Synthesis and evaluation of analogues of N-phthaloyl-l-tryptophan (RG108) as inhibitors of DNA methyltransferase 1

Journal of Medicinal Chemistry

Volumn 57, Issue 2, 2014, Pages 421-434

  Asgatay, Saaîdia ^a   Champion, Christine ^b,c   Marloie, Gaël ^a   Drujon, Thierry ^a   Senamaud Beaufort, Catherine ^b   Ceccaldi, Alexandre ^b,c   Erdmann, Alexandre ^e   Rajavelu, Arumugam ^d   Schambel, Philippe ^e   Jeltsch, Albert ^d   Lequin, Olivier ^a   Karoyan, Philippe ^a   Arimondo, Paola B ^b,e   Guianvarc'H, Dominique ^a  

^a CNRS   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITY OF STUTTGART   (Germany)

^e INSTITUT DE RECHERCHE PIERRE FABRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

(N BENZYLINDOYL)PROPANOIC ACID; (N TERT BUTYLOXYCARBONYLAMINOMETHYL) 3 N BENZYLINDOLYLPROPANOIC ACID; 2 (1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL) 3 (1H INDOLE 3 YL)BUTANOIC ACID; 2 (1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL) 3 (1H INDOLE 3 YL)PROPANAMIDE; 2 (1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL) 3 (1H INDOLE 3 YL)PROPANOIC ACID; 2 (1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL) 3 (1H INDOLE 3 YL)PROPANOIC ACID, ALPHA(AMINOMETHYL); 2 (1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL) 4 QUINOLINE PROPANOIC ACID; 2(1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL) 3 (3H IMIDAZOL 4 YL)PROPANOIC ACID; 2(1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL) 3 (5 HYDROXY 1H INDOLE 3-YL)PROPANOIC ACID; 2(1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL) 3 PHENYLPROPANOIC ACID; 3 (2H)QUINAZOLINEACETIC ACID 1,4 DIHYDRO ALPHA (1H INDOL 3 YLMETHYL) 2,4 DIOXO; 3 (BENZOTHIEN 3 YLMETHYL) 2 (1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL)PROPIONIC ACID; 3 [(1H INDOL 3 YL)METHYL] 1 [2 (1,3 DIOXOISOINDOLIN 2 YL)ACETYL PYRROLIDINE 2 CARBOXYLIC ACID; 3 [[1 (TERT BUTOXYCARBONYL) 1H INDOL 3 YL]METHYL]PYRROLIDINE 2 CARBOXYLIC ACID; ANTINEOPLASTIC AGENT; CARBOXYLIC ACID; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE INHIBITOR; INDOLE; N 2 [(3 NITRO 2 PYRIDINYL)THIO]L TRYPTOPHAN; N 3 (N BENZYLINDOYLPROPANOYL)CAMPHORSULTAM; N(2 DIBENZYLAMINOETHYL 3 N BENZYLINDOYL PROPANOYL)CAMPHORSULTAM; N2 [(2,4 DINITROPHENYL)THIO]L TRYPTOPHAN; N[2 (1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL)ACETYL]L TRYPTOPHAN; N[2 (1,3 DIHYDRO 1,3 DIOXO 2H ISOINDOL 2 YL)ACETYL]L TRYPTOPHAN PHENYLMETHYL ESTER; PHTHALIMIDE; TRYPTOPHAN DERIVATIVE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CHEMICAL MODIFICATION; CYCLIZATION; CYTOTOXICITY ASSAY; DRUG POTENCY; DRUG SYNTHESIS; EVALUATION STUDY; HUMAN; HUMAN CELL; METHODOLOGY; MOLECULAR INTERACTION;

CATALYTIC DOMAIN; CELL LINE, TUMOR; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; HUMANS; MOLECULAR DOCKING SIMULATION; PHTHALIC ACIDS; PHTHALIMIDES; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP; TRYPTOPHAN;

EID: 84893061501     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm401419p     Document Type: Article

References (58)

1. Berger, S. L.; Kouzarides, T.; Shiekhattar, R.; Shilatifard, A. An operational definition of epigenetics Genes Dev. 2009, 23, 781-783
2. Illingworth, R. S.; Bird, A. P. CpG islands-"a rough guide" FEBS Lett. 2009, 583, 1713-1720
3. Weber, M.; Hellmann, I.; Stadler, M. B.; Ramos, L.; Pääbo, S.; Rebhan, M.; Schübeler, D. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome Nat. Genet. 2007, 39, 457-466 (Pubitemid 46514772)
4. Esteller, M. Epigenetics in cancer N. Engl. J. Med. 2008, 358, 1148-1159
5. Feinberg, A. P. Phenotypic plasticity and the epigenetics of human disease Nature 2007, 447, 433-440 (Pubitemid 46816750)
6. Portela, A.; Esteller, M. Epigenetic modifications and human disease Nat. Biotechnol. 2010, 28, 1057-1068
7. Kelly, T. K.; De Carvalho, D. D.; Jones, P. A. Epigenetic modifications as therapeutic targets Nat. Biotechnol. 2010, 28, 1069-1078
8. Greger, V.; Passarge, E.; Höpping, W.; Messmer, E.; Horsthemke, B. Epigenetic changes may contribute to the formation and spontaneous regression of retinoblastoma Hum. Genet. 1989, 83, 155-158 (Pubitemid 19234564)
9. Baylin, S. B.; Herman, J. G. Promoter hypermethylation-Can this change alone ever designate true tumor suppressor gene function? J. Natl. Cancer Inst. 2001, 93, 664-665 (Pubitemid 32492799)
10. Jones, P. A.; Baylin, S. B. The epigenomics of cancer Cell 2007, 128, 683-692 (Pubitemid 46273572)
11. Jurkowska, R. Z.; Jurkowski, T. P.; Jeltsch, A. Structure and function of mammalian DNA methyltransferases ChemBioChem 2011, 12, 206-222
12. Yu, N.; Wang, M. Anticancer drug discovery targeting DNA hypermethylation Curr. Med. Chem. 2008, 15, 1350-1375 (Pubitemid 351997787)
13. Szyf, M. Epigenetics, DNA methylation, and chromatin modifying drugs Annu. Rev. Pharmacol. Toxicol. 2009, 49, 243-263
14. Mai, A.; Altucci, L. Epi-drugs to fight cancer: from chemistry to cancer treatment, the road ahead Int. J. Biochem. Cell Biol. 2009, 41, 199-213
15. Stresemann, C.; Lyko, F. Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine Int. J. Cancer 2008, 123, 8-13 (Pubitemid 351705186)
16. Juergens, R. A.; Wrangle, J.; Vendetti, F. P.; Murphy, S. C.; Zhao, M.; Coleman, B.; Sebree, R.; Rodgers, K.; Hooker, C. M.; Franco, N.; Lee, B.; Tsai, S.; Delgado, I. E.; Rudek, M. A.; Belinsky, S. A.; Herman, J. G.; Baylin, S. B.; Brock, M. V.; Rudin, C. M. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer Cancer Discovery 2011, 1, 598-607
17. Chuang, J. C.; Warner, S. L.; Vollmer, D.; Vankayalapati, H.; Redkar, S.; Bearss, D. J.; Qiu, X.; Yoo, C. B.; Jones, P. A. S110, a 5-Aza-2′- deoxycytidine-containing dinucleotide, is an effective DNA methylation inhibitor in vivo and can reduce tumor growth Mol. Cancer Ther. 2010, 9, 1443-1450
18. Chuang, J. C.; Yoo, C. B.; Kwan, J. M.; Li, T. W. H.; Liang, G.; Yang, A. S.; Jones, P. A. Comparison of biological effects of non-nucleoside DNA methylation inhibitors versus 5-aza-2′-deoxycytidine Mol. Cancer Ther. 2005, 4, 1515-1520 (Pubitemid 41556433)
19. Rajavelu, A.; Tulyasheva, Z.; Jaiswal, R.; Jeltsch, A.; Kuhnert, N. The inhibition of the mammalian DNA methyltransferase 3a (Dnmt3a) by dietary black tea and coffee polyphenols BMC Biochem. 2011, 12, 16
20. Fang, M. Z.; Wang, Y.; Ai, N.; Hou, Z.; Sun, Y.; Lu, H.; Welsh, W.; Yang, C. S. Tea polyphenol (-)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines Cancer Res. 2003, 63, 7563-7570 (Pubitemid 37466673)
21. Fang, M. Z.; Chen, D.; Sun, Y.; Jin, Z.; Christman, J. K.; Yang, C. S. Reversal of hypermethylation and reactivation of p16INK4a, RARβ, and MGMT genes by genistein and other isoflavones from soy Clin. Cancer Res. 2005, 11, 7033-7041 (Pubitemid 41428763)
22. Kuck, D.; Caulfield, T.; Lyko, F.; Medina-Franco, J. L. Nanaomycin A selectively inhibits DNMT3B and reactivates silenced tumor suppressor genes in human cancer cells Mol. Cancer Ther. 2010, 9, 3015-3023
23. Piña, I. C.; Gautschi, J. T.; Wang, G.-Y.-S.; Sanders, M. L.; Schmitz, F. J.; France, D.; Cornell-Kennon, S.; Sambucetti, L. C.; Remiszewski, S. W.; Perez, L. B.; Bair, K. W.; Crews, P. Psammaplins from the sponge Pseudoceratina purpurea: inhibition of both histone deacetylase and DNA methyltransferase J. Org. Chem. 2003, 68, 3866-3873 (Pubitemid 36576636)
24. Fagan, R. L.; Cryderman, D. E.; Kopelovich, L.; Wallrath, L. L.; Brenner, C. Laccaic acid A is a direct, DNA-competitive inhibitor of DNA methyltransferase 1 J. Biol. Chem. 2013, 288, 23858-23867
25. Singh, N.; Dueñas-González, A.; Lyko, F.; Medina-Franco, J. L. Molecular modeling and molecular dynamics studies of hydralazine with human DNA methyltransferase 1 ChemMedChem 2009, 4, 792-799
26. Villar-Garea, A.; Fraga, M. F.; Espada, J.; Esteller, M. Procaine is a DNA-demethylating agent with growth-inhibitory effects in human cancer cells Cancer Res. 2003, 63, 4984-4989 (Pubitemid 37022635)
27. Lee, B. H.; Yegnasubramanian, S.; Lin, X.; Nelson, W. G. Procainamide is a specific inhibitor of DNA methyltransferase 1 J. Biol. Chem. 2005, 280, 40749-40756 (Pubitemid 41780565)
28. Kuck, D.; Singh, N.; Lyko, F.; Medina-Franco, J. L. Novel and selective DNA methyltransferase inhibitors: docking-based virtual screening and experimental evaluation Bioorg. Med. Chem. 2010, 18, 822-829
29. Medina-Franco, J. L.; López-Vallejo, F.; Kuck, D.; Lyko, F. Natural products as DNA methyltransferase inhibitors: a computer-aided discovery approach Mol. Diversity 2011, 15, 293-304
30. Brueckner, B.; Boy, R. G.; Siedlecki, P.; Musch, T.; Kliem, H. C.; Zielenkiewicz, P.; Suhai, S.; Wiessler, M.; Lyko, F. Epigenetic reactivation of tumor suppressor genes by a novel small-molecule inhibitor of human DNA methyltransferases Cancer Res. 2005, 65, 6305-6311 (Pubitemid 40994416)
31. Stresemann, C.; Brueckner, B.; Musch, T.; Stopper, H.; Lyko, F. Functional diversity of DNA methyltransferase inhibitors in human cancer cell lines Cancer Res. 2006, 66, 2794-2800
32. Datta, J.; Ghoshal, K.; Denny, W. A.; Gamage, S. A.; Brooke, D. G.; Phiasivongsa, P.; Redkar, S.; Jacob, S. T. A new class of quinoline-based DNA hypomethylating agents reactivates tumor suppressor genes by blocking DNA methyltransferase 1 activity and inducing its degradation Cancer Res. 2009, 69, 4277-4285
33. Isakovic, L.; Saavedra, O. M.; Llewellyn, D. B.; Claridge, S.; Zhan, L.; Bernstein, N.; Vaisburg, A.; Elowe, N.; Petschner, A. J.; Rahil, J.; Beaulieu, N.; Gauthier, F.; MacLeod, A. R.; Delorme, D.; Besterman, J. M.; Wahhab, A. Constrained (l -)- S -adenosyl- l -homocysteine (SAH) analogues as DNA methyltransferase inhibitors Bioorg. Med. Chem. Lett. 2009, 19, 2742-2746
34. Saavedra, O. M.; Isakovic, L.; Llewellyn, D. B.; Zhan, L.; Bernstein, N.; Claridge, S.; Raeppel, F.; Vaisburg, A.; Elowe, N.; Petschner, A. J.; Rahil, J.; Beaulieu, N.; MacLeod, A. R.; Delorme, D.; Besterman, J. M.; Wahhab, A. SAR around (l)- S -adenosyl- l -homocysteine, an inhibitor of human DNA methyltransferase (DNMT) enzymes Bioorg. Med. Chem. Lett. 2009, 19, 2747-2751
35. Gros, C.; Fahy, J.; Halby, L.; Dufau, I.; Erdmann, A.; Gregoire, J.-M.; Ausseil, F.; Vispé, S.; Arimondo, P. B. DNA methylation inhibitors in cancer: recent and future approaches Biochimie 2012, 94, 2280-2296
36. 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.; Arimondo, P. B. C5-DNA methyltransferase inhibitors: from screening to effects on zebrafish embryo development ChemBioChem 2011, 12, 1337-1345
37. Halby, L.; Champion, C.; Sénamaud-Beaufort, C.; Ajjan, S.; Drujon, T.; Rajavelu, A.; Ceccaldi, A.; Jurkowska, R.; Lequin, O.; Nelson, W. G.; Guy, A.; Jeltsch, A.; Guianvarc'h, D.; Ferroud, C.; Arimondo, P. B. Rapid synthesis of new DNMT inhibitors derivatives of procainamide ChemBioChem 2012, 13, 157-165
38. Suzuki, T.; Tanaka, R.; Hamada, S.; Nakagawa, H.; Miyata, N. Design, synthesis, inhibitory activity, and binding mode study of novel DNA methyltransferase 1 inhibitors Bioorg. Med. Chem. Lett. 2010, 20, 1124-1127
39. Castellano, S.; Kuck, D.; Sala, M.; Novellino, E.; Lyko, F.; Sbardella, G. Constrained analogues of procaine as novel small molecule inhibitors of DNA methyltransferase-1 J. Med. Chem. 2008, 51, 2321-2325 (Pubitemid 351503289)
40. Castellano, S.; Kuck, D.; Viviano, M.; Yoo, J.; López-Vallejo, F.; Conti, P.; Tamborini, L.; Pinto, A.; Medina-Franco, J. L.; Sbardella, G. Synthesis and biochemical evaluation of δ(2)-isoxazoline derivatives as DNA methyltransferase 1 inhibitors J. Med. Chem. 2011, 54, 7663-7677
41. Casimir, J. R.; Guichard, G.; Briand, J.-P. Methyl 2-((succinimidooxy) carbonyl)benzoate (MSB): a new, efficient reagent for N-phthaloylation of amino acid and peptide derivatives J. Org. Chem. 2002, 67, 3764-3768 (Pubitemid 34563988)
42. Canonne, P.; Akssira, M.; Dahdouh, A.; Kasmi, H.; Boumzebra, M. Synthesis of chiral 3-substituted 2,4(1 H,3 H)-quinazolinediones Heterocycles 1993, 36, 1305
43. Moumne, R.; Larregola, M.; Boutadla, M.; Karoyan, P. Aminomethylation of chiral silyl enol ethers; access to beta(2)-homotryptophane and beta(2)-homolysine derivatives Tethradron Lett. 2009, 49, 4704-4706
44. Mothes, C.; Lavielle, S.; Karoyan, P. Amino-zinc-ene-enolate cyclization: a short access to cis-3-substituted prolino-homotryptophane derivatives J. Org. Chem. 2008, 73, 6706-6710
45. Siedlecki, P.; Garcia Boy, R.; Musch, T.; Brueckner, B.; Suhai, S.; Lyko, F.; Zielenkiewicz, P. Discovery of two novel, small-molecule inhibitors of DNA methylation J. Med. Chem. 2006, 49, 678-683 (Pubitemid 43157497)
46. Siedlecki, P.; Garcia Boy, R.; Comagic, S.; Schirrmacher, R.; Wiessler, M.; Zielenkiewicz, P.; Suhai, S.; Lyko, F. Establishment and functional validation of a structural homology model for human DNA methyltransferase 1 Biochem. Biophys. Res. Commun. 2003, 306, 558-563 (Pubitemid 36683111)
47. Baud, M. G. J.; Leiser, T.; Haus, P.; Samlal, S.; Wong, A. C.; Wood, R. J.; Petrucci, V.; Gunaratnam, M.; Hughes, S. M.; Buluwela, L.; Turlais, F.; Neidle, S.; Meyer-Almes, F.-J.; White, A. J. P.; Fuchter, M. J. Defining the mechanism of action and enzymatic selectivity of psammaplin A against its epigenetic targets J. Med. Chem. 2012, 55, 1731-1750
48. Dalvit, C.; Pevarello, P.; Tatò, M.; Veronesi, M.; Vulpetti, A.; Sundström, M. Identification of compounds with binding affinity to proteins via magnetization transfer from bulk water J. Biomol. NMR 2000, 18, 65-68
49. Dalvit, C.; Fogliatto, G.; Stewart, A.; Veronesi, M.; Stockman, B. WaterLOGSY as a method for primary NMR screening: practical aspects and range of applicability J. Biomol. NMR 2001, 21, 349-359 (Pubitemid 34071389)
50. Dalvit, C. Theoretical analysis of the competition ligand-based NMR experiments and selected applications to fragment screening and binding constant measurements Concepts Magn. Reson., Part A 2008, 32A, 341-372
51. Schirrmacher, E.; Beck, C.; Brueckner, B.; Schmitges, F.; Siedlecki, P.; Bartenstein, P.; Lyko, F.; Schirrmacher, R. Synthesis and in vitro evaluation of biotinylated RG108: a high affinity compound for studying binding interactions with human DNA methyltransferases Bioconjugate Chem. 2006, 17, 261-266
52. Song, J.; Teplova, M.; Ishibe-Murakami, S.; Patel, D. J. Structure-based mechanistic insights into DNMT1-mediated maintenance DNA methylation Science 2012, 335, 709-712
53. Rathert, P.; Cheng, X.; Jeltsch, A. Continuous enzymatic assay for histone lysine methyltransferases BioTechniques 2007, 43, 602-608 (Pubitemid 350174910)
54. Urig, S.; Gowher, H.; Hermann, A.; Beck, C.; Fatemi, M.; Humeny, A.; Jeltsch, A. The Escherichia coli dam DNA methyltransferase modifies DNA in a highly processive reaction J. Mol. Biol. 2002, 319, 1085-1096 (Pubitemid 34729420)
55. Horton, J. R.; Liebert, K.; Hattman, S.; Jeltsch, A.; Cheng, X. Transition from nonspecific to specific DNA interactions along the substrate-recognition pathway of dam methyltransferase Cell 2005, 121, 349-361 (Pubitemid 40692296)
56. Liebert, K.; Horton, J. R.; Chahar, S.; Orwick, M.; Cheng, X.; Jeltsch, A. Two alternative conformations of S -adenosyl- l -homocysteine bound to Escherichia coli DNA adenine methyltransferase and the implication of conformational changes in regulating the catalytic cycle J. Biol. Chem. 2007, 282, 22848-22855 (Pubitemid 47267332)
57. Roth, M.; Jeltsch, A. Biotin-avidin microplate assay for the quantitative analysis of enzymatic methylation of DNA by DNA methyltransferases Biol. Chem. 2000, 381, 269-272 (Pubitemid 30179562)
58. Jia, D.; Jurkowska, R. Z.; Zhang, X.; Jeltsch, A.; Cheng, X. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation Nature 2007, 449, 248-251 (Pubitemid 47402375)