009;24(11):1271-1279.
96. Jayaram HN, Cooney DA, Grusch M, Krupitza G. Consequences of IMP dehydrogenase inhibition, and its relationship to cancer and apoptosis. Curr Med Chem 1999;6(7):561-574.
97. Birkinshaw JH, Raistrick H, Ross DJ. Studies in the biochemistry of micro-organisms. 86. The molecular constitution of mycophenolic acid, a metabolic product of Penicillium Brevi-compactum Dierckx. Part III. Further observations on the structural formula for mycophenolic acid. Biochem J 1952;50(5):630-634.
98. Floryk D, Huberman E. Mycophenolic acid-induced replication arrest, differentiation markers and cell death of androgen-independent prostate cancer cells DU145. Cancer Lett 2006;231(1):20-29.
99. Floryk D, Tollaksen SL, Giometti CS, Huberman E. Differentiation of human prostate cancer PC-3 cells induced by inhibitors of inosine 5'-monophosphate dehydrogenase. Cancer Res 2004;64(24):9049-9056.
100. Chen L, Wilson D, Jayaram HN, Pankiewicz KW. Dual inhibitors of inosine monophosphate dehydrogenase and histone deacetylases for cancer treatment. J Med Chem 2007;50(26):6685-6691.
101. Mitsuhashi S, Takenaka J, Iwamori K, Nakajima N, Ubukata M. Structure-activity relationships for inhibition of inosine monophosphate dehydrogenase and differentiation induction of K562 cells among the mycophenolic acid derivatives. Bioorg Med Chem 2010;18(22):8106-8111.
102. Batovska DI, Kim DH, Mitsuhashi S, Cho YS, Kwon HJ, Ubukata M. Hydroxamic acid derivatives of mycophenolic acid inhibit histone deacetylase at the cellular level. Biosci Biotech Biochem 2008;72(10):2623-2631.
103. Chen L, Petrelli R, Gao G, Wilson DJ, McLean GT, Jayaram HN, Sham YY, Pankiewicz KW. Dual inhibitors of inosine monophosphate dehydrogenase and histone deacetylase based on a cinnamic hydroxamic acid core structure. Bioorg Med Chem 2010;18(16):5950-5964.
104. Robinson DR, Wu YM, Lin SF. The protein tyrosine kinase family of the human genome. Oncogene 2000;19(49):5548-5557.
105. Sangwan V, Park M. Receptor tyrosine kinases: Role in cancer progression. Curr Oncol 2006;13(5):191-193.
106. Takeuchi K, Ito F. Receptor tyrosine kinases and targeted cancer therapeutics. Biol Pharm Bull 2011;34(12):1774-1780.
107. Stegmeier F, Warmuth M, Sellers WR, Dorsch M. Targeted cancer therapies in the twenty-first century: Lessons from imatinib. Clin Pharm Ther 2010;87(5):543-552.
108. Kantarjian H, Giles F, Wunderle L, Bhalla K, O'Brien S, Wassmann B, Tanaka C, Manley P, Rae P, Mietlowski W, Bochinski K, Hochhaus A, Griffin JD, Hoelzer D, Albitar M, Dugan M, Cortes J, Alland L, Ottmann OG. Nilotinib in imatinib-resistant CML and Philadelphia chromosome-positive ALL. New Engl J Med 2006;354(24):2542-2551.
109. Das J, Chen P, Norris D, Padmanabha R, Lin J, Moquin RV, Shen Z, Cook LS, Doweyko AM, Pitt S, Pang S, Shen DR, Fang Q, de Fex HF, McIntyre KW, Shuster DJ, Gillooly KM, Behnia K, Schieven GL, Wityak J, Barrish JC. 2-Aminothiazole as a novel kinase inhibitor template. Structure-activity relationship studies toward the discovery of N-(2-chloro-6-methylphenyl)-2-[[6-[4-(2-hydroxyethyl)-1-piperazinyl)]-2-methyl-4-pyrimidinyl]amino)]-1, 3-thiazole-5-carboxamide (dasatinib, BMS-354825) as a potent pan-Src kinase inhibitor. J Med Chem 2006;49(23):6819-6832.
110. Keating GM, Santoro A. Sorafenib: A review of its use in advanced hepatocellular carcinoma. Drugs 2009;69(2):223-240.
111. Kim MS, Kwon HJ, Lee YM, Baek JH, Jang JE, Lee SW, Moon EJ, Kim HS, Lee SK, Chung HY, Kim CW, Kim KW. Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat Med 2001;7(4):437-443.
112. Deroanne CF, Bonjean K, Servotte S, Devy L, Colige A, Clausse N, Blacher S, Verdin E, Foidart JM, Nusgens BV, Castronovo V. Histone deacetylases inhibitors as anti-angiogenic agents altering vascular endothelial growth factor signaling. Oncogene 2002;21(3):427-436.
113. Rossig L, Li H, Fisslthaler B, Urbich C, Fleming I, Forstermann U, Zeiher AM, Dimmeler S. Inhibitors of histone deacetylation downregulate the expression of endothelial nitric oxide synthase and compromise endothelial cell function in vasorelaxation and angiogenesis. Circ Res 2002;91(9):837-844.
114. Kwon HJ, Kim MS, Kim MJ, Nakajima H, Kim KW. Histone deacetylase inhibitor FK228 inhibits tumor angiogenesis. Int J Cancer 2002;97(3):290-296.
115. Pili R, Kruszewski MP, Hager BW, Lantz J, Carducci MA. Combination of phenylbutyrate and 13-cis retinoic acid inhibits prostate tumor growth and angiogenesis. Cancer Res 2001;61(4):1477-1485.
116. Qian DZ, Kato Y, Shabbeer S, Wei Y, Verheul HM, Salumbides B, Sanni T, Atadja P, Pili R. Targeting tumor angiogenesis with histone deacetylase inhibitors: The hydroxamic acid derivative LBH589. Clin Cancer Res 2006;12(2):634-642.
117. Qian DZ, Wang X, Kachhap SK, Kato Y, Wei Y, Zhang L, Atadja P, Pili R. The histone deacetylase inhibitor NVP-LAQ824 inhibits angiogenesis and has a greater antitumor effect in combination with the vascular endothelial growth factor receptor tyrosine kinase inhibitor PTK787/ZK222584. Cancer Res 2004;64(18):6626-6634.
118. Mahboobi S, Dove S, Sellmer A, Winkler M, Eichhorn E, Pongratz H, Ciossek T, Baer T, Maier T, Beckers T. Design of chimeric histone deacetylase- and tyrosine kinase-inhibitors: A series of imatinib hybrides as potent inhibitors of wild-type and mutant BCR-ABL, PDGF-Rbeta, and histone deacetylases. J Med Chem 2009;52(8):2265-2279.
119. Mahboobi S, Sellmer A, Winkler M, Eichhorn E, Pongratz H, Ciossek T, Baer T, Maier T, Beckers T. Novel chimeric histone deacetylase inhibitors: A series of lapatinib hybrides as potent inhibitors of epidermal growth factor receptor (EGFR), human epidermal growth factor receptor 2 (HER2), and histone deacetylase activity. J Med Chem 2010;53(24):8546-8555.
120. Cai X, Zhai HX, Wang J, Forrester J, Qu H, Yin L, Lai CJ, Bao R, Qian C. Discovery of 7-(4-(3-ethynylphenylamino)-7-methoxyquinazolin-6-yloxy)-N-hydroxyheptanamide (CUDc-101) as a potent multi-acting HDAC, EGFR, and HER2 inhibitor for the treatment of cancer. J Med Chem 2010;53(5):2000-2009.
121. Lai CJ, Bao R, Tao X, Wang J, Atoyan R, Qu H, Wang DG, Yin L, Samson M, Forrester J, Zifcak B, Xu GX, DellaRocca S, Zhai HX, Cai X, Munger WE, Keegan M, Pepicelli CV, Qian C. CUDC-101, a multitargeted inhibitor of histone deacetylase, epidermal growth factor receptor, and human epidermal growth factor receptor 2, exerts potent anticancer activity. Cancer Res 2010;70(9):3647-3656.
122. Wang J, Pursell NW, Samson ME, Atoyan R, Ma AW, Selmi A, Xu W, Cai X, Voi M, Savagner P, Lai CJ. Potential advantages of CUDC-101, a multitargeted HDAC, EGFR, and HER2 inhibitor, in treating drug resistance and preventing cancer cell migration and invasion. Mol Cancer Ther 2013;12(6):925-936.
123. Champoux JJ. DNA topoisomerases: Structure, function, and mechanism. Ann Rev Biochem 2001;70:369-413.
124. Pommier Y, Leo E, Zhang H, Marchand C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol 2010;17(5):421-433.
125. Piccart-Gebhart MJ. Anthracyclines and the tailoring of treatment for early breast cancer. N Engl J Med 2006;354(20):2177-2179.
126. Marchion DC, Bicaku E, Daud AI, Richon V, Sullivan DM, Munster PN. Sequence-specific potentiation of topoisomerase II inhibitors by the histone deacetylase inhibitor suberoylanilide hydroxamic acid. J Cell Biochem 2004;92(2):223-237.
127. Guerrant W, Patil V, Canzoneri JC, Oyelere AK. Dual targeting of histone deacetylase and topoisomerase II with novel bifunctional inhibitors. J Med Chem 2012;55(4):1465-1477.
128. Guo T, Li B, Gu C. Expression of hPEBP4 negatively correlates with estrogen and progesterone receptors in endometrial carcinoma. J BUON 2013;18(2):465-470.
129. Singh M, Zaino RJ, Filiaci VJ, Leslie KK. Relationship of estrogen and progesterone receptors to clinical outcome in metastatic endometrial carcinoma: A Gynecologic Oncology Group Study. Gynecol Oncol 2007;106(2):325-333.
130. Arias-Loza PA, Muehlfelder M, Pelzer T. Estrogen and estrogen receptors in cardiovascular oxidative stress. Pflugers Arch Eur J Phy 2013;465(5):739-746.
131. Otsuki M, Dahlman-Wright K, Gustafsson JA. Cardiovascular roles of estrogen receptors: Insights gained from knockout models. Nucl Recept Signal 2003;1:e003.
132. Zou SE, Zhang SF, Zhang R, Zhang J. Role of the cross-talk between estrogen receptors and peroxisome proliferator-activated receptor gamma in daidzein's prevention and treatment of osteoporosis in ovariectomized rats. Zhonghua Yi Xue Za Zhi 2009;89(42):2972-2975.
133. Carlsten H. Interaction with estrogen receptors as treatment of arthritis and osteoporosis. Adv Exp Med Biol 2007;602:83-92.
134. Hong-Goka BC, Chang FL. Estrogen receptors alpha and beta in choroid plexus epithelial cells in Alzheimer's disease. Neurosci Lett 2004;360(3):113-116.
135. Duffy MJ. Estrogen receptors: Role in breast cancer. Crit Rev Clin Lab Sci 2006;43(4):325-347.
136. Jordan VC. Tamoxifen (ICI46, 474) as a targeted therapy to treat and prevent breast cancer. Br J Pharmacol 2006;147(Suppl 1):S269-S276.
137. Lippert C, Seeger H, Wallwiener D, Mueck AO. Comparison of the effects of 17alpha-ethinylestradiol and 17beta-estradiol on the proliferation of human breast cancer cells and human umbilical vein endothelial cells. Clin Exp Obstet Gynecol 2002;29(2):87-90.
138. Speirs V, Malone C, Walton DS, Kerin MJ, Atkin SL. Increased expression of estrogen receptor beta mRNA in tamoxifen-resistant breast cancer patients. Cancer Res 1999;59(21):5421-5424.
139. Osborne CK, Fuqua SA. Mechanisms of tamoxifen resistance. Breast Cancer Res Treat 1994;32(1):49-55.
140. Hirokawa Y, Arnold M, Nakajima H, Zalcberg J, Maruta H. Signal therapy of breast cancers by the HDAC inhibitor FK228 that blocks the activation of PAK1 and abrogates the tamoxifen-resistance. Cancer Biol Ther 2005;4(9):956-960.
141. Gryder BE, Rood MK, Johnson KA, Patil V, Raftery ED, Yao LP, Rice M, Azizi B, Doyle DF, Oyelere AK. Histone deacetylase inhibitors equipped with estrogen receptor modulation activity. J Med Chem 2013;56(14):5782-5796.