Synthetic modified pyrrolo[1,4] benzodiazepine molecules demonstrate selective anticancer activity by targeting the human ligase 1 enzyme: An in silico and in vitro mechanistic study

Chemico-Biological Interactions

Volumn 237, Issue , 2015, Pages 115-124

  Shameem, Mohammad ^a   Kumar, Ravi ^a   Krishna, Shagun ^a   Kumar, Chandan ^a   Siddiqi, Mohammad Imran ^a   Kundu, Bijoy ^a   Banerjee, Dibyendu ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

Apoptosis; Colon cancer; DNA ligase 1; Hepatic cancer; Ligase inhibitor; PBD derivatives; Replication

Indexed keywords

AMINO ACID; ANTINEOPLASTIC AGENT; BENZODIAZEPINE DERIVATIVE; DNA LIGASE 1; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PYRROLO[1,4]BENZODIAZEPINE DERIVATIVE; S 010 015; S 010 018; UNCLASSIFIED DRUG; DNA; DNA LIGASE (ATP); PRIMER DNA; S010-015; S010-018;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL LINE; CELL VIABILITY; CHEMICAL MODIFICATION; COLON CANCER; COLONY FORMATION; COMPUTER MODEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DLD 1 CELL LINE; DRUG CYTOTOXICITY; DRUG DNA INTERACTION; DRUG SELECTIVITY; DRUG STRUCTURE; DRUG SYNTHESIS; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; METASTASIS INHIBITION; MIGRATION INHIBITION; MOLECULAR DOCKING; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; NUCLEOTIDE BINDING SITE; WOUND HEALING; CELL LINE; DRUG EFFECTS; GEL MOBILITY SHIFT ASSAY; IC50; METABOLISM; NUCLEOTIDE SEQUENCE; SPECTROFLUOROMETRY;

MAMMALIA;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BASE SEQUENCE; BENZODIAZEPINONES; CELL LINE; DNA; DNA LIGASES; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HUMANS; IN VITRO TECHNIQUES; INHIBITORY CONCENTRATION 50; MOLECULAR DOCKING SIMULATION; SPECTROMETRY, FLUORESCENCE; WOUND HEALING;

EID: 84935914003     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2015.05.024     Document Type: Article

References (38)

1. R. Okazaki, T. Okazaki, K. Sakabe, K. Sugimoto, and A. Sugino Mechanism of DNA chain growth. I. Possible discontinuity and unusual secondary structure of newly synthesized chains Proc. Natl. Acad. Sci. U.S.A. 59 2 1968 598 605
2. I.R. Lehman DNA ligase: structure, mechanism, and function Science 186 4166 1974 790 797
3. F. Fabre, and H. Roman Evidence that a single DNA ligase is involved in replication and recombination in yeast Proc. Natl. Acad. Sci. U.S.A. 76 9 1979 4586 4588
4. C. Prigent, M.S. Satoh, G. Daly, D.E. Barnes, and T. Lindahl Aberrant DNA repair and DNA replication due to an inherited enzymatic defect in human DNA ligase I Mol. Cell. Biol. 14 1 1994 310 317
5. A.E. Tomkinson, S. Vijayakumar, J.M. Pascal, and T. Ellenberger DNA ligases: structure, reaction mechanism, and function Chem. Rev. 106 2 2006 687 699
6. D.S. Levin, A.E. McKenna, T.A. Motycka, Y. Matsumoto, and A.E. Tomkinson Interaction between PCNA and DNA ligase I is critical for joining of Okazaki fragments and long-patch base-excision repair Curr. Biol. 10 15 2000 919 922
7. S. Soderhall, and T. Lindahl Mammalian deoxyribonucleic acid ligase Isolation of an active enzyme-adenylate complex, J Biol Chem 248 2 1973 672 675
8. S. Soderhall Properties of a DNA-adenylate complex formed in the reaction between mammalian DNA ligase I and DNA containing single-strand breaks Eur. J. Biochem. 51 1 1975 129 136
9. L.M. Henderson, C.F. Arlett, S.A. Harcourt, A.R. Lehmann, and B.C. Broughton Cells from an immunodeficient patient (46BR) with a defect in DNA ligation are hypomutable but hypersensitive to the induction of sister chromatid exchanges Proc. Natl. Acad. Sci. U.S.A. 82 7 1985 2044 2048
10. D.E. Barnes, A.E. Tomkinson, A.R. Lehmann, A.D. Webster, and T. Lindahl Mutations in the DNA ligase I gene of an individual with immunodeficiencies and cellular hypersensitivity to DNA-damaging agents Cell 69 3 1992 495 503
11. S. Das-Bradoo, H.D. Nguyen, J.L. Wood, R.M. Ricke, J.C. Haworth, and A.K. Bielinsky Defects in DNA ligase I trigger PCNA ubiquitylation at Lys 107 Nat. Cell Biol. 12 1 2009 74 79 (sup pp. 71-20)
12. D. Sun, R. Urrabaz, M. Nguyen, J. Marty, S. Stringer, E. Cruz, L. Medina-Gundrum, and S. Weitman Elevated expression of DNA ligase I in human cancers Clin. Cancer Res. 7 12 2001 4143 4148
13. T. Kaneko, H. Wong, and T.W. Doyle A total synthesis of chicamycin A a new pyrrolo[1,4]benzodiazepine antitumor agent J. Antibiot. (Tokyo) 37 3 1984 300 302
14. R.L. Clark, K.C. Carter, A.B. Mullen, G.D. Coxon, G. Owusu-Dapaah, E. McFarlane, M.D. DuongThi, M.H. Grant, J.N. Tettey, and S.P. Mackay Identification of the benzodiazepines as a new class of antileishmanial agent Bioorg. Med. Chem. Lett. 17 3 2007 624 627
15. L. Cipolla, A.C. Araujo, C. Airoldi, and D. Bini Pyrrolo[2,1-c][1,4]benzodiazepine as a scaffold for the design and synthesis of anti-tumour drugs Anticancer Agents Med. Chem. 9 1 2009 1 31
16. P.G. Baraldi, G. Balboni, B. Cacciari, A. Guiotto, S. Manfredini, R. Romagnoli, G. Spalluto, D.E. Thurston, P.W. Howard, N. Bianchi, C. Rutigliano, C. Mischiati, and R. Gambari Synthesis, in vitro antiproliferative activity, and DNA-binding properties of hybrid molecules containing pyrrolo[2,1-c] [1,4]benzodiazepine and minor-groove-binding oligopyrrole carriers J. Med. Chem. 42 25 1999 5131 5141
17. S.K. Sharma, A.K. Mandadapu, K. Kumaresan, A. Arora, H.M. Gauniyal, and B. Kundu Efficient synthesis of naturally occurring skeleton 5-7-6 tricyclic pyrrolo[2,1-c] [1,4]benzodiazepin-5-one and its derivatives via cationic pi-cyclization Synthesis-Stuttgart 23 2010 4087 4095
18. J.M. Pascal, P.J. O'Brien, A.E. Tomkinson, and T. Ellenberger Human DNA ligase I completely encircles and partially unwinds nicked DNA Nature 432 7016 2004 473 478
19. M. Rarey, B. Kramer, T. Lengauer, and G. Klebe A fast flexible docking method using an incremental construction algorithm J. Mol. Biol. 261 3 1996 470 489
20. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 13 2004 1605 1612
21. H. Teraoka, H. Minami, S. Iijima, K. Tsukada, O. Koiwai, and T. Date Expression of active human DNA ligase I in Escherichia coli cells that harbor a full-length DNA ligase I cDNA construct J. Biol. Chem. 268 32 1993 24156 24162
22. S. Krishna, D.K. Singh, S. Meena, D. Datta, M.I. Siddiqi, and D. Banerjee Pharmacophore-based screening and identification of novel human ligase I inhibitors with potential anticancer activity J. Chem. Inf. Model. 2014 781 792
23. H. Zhao, Z. Yang, X. Wang, X. Zhang, M. Wang, Y. Wang, Q. Mei, and Z. Wang Triptolide inhibits ovarian cancer cell invasion by repression of matrix metalloproteinase 7 and 19 and upregulation of E-cadherin Exp. Mol. Med. 44 11 2012 633 641
24. R.L.A. Furlan, L.M. Garrido, G. Brumatti, G.P. Amarante-Mendes, R.A. Martins, M.C.R. Facciotti, and G. Padilla A rapid and sensitive method for the screening of DNA intercalating antibiotics Biotechnol. Lett. 24 21 2002 1807 1813
25. J.B. LePecq, and C. Paoletti A fluorescent complex between ethidium bromide and nucleic acids. Physical-chemical characterization J. Mol. Biol. 27 1 1967 87 106
26. G. Ciarrocchi, M. Lestingi, M. Fontana, S. Spadari, and A. Montecucco Correlation between anthracycline structure and human DNA ligase inhibition Biochem. J. 279 Pt 1 1991 141 146
27. A. Montecucco, M. Fontana, F. Focher, M. Lestingi, S. Spadari, and G. Ciarrocchi Specific inhibition of human DNA ligase adenylation by a distamycin derivative possessing antitumor activity Nucleic Acids Res. 19 5 1991 1067 1072
28. D.K. Singh, S. Krishna, S. Chandra, M. Shameem, A.L. Deshmukh, and D. Banerjee Human DNA ligases: a comprehensive new look for cancer therapy Med. Res. Rev. 34 3 2014 567 595
29. X. Chen, S. Zhong, X. Zhu, B. Dziegielewska, T. Ellenberger, G.M. Wilson, A.D. MacKerell Jr., and A.E. Tomkinson Rational design of human DNA ligase inhibitors that target cellular DNA replication and repair Cancer Res. 68 9 2008 3169 3177
30. A.E. Tomkinson, and D.S. Levin Mammalian DNA ligases BioEssays 19 10 1997 893 901
31. M. Srivastava, M. Nambiar, S. Sharma, S.S. Karki, G. Goldsmith, M. Hegde, S. Kumar, M. Pandey, R.K. Singh, P. Ray, R. Natarajan, M. Kelkar, A. De, B. Choudhary, and S.C. Raghavan An inhibitor of nonhomologous end-joining abrogates double-strand break repair and impedes cancer progression Cell 151 7 2012 1474 1487
32. J.J. Wang, Y.K. Shen, W.P. Hu, M.C. Hsieh, F.L. Lin, M.K. Hsu, and M.H. Hsu Design, synthesis, and biological evaluation of pyrrolo[2,1-c] [1,4]benzodiazepine and indole conjugates as anticancer agents J. Med. Chem. 49 4 2006 1442 1449
33. A. Kamal, J.S. Reddy, M.J. Ramaiah, E.V. Bharathi, D. Dastagiri, M.K. Reddy, S.N. Pushpavalli, and M. Pal-Bhadra Synthesis and biological evaluation of anilino substituted pyrimidine linked pyrrolobenzodiazepines as potential anticancer agents Bioorg. Med. Chem. Lett. 20 17 2010 5232 5236
34. K.W. Kohn, and C.L. Spears Reaction of anthramycin with deoxyribonucleic acid J. Mol. Biol. 51 3 1970 551 572
35. K.W. Kohn, D. Glaubiger, and C.L. Spears The reaction of anthramycin with DNA. II. Studies of kinetics and mechanism Biochim. Biophys. Acta 361 3 1974 288 302
36. Y. Nishioka, T. Beppu, M. Kosaka, and K. Arima Mode of action of tomaymycin J. Antibiot. (Tokyo) 25 11 1972 660 667
37. J.H. Petrini, Y. Xiao, and D.T. Weaver DNA ligase I mediates essential functions in mammalian cells Mol. Cell. Biol. 15 8 1995 4303 4308
38. A. Kamal, M.K. Reddy, M.J. Ramaiah, Y.V. Srikanth, Rajender, V.S. Reddy, G.B. Kumar, S.N. Pushpavalli, I. Bag, A. Juvekar, S. Sen, S.M. Zingde, and M. Pal-Bhadra Synthesis of aryl-substituted naphthalene-linked pyrrolobenzodiazepine conjugates as potential anticancer agents with apoptosis-inducing ability ChemMedChem 6 9 2011 1665 1679