Laccaic acid A is a direct, DNA-competitive inhibitor of DNA methyltransferase 1

Journal of Biological Chemistry

Volumn 288, Issue 33, 2013, Pages 23858-23867

  Fagan, Rebecca L ^a   Cryderman, Diane E ^a   Kopelovich, Levy ^b   Wallrath, Lori L ^a   Brenner, Charles ^a  

^a UNIVERSITY OF IOWA   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER CELLS; DNA METHYLATION; DNA METHYLTRANSFERASES; METHYLTRANSFERASES; NATURAL PRODUCTS; SMALL MOLECULES;

LIFE CYCLE;

DNA;

5 AZA 2' DEOXYCYTIDINE; ANTINEOPLASTIC AGENT; CYTOCHROME P450 1A; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE INHIBITOR; LACCAIC ACID A; SGI 1027; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL; CEACAM5 GENE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CPG ISLAND; DHRS3 GENE; DNA METHYLATION; DOWN REGULATION; DRUG DNA BINDING; DRUG EFFECT; DRUG IDENTIFICATION; DRUG SPECIFICITY; DRUG STRUCTURE; ENZYME INHIBITION; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MAL GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RGS16 GENE; UPREGULATION; VGF GENE;

CANCER THERAPY; CHEMICAL BIOLOGY; DNA METHYLATION; DNA METHYLTRANSFERASE; DRUG ACTION; DRUG DISCOVERY; ENZYME INHIBITORS; FRET; GENE SILENCING; MICROARRAY;

AMINOQUINOLINES; ANTHRAQUINONES; AZACITIDINE; AZO COMPOUNDS; BASE SEQUENCE; BREAST NEOPLASMS; DNA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA REPLICATION; ENZYME INHIBITORS; FEMALE; FLUOROMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PYRIMIDINES; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TRANSITION TEMPERATURE;

EID: 84882386706     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.480517     Document Type: Article

References (59)

1. Bird, A. (2002) DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21
2. Yokochi, T., and Robertson, K. D. (2002) Preferential methylation of unmethylated DNA by Mammalian de novo DNA methyltransferase Dnmt3a. J. Biol. Chem. 277, 11735-11745
3. Yoder, J. A., Soman, N. S., Verdine, G. L., and Bestor, T. H. (1997) DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J. Mol. Biol. 270, 385-395
4. Szyf, M. (1994) DNA methylation properties. Consequences for pharmacology. Trends Pharmacol. Sci. 15, 233-238
5. MacLeod, A. R., Rouleau, J., and Szyf, M. (1995) Regulation of DNA methylation by the Ras signaling pathway. J. Biol. Chem. 270, 11327-11337
6. Slack, A., Cervoni, N., Pinard, M., and Szyf, M. (1999) DNA methyltransferase is a downstream effector of cellular transformation triggered by simian virus 40 large T antigen. J. Biol. Chem. 274, 10105-10112
7. Bigey, P., Ramchandani, S., Theberge, J., Araujo, F. D., and Szyf, M. (2000) Transcriptional regulation of the humanDNAMethyltransferase (dnmt1) gene. Gene 242, 407-418
8. Detich, N., Ramchandani, S., and Szyf, M. (2001) A conserved 3-untranslated element mediates growth regulation of DNA methyltransferase 1 and inhibits its transforming activity. J. Biol. Chem. 276, 24881-24890
9. Daniel, F. I., Cherubini, K., Yurgel, L. S., de Figueiredo, M. A., and Salum, F. G. (2011) The role of epigenetic transcription repression and DNA methyltransferases in cancer. Cancer 117, 677-687
10. Teodoridis, J. M., Hardie, C., and Brown, R. (2008) CpG island methylator phenotype (CIMP) in cancer. Causes and implications. Cancer Lett. 268, 177-186
11. Eads, C. A., Nickel, A. E., and Laird, P. W. (2002) Complete genetic suppression of polyp formation and reduction of CpG-island hypermethylation in Apc(Min/) Dnmt1-hypomorphic Mice. Cancer Res. 62, 1296-1299
12. MacLeod, A. R., and Szyf, M. (1995) Expression of antisense to DNA methyltransferase mRNA induces DNA demethylation and inhibits tumorigenesis. J. Biol. Chem. 270, 8037-8043
13. Ramchandani, S., MacLeod, A. R., Pinard, M., von Hofe, E., and Szyf, M. (1997) Inhibition of tumorigenesis by a cytosine-DNA, methyltransferase, antisense oligodeoxynucleotide. Proc. Natl. Acad. Sci. U.S.A. 94, 684-689
14. Ley, T. J., Ding, L., Walter, M. J., McLellan, M. D., Lamprecht, T., Larson, D. E., Kandoth, C., Payton, J. E., Baty, J., Welch, J., Harris, C. C., Lichti, C. F., Townsend, R. R., Fulton, R. S., Dooling, D. J., Koboldt, D. C., Schmidt, H., Zhang, Q., Osborne, J. R., Lin, L., O'Laughlin, M., McMichael, J. F., Delehaunty, K. D., McGrath, S. D., Fulton, L. A., Magrini, V. J., Vickery, T. L., Hundal, J., Cook, L. L., Conyers, J. J., Swift, G. W., Reed, J. P., Alldredge, P. A., Wylie, T., Walker, J., Kalicki, J., Watson, M. A., Heath, S., Shannon, W. D., Varghese, N., Nagarajan, R., Westervelt, P., Tomasson, M. H., Link, D. C., Graubert, T. A., DiPersio, J. F., Mardis, E. R., and Wilson, R. K. (2010) DNMT3A mutations in acute myeloid leukemia. N. Engl. J. Med. 363, 2424-2433
15. Yoo, C. B., and Jones, P. A. (2006) Epigenetic therapy of cancer. Past, present, and future. Nat. Rev. Drug Discov. 5, 37-50
16. Stresemann, C., and Lyko, F. (2008) Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int. J. Cancer 123, 8-13
17. Taberlay, P. C., and Jones, P. A. (2011)DNAmethylation and cancer. Prog. Drug. Res. 67, 1-23
18. Rountree, M. R., Bachman, K. E., and Baylin, S. B. (2000) DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat. Genet. 25, 269-277
19. Chuang, L. S., Ian, H. I., Koh, T. W., Ng, H. H., Xu, G., and Li, B. F. (1997) Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 277, 1996-2000
20. Leonhardt, H., Page, A. W., Weier, H. U., and Bestor, T. H. (1992) A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 71, 865-873
21. Bestor, T. H. (1992) Activation of mammalian DNA methyltransferase by cleavage of a zinc binding regulatory domain. EMBO J. 11, 2611-2617
22. Callebaut, I., Courvalin, J. C., and Mornon, J. P. (1999) The BAH (bromoadjacent homology) domain. A link between DNA methylation, replication and transcriptional regulation. FEBS Lett. 446, 189-193
23. Song, J., Rechkoblit, O., Bestor, T. H., and Patel, D. J. (2011) Structure of DNMT1-DNA complex reveals a role for autoinhibition in maintenance DNA methylation. Science 331, 1036-1040
24. Syeda, F., Fagan, R. L., Wean, M., Avvakumov, G. V., Walker, J. R., Xue, S., Dhe-Paganon, S., and Brenner, C. (2011) The replication focus targeting sequence (RFTS) domain is a DNA-competitive inhibitor of Dnmt1. J. Biol. Chem. 286, 15344-15351
25. Takeshita, K., Suetake, I., Yamashita, E., Suga, M., Narita, H., Nakagawa, A., and Tajima, S. (2011) Structural insight into maintenance methylation by mouse DNA methyltransferase 1 (Dnmt1). Proc. Natl. Acad. Sci. U.S.A. 108, 9055-9059
26. Song, J., Teplova, M., Ishibe-Murakami, S., and Patel, D. J. (2012) Structure-based mechanistic insights into DNMT1-mediated maintenance DNA methylation. Science 335, 709-712
27. Liu, Z., and Fisher, R. A. (2004) RGS6 interacts with DMAP1 and DNMT1 and inhibits DMAP1 transcriptional repressor activity. J. Biol. Chem. 279, 14120-14128
28. Niesen, F. H., Berglund, H., and Vedadi, M. (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2, 2212-2221
29. Wang, J., Duncan, D., Shi, Z., and Zhang, B. (2013) WEB-based GEne SeT AnaLysis Toolkit (WebGestalt). Update 2013. Nucleic Acids Res. 41, W77-W83
30. Zhang, B., Kirov, S., and Snoddy, J. (2005) WebGestalt. An integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res. 33, W741-W748
31. Datta, J., Ghoshal, K., Denny, W. A., Gamage, S. A., Brooke, D. G., Phiasivongsa, P., Redkar, S., and Jacob, S. T. (2009) A new class of quinolinebased DNA hypomethylating agents reactivates tumor suppressor genes by blocking DNA methyltransferase 1 activity and inducing its degradation. Cancer Res. 69, 4277-4285
32. Gros, C., Fahy, J., Halby, L., Dufau, I., Erdmann, A., Gregoire, J. M., Ausseil, F., Vispé, S., and Arimondo, P. B. (2012) DNA methylation inhibitors in cancer. Recent and future approaches. Biochimie 94, 2280-2296
33. Wood, R. J., McKelvie, J. C., Maynard-Smith, M. D., and Roach, P. L. (2010) A real-time assay for CpG-specific cytosine-C5 methyltransferase activity. Nucleic Acids Res. 38, e107
34. Gowher, H., and Jeltsch, A. (2001) Enzymatic properties of recombinant Dnmt3aDNAmethyltransferase from mouse. The enzyme modifiesDNA in a non-processive manner and also methylates non-CpG [correction of non-CpA] sites. J. Mol. Biol. 309, 1201-1208
35. Aoki, A., Suetake, I., Miyagawa, J., Fujio, T., Chijiwa, T., Sasaki, H., and Tajima, S. (2001) Enzymatic properties of de novo-type mouse DNA (cytosine-5) methyltransferases. Nucleic Acids Res. 29, 3506-3512
36. Rao, C. N., Segawa, T., Navari, J. R., Xu, L., Srivastava, S., Moul, J. W., and Phillips, B. (2003) Methylation of TFPI-2 gene is not the sole cause of its silencing. Int. J. Oncol. 22, 843-848
37. Segura-Pacheco, B., Trejo-Becerril, C., Perez-Cardenas, E., Taja-Chayeb, L., Mariscal, I., Chavez, A., Acuña, C., Salazar, A. M., Lizano, M., and Dueñas-Gonzalez, A. (2003) Reactivation of tumor suppressor genes by the cardiovascular drugs hydralazine and procainamide and their potential use in cancer therapy. Clin. Cancer Res. 9, 1596-1603
38. Ostrow, K. L., Park, H. L., Hoque, M. O., Kim, M. S., Liu, J., Argani, P., Westra, W., Van Criekinge, W., and Sidransky, D. (2009) Pharmacologic unmasking of epigenetically silenced genes in breast cancer. Clin. Cancer Res. 15, 1184-1191
39. Paluszczak, J., Krajka-Kúlzniak, V., and Baer-Dubowska, W. (2010) The effect of dietary polyphenols on the epigenetic regulation of gene expression in MCF7 breast cancer cells. Toxicol. Lett. 192, 119-125
40. Place, T. L., Fitzgerald, M. P., Venkataraman, S., Vorrink, S. U., Case, A. J., Teoh, M. L., and Domann, F. E. (2011) Aberrant promoter CpG methylation is a mechanism for impaired PHD3 expression in a diverse set of malignant cells. PLoS ONE 6, e14617
41. Tao, Y., Liu, S., Briones, V., Geiman, T. M., and Muegge, K. (2011) Treatment of breast cancer cells with DNA demethylating agents leads to a release of Pol II stalling at genes with DNA-hypermethylated regions upstream of TSS. Nucleic Acids Res. 39, 9508-9520
42. Ohno, M., Ikenaka, Y., and Ishizuka, M. (2012) Sudan III dye strongly induces CYP1A1mRNAexpression in HepG2 cells. J. Biochem. Mol. Toxicol. 26, 16-22
43. Oleaga, C., García, M., Solé, A., Ciudad, C. J., Izquierdo-Pulido, M., and Noé, V. (2012) CYP1A1 is overexpressed upon incubation of breast cancer cells with a polyphenolic cocoa extract. Eur. J. Nutr. 51, 465-476
44. Norwood, L. E., Grade, S. K., Cryderman, D. E., Hines, K. A., Furiasse, N., Toro, R., Li, Y., Dhasarathy, A., Kladde, M. P., Hendrix, M. J., Kirschmann, D. A., and Wallrath, L. L. (2004) Conserved properties of HP1(Hs+). Gene 336, 37-46
45. Azad, N., Zahnow, C. A., Rudin, C. M., and Baylin, S. B. (2013) The future of epigenetic therapy in solid tumours-lessons from the past. Nat. Rev. Clin. Oncol. 10, 256-266
46. Karahoca, M., and Momparler, R. L. (2013) Pharmacokinetic and pharmacodynamic analysis of 5-aza-2-deoxycytidine (decitabine) in the design of its dose-schedule for cancer therapy. Clin. Epigenetics 5, 3
47. Robertson, K. D. (2001) DNA methylation, methyltransferases, and cancer. Oncogene 20, 3139-3155
48. Khan, S. I., Aumsuwan, P., Khan, I. A., Walker, L. A., and Dasmahapatra, A. K. (2012) Epigenetic events associated with breast cancer and their prevention by dietary components targeting the epigenome. Chem. Res. Toxicol. 25, 61-73
49. Tanaka, T. (1997) Reproductive and neurobehavioural effects of lac dye administered in the diet to mice. Food Addit. Contam. 14, 373-380
50. Ceccaldi, A., Rajavelu, A., Champion, C., Rampon, C., Jurkowska, R., Jankevicius, G., Sénamaud-Beaufort, C., Ponger, L., Gagey, N., Ali, H. D., Tost, J., Vriz, S., Ros, S., Dauzonne, D., Jeltsch, A., Guianvarc'h, D., and Arimondo, P. B. (2011) C5-DNA methyltransferase inhibitors. From screening to effects on zebrafish embryo development. Chembiochem. 12, 1337-1345
51. Jurkowska, R. Z., Jurkowski, T. P., and Jeltsch, A. (2011) Structure and function of mammalian DNA methyltransferases. Chembiochem 12, 206-222
52. Vilkaitis, G., Suetake, I., Klimasauskas, S., and Tajima, S. (2005) Processive methylation of hemimethylated CpG sites by mouse Dnmt1 DNA methyltransferase. J. Biol. Chem. 280, 64-72
53. Goyal, R., Reinhardt, R., and Jeltsch, A. (2006) Accuracy of DNA methylation pattern preservation by the Dnmt1 methyltransferase. Nucleic Acids Res. 34, 1182-1188
54. Mueller, E., Sarraf, P., Tontonoz, P., Evans, R. M., Martin, K. J., Zhang, M., Fletcher, C., Singer, S., and Spiegelman, B. M. (1998) Terminal differentiation of human breast cancer through PPAR . Mol. Cell 1, 465-470
55. Subbaramaiah, K., Howe, L. R., Zhou, X. K., Yang, P., Hudis, C. A., Kopelovich, L., and Dannenberg, A. J. (2012) Pioglitazone, a PPAR+ agonist, suppresses CYP19 transcription. evidence for involvement of 15- hydroxyprostaglandin dehydrogenase and BRCA1. Cancer Prev. Res. (Phila) 5, 1183-1194
56. Furuta, J., Nobeyama, Y., Umebayashi, Y., Otsuka, F., Kikuchi, K., and Ushijima, T. (2006) Silencing of peroxiredoxin 2 and aberrant methylation of 33 CpG islands in putative promoter regions in human malignant melanomas. Cancer Res. 66, 6080-6086
57. Rivenbark, A. G., Jones, W. D., Risher, J. D., and Coleman, W. B. (2006) DNA methylation-dependent epigenetic regulation of gene expression in MCF-7 breast cancer cells. Epigenetics 1, 32-44
58. Wiechec, E., Overgaard, J., and Hansen, L. L. (2008) A fragile site within the HPC1 region at 1q25.3 affecting RGS16, RGSL1, and RGSL2 in human breast carcinomas. Genes Chromosomes Cancer 47, 766-780
59. Huang, J., Stewart, A., Maity, B., Hagen, J., Fagan, R. L., Yang, J., Quelle, D. E., Brenner, C., and Fisher, R. A. (2013) RGS6 supresses Ras-induced cellular transformation by facilitating Tip60-mediated Dnmt1 degradation and promoting apoptosis. Oncogene, in press