Approaches to target the genome and its epigenome in cancer

Future Medicinal Chemistry

Volumn 1, Issue 8, 2009, Pages 1481-1495

  Chapman Rothe, Nadine ^b   Brown, Robert ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

4 [N (2 HYDROXYETHYL) N [2 (3 INDOLYL)ETHYL]AMINOMETHYL]CINNAMOHYDROXAMIC ACID; 5 AZA 2' DEOXYCYTIDINE; 6 (1,3 DIOXO 1H,3H BENZO[DE]ISOQUINOLIN 2 YL) N HYDROXYHEXANAMIDE; APICIDIN; ARYLBUTYRIC ACID DERIVATIVE; AZACITIDINE; AZELAIC BISHYDROXAMIC ACID; BACECA; BELINOSTAT; CG 1521; CYCLIC HYDROXAMIC ACID CONTAINING PEPTIDE; HISTONE; HISTONE DEACETYLASE INHIBITOR; MICRORNA; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE; N (2 AMINOPHENYL) 4 [4 (3 PYRIDINYL) 2 PYRIMIDINYLAMINOMETHYL]BENZAMIDE; OXAMFLATIN; PANOBINOSTAT; PIVALOYLOXYMETHYL BUTYRATE; POLYAMIDE; PYROXAMIDE; ROMIDEPSIN; SAVICOL; SK 7041; SK 7068; SUBERIC BISHYDROXAMIC ACID; TRAPOXIN A; TRICHOSTATIN A; TUBACIN; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT; ZINC FINGER PROTEIN;

ACETYLATION; CANCER THERAPY; CELL DIFFERENTIATION; CELL FATE; CLINICAL TRIAL; DNA METHYLATION; EPIGENETICS; EPIGENOME; GENETIC ASSOCIATION; GENOME; HUMAN; IN VITRO STUDY; MEDIATOR RELEASE; METHYLATION; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; T CELL LYMPHOMA; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CHROMATIN; DNA METHYLATION; EPIGENESIS, GENETIC; GENOME; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONES; HUMANS; NEOPLASMS; RNA INTERFERENCE;

EID: 77953460884     PISSN: 17568919     EISSN: None     Source Type: Journal    
DOI: 10.4155/fmc.09.105     Document Type: Review

References (91)

1. Stratton MR, Campbell PJ, Futreal PA. The cancer genome. Nature 458(7239), 719-724 (2009).
2. Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell 128(4), 635-638 (2007).
3. Luger K, Rechsteiner TJ, Flaus AJ, Waye MM, Richmond TJ. Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol. 272(3), 301-311 (1997).
4. Kouzarides T. Chromatin modifications and their function. Cell 128(4), 693-705 (2007).
5. Holliday R, Pugh JE. DNA modification mechanisms and gene activity during development. Science 187(4173), 226-232 (1975).
6. Riggs AD. X inactivation, differentiation, and DNA methylation. Cytogenet. Cell Genet. 14(1), 9-25 (1975).
7. Jorgensen HF, Bird A. MeCP2 and other methyl-CpG binding proteins. Ment. Retard. Dev. Disabil. Res. Rev. 8(2), 87-93 (2002).
8. Ng HH, Zhang Y, Hendrich B et al. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23(1), 58-61 (1999).
9. Bestor TH, Ingram VM. Two DNA methyltransferases from murine erythroleukemia cells: purification, sequence specificity, and mode of interaction with DNA. Proc. Natl Acad. Sci. USA 80(18), 5559-5563 (1983).
10. Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69(6), 915-926 (1992).
11. Bird A, Taggart M, Frommer M, Miller OJ, Macleod D. A fraction of the mouse genome .that is derived from islands of nonmethylated, CpG-rich DNA. Cell 40(1), 91-99 (1985).
12. Shen L, Kondo Y, Ahmed S et al. Drug sensitivity prediction by CpG island methylation profile in the NCI-60 cancer cell line panel. Cancer Res. 67(23), 11335-11343 (2007).
13. Shen L, Ahuja N, Shen Y et al. DNA methylation and environmental exposures in human hepatocellular carcinoma. J. Natl Cancer Inst. 94(10), 755-761 (2002).
14. Bennett MR, Hasty J. A DNA methylationbased switch generates bistable gene expression. Nat. Genet. 39(2), 146-147 (2007).
15. Schoeftner S, Sengupta AK, Kubicek S et al. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 25(13), 3110-3122 (2006).
16. Ullmannova-Benson V, Guan M, Zhou X et al. DLC1 tumor suppressor gene inhibits migration and invasion of multiple myeloma cells through RhoA GTPase pathway. Leukemia 23(2), 383-390 (2009).
17. Jones PA, Baylin SB. The epigenomics of cancer. Cell 128(4), 683-692 (2007).
18. Lyko F, Brown R. DNA methyltransferase inhibitors and the development of epigenetic cancer therapies. J. Natl Cancer Inst. 97(20), 1498-1506 (2005).
19. Santi DV, Norment A, Garrett CE. Covalent bond formation between a DNA-cytosine methyltransferase and DNA containing 5-azacytosine. Proc. Natl Acad. Sci. USA 81(22), 6993-6997 (1984).
20. Baylin SB. DNA methylation and gene silencing in cancer. Nat. Clin. Pract. Oncol. 2(Suppl. 1), S4-S11 (2005).
21. Bachman KE, Park BH, Rhee I et al. Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell 3(1), 89-95 (2003).
22. Yoo CB, Jeong S, Egger G et al. Delivery of 5-aza-2́-deoxycytidine to cells using oligodeoxynucleotides. Cancer Res. 67(13), 6400-6408 (2007).
23. Brueckner B, Kuck D, Lyko F. DNA methyltransferase inhibitors for cancer therapy. Cancer J. 13(1), 17-22 (2007).
24. Plummer R, Vidal L, Griffin M et al. Phase I study of MG98, an oligonucleotide antisense inhibitor of human DNA methyltransferase 1, given as a 7-day infusion in patients with advanced solid tumors. Clin. Cancer Res. 15(9), 3177-3183 (2009).
25. Klisovic RB, Stock W, Cataland S et al. A Phase I biological study of MG98, an oligodeoxynucleotide antisense to DNA methyltransferase 1, in patients with high-risk myelodysplasia and acute myeloid leukemia. Clin. Cancer Res. 14(8), 2444-2449 (2008).
26. Graham JS, Kaye SB, Brown R. The promises and pitfalls of epigenetic therapies in solid tumors. Eur. J. Cancer 45(7), 1129-1136 (2009).
27. Schwartsmann G, Schunemann H, Gorini CN et al. A Phase I trial of cisplatin plus decitabine, a new DNA-hypomethylating agent, in patients with advanced solid tumors and a follow-up early Phase II evaluation in patients with inoperable non-small cell lung cancer. Invest. New Drugs 18(1), 83-91 (2000).
28. Appleton K, Mackay HJ, Judson I et al. Phase I and pharmacodynamic trial of the DNA methyltransferase inhibitor decitabine and carboplatin in solid tumors. J. Clin. Oncol. 25(29), 4603-4609 (2007).
29. Unoki M, Kelly JD, Neal DE, Ponder BA, Nakamura Y, Hamamoto R. UHRF1 is a novel molecular marker for diagnosis and the prognosis of bladder cancer. Br. J. Cancer 101(1), 98-105 (2009).
30. Unoki M, Brunet J, Mousli M. Drug discovery targeting epigenetic codes: the great potential of UHRF1, which links DNA methylation and histone modifications, as a drug target in cancers and toxoplasmosis. Biochem. Pharmacol. 78(10), 1279-1288 (2009).
31. Martin V, Jørgensen HF, Chaubert AS et al. MBD2-mediated transcriptional repression of the p14ARF tumor suppressor gene in human colon cancer cells. Pathobiology 75(5), 281-287 (2008).
32. Campbell PM, Bovenzi V, Szyf M. Methylated DNA-binding protein 2 antisense inhibitors suppress tumorigenesis of human cancer cell lines in vitro and in vivo. Carcinogenesis 25(4), 499-507 (2004).
33. Phesse TJ, Parry L, Reed KR et al. Deficiency of Mbd2 attenuates Wnt signaling. Mol. Cell Biol. 28(19), 6094-6103 (2008).
34. Komatsu S, Imoto I, Tsuda H et al. Overexpression of SMYD2 relates to tumor cell proliferation and malignant outcome of esophageal squamous cell carcinoma. Carcinogenesis 30(7), 1139-1146 (2009).
35. Kassambara A, Klein B, Moreaux J. MMSET is overexpressed in cancers: link with tumor aggressiveness. Biochem. Biophys. Res. Commun. 379(4), 840-845 (2009).
36. Xiang Y, Zhu Z, Han G et al. JARID1B is a histone H3 lysine 4 demethylase up-regulated in prostate cancer. Proc. Natl Acad. Sci. USA 104(49), 19226-19231 (2007).
37. Simon JA, Lange CA. Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat. Res. 647(1-2), 21-29 (2008).
38. Kondo Y, Shen L, Cheng AS et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat. Genet. 40(6), 741-750 (2008).
39. Tan J, Yang X, Zhuang L et al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev. 21(9), 1050-1063 (2007).
40. Miranda TB, Cortez CC, Yoo CB et al. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol. Cancer Ther. 8(6), 1579-1588 (2009).
41. Kubicek S, O'Sullivan RJ, August EM et al. Reversal of H3K9me2 by a small-molecule inhibitor for the G9a histone methyltransferase. Mol. Cell 25(3), 473-481 (2007).
42. Chang Y, Zhang X, Horton JR et al. Structural basis for G9a-like protein lysine methyltransferase inhibition by BIX-01294. Nat. Struct. Mol. Biol. 16(3), 312-317 (2009).
43. Greiner D, Bonaldi T, Eskeland R, Roemer E, Imhof A. Identification of a specific inhibitor of the histone methyltransferase SU(VAR)3-9. Nat. Chem. Biol. 1(3), 143-145 (2005).
44. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov. 5(9), 769-784 (2006).
45. Bandyopadhyay D, Mishra A, Medrano EE. Overexpression of histone deacetylase 1 confers resistance to sodium butyratemediated apoptosis in melanoma cells through a p53-mediated pathway. Cancer Res. 64(21), 7706-7710 (2004).
46. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 26(37), 5541-5552 (2007).
47. Warrener R, Beamish H, Burgess A et al. Tumor cell-selective cytotoxicity by targeting cell cycle checkpoints. FASEB J. 17(11), 1550-1552 (2003).
48. Gui CY, Ngo L, Xu WS, Richon VM, Marks PA. Histone deacetylase (HDAC) inhibitor activation of p21WAF1 involves changes in promoter-associated proteins, including HDAC1. Proc. Natl Acad. Sci. USA 101(5), 1241-1246 (2004).
49. Bi G, Jiang G. The molecular mechanism of HDAC inhibitors in anticancer effects. Cell Mol. Immunol. 3(4), 285-290 (2006).
50. Nusinzon I, Horvath CM. Interferonstimulated transcription and innate antiviral immunity require deacetylase activity and histone deacetylase 1. Proc. Natl Acad. Sci. USA 100(25), 14742-14747 (2003).
51. Yuan ZL, Guan YJ, Chatterjee D, Chin YE. Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 307(5707), 269-273 (2005).
52. Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NF-kB action regulated by reversible acetylation. Science 293(5535), 1653-1657 (2001).
53. Gu W, Roeder RG. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90(4), 595-606 (1997).
54. Martinez-Balbas MA, Bauer UM, Nielsen SJ, Brehm A, Kouzarides T. Regulation of E2F1 activity by acetylation. EMBO J. 19(4), 662-671 (2000).
55. Luo J, Su F, Chen D, Shiloh A, Gu W. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 408(6810), 377-381 (2000).
56. Pediconi N, Ianari A, Costanzo A et al. Differential regulation of E2F1 apoptotic target genes in response to DNA damage. Nat. Cell Biol. 5(6), 552-558 (2003).
57. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL. Domainselective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl Acad. Sci. USA 100(8), 4389-4394 (2003).
58. Chiang GG, Abraham RT. Targeting the mTOR signaling network in cancer. Trends Mol. Med. 13(10), 433-442 (2007).
59. Cloughesy TF, Yoshimoto K, Nghiemphu P et al. Anti-tumor activity of rapamycin in a Phase I trial for patients with recurrent PTEN-deficient glioblastoma. PLoS Med. 5(1), e8 (2008).
60. Neshat MS, Mellinghoff IK, Tran C et al. Enhanced sensitivity of PTEN-deficient tumors to inhibition of FRAP/mTOR. Proc. Natl Acad. Sci. USA 98(18), 10314-10319 (2001).
61. Podsypanina K, Lee RT, Politis C et al. An inhibitor of mTOR reduces neoplasia and normalizes p70/S6 kinase activity in Pten+/- mice. Proc. Natl Acad. Sci. USA 98(18), 10320-10325 (2001).
62. Yu K, Toral-Barza L, Discafani C et al. mTOR, a novel target in breast cancer: the effect of CCI-779, an mTOR inhibitor, in preclinical models of breast cancer. Endocr. Relat. Cancer 8(3), 249-258 (2001).
63. Majumder PK, Febbo PG, Bikoff R et al. mTOR inhibition reverses Akt-dependent prostate intraepithelial neoplasia through regulation of apoptotic and HIF-1-dependent pathways. Nat. Med. 10(6), 594-601 (2004).
64. Grimm D. Small silencing RNAs: state-ofthe- art. Adv. Drug Del. Rev. 61, 672-703 (2009).
65. Kim DH, Saetrom P, Snøve O Jr, Rossi JJ. MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc. Natl Acad. Sci. USA 105(42), 16230-16235 (2008).
66. Castanotto D, Rossi JJ. The promises and pitfalls of RNA-interference- based therapeutics. Nature 457(7228), 426-433 (2009).
67. Grimm D, Streetz KL, Jopling CL et al. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441(7092), 537-541 (2006).
68. Armstrong ME, Gantier M, Li L et al. Small interfering RNAs induce macrophage migration inhibitory factor production and proliferation in breast cancer cells via a double-stranded RNA-dependent protein kinase-dependent mechanism. J. Immunol. 180(11), 7125-7133 (2008).
69. Dervan PB, Edelson BS. Recognition of the DNA minor groove by pyrrole-imidazole polyamides. Curr. Opin. Struct. Biol. 13(3), 284-299 (2003).
70. Harki DA, Satyamurthy N, Stout DB, Phelps ME, Dervan PB. In vivo imaging of pyrrole-imidazole polyamides with positron emission tomography. Proc. Natl Acad. Sci. USA 105(35), 13039-13044 (2008).
71. Nickols NG, Jacobs CS, Farkas ME, Dervan PB. Improved nuclear localization of DNA-binding polyamides. Nucleic Acids Res. 35(2), 363-370 (2007).
72. Dudouet B, Burnett R, Dickinson LA et al. Accessibility of nuclear chromatin by DNA binding polyamides. Chem. Biol. 10(9), 859-867 (2003).
73. Edelson BS, Best TP, Olenyuk B et al. Influence of structural variation on nuclear localization of DNA-binding polyamidefluorophore conjugates. Nucleic Acids Res. 32(9), 2802-2818 (2004).
74. Best TP, Edelson BS, Nickols NG, Dervan PB. Nuclear localization of pyrrole-imidazole polyamide-fluorescein conjugates in cell culture. Proc. Natl Acad. Sci. USA 100(21), 12063-12068 (2003).
75. Janssen S, Durussel T, Laemmli UK. Chromatin opening of DNA satellites by targeted sequence-specific drugs. Mol. Cell 6(5), 999-1011 (2000).
76. Burnett R, Melander C, Puckett JW et al. DNA sequence-specific polyamides alleviate transcription inhibition associated with long GAA.TTC repeats in Friedreich's ataxia. Proc. Natl Acad. Sci. USA 103(31), 11497-11502 (2006).
77. Olenyuk BZ, Zhang GJ, Klco JM et al. Inhibition of vascular endothelial growth factor with a sequence-specific hypoxia response element antagonist. Proc. Natl Acad. Sci. USA 101(48), 16768-16773 (2004).
78. Nickols NG, Dervan PB. Suppression of androgen receptor-mediated gene expression by a sequence-specific DNA-binding polyamide. Proc. Natl Acad. Sci. USA 104(25), 10418-10423 (2007).
79. Wurtz NR, Dervan PB. Sequence specific alkylation of DNA by hairpin pyrrole- imidazole polyamide conjugates. Chem. Biol. 7(3), 153-161 (2000).
80. Oyoshi T, Kawakami W, Narita A, Bando T, Sugiyama H. Inhibition of transcription at a coding sequence by alkylating polyamide. J. Am. Chem. Soc. 125(16), 4752-4754 (2003).
81. Shinohara K, Narita A, Oyoshi T, Bando T, Teraoka H, Sugiyama H. Sequence-specific gene silencing in mammalian cells by alkylating pyrrole-imidazole polyamides. J. Am. Chem. Soc. 126(16), 5113-5118 (2004).
82. Dickinson LA, Burnett R, Melander C et al. Arresting cancer proliferation by smallmolecule gene regulation. Chem. Biol. 11(11), 1583-1594 (2004).
83. Alvarez D, Chou CJ, Latella L et al. A two-hit mechanism for pre-mitotic arrest of cancer cell proliferation by a polyamide-alkylator conjugate. Cell Cycle 5(14), 1537-1548 (2006).
84. Tsai SM, Farkas ME, Chou CJ, Gottesfeld JM, Dervan PB. Unanticipated differences between a- and g-diaminobutyric acid-linked hairpin polyamide-alkylator conjugates. Nucleic Acids Res. 35(1), 307-316 (2007).
85. Chou CJ, Farkas ME, Tsai SM et al. Small molecules targeting histone H4 as potential therapeutics for chronic myelogenous leukemia. Mol. Cancer Ther. 7(4), 769-778 (2008).
86. Gommans WM, McLaughlin PM, Lindhout BI et al. Engineering zinc finger protein transcription factors to downregulate the epithelial glycoprotein-2 promoter as a novel anti-cancer treatment. Mol. Carcinog. 46(5), 391-401 (2007).
87. Greisman HA, Pabo CO. A general strategy for selecting high-affinity zinc finger proteins for diverse DNA target sites. Science 275(5300), 657-661 (1997).
88. Isalan M, Choo Y. Rapid, high-throughput engineering of sequence-specific zinc finger DNA-binding proteins. Methods Enzymol. 340, 593-609 (2001).
89. Margolin JF, Friedman JR, Meyer WK, Vissing H, Thiesen HJ, Rauscher FJ 3rd. Kruppel-associated boxes are potent transcriptional repression domains. Proc. Natl Acad. Sci. USA 91(10), 4509-4513 (1994).
90. Cloos PA, Christensen J, Agger K, Helin K. Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev. 22(9), 1115-1140 (2008).
91. Volkel P, Angrand PO. The control of histone lysine methylation in epigenetic regulation. Biochimie 89(1), 1-20 (2007).