NMR solution structure of an oxaliplatin 1,2-d(GG) intrastrand cross-link in a DNA dodecamer duplex

Journal of Molecular Biology

Volumn 341, Issue 5, 2004, Pages 1251-1269

  Wu, Yibing ^a   Pradhan, Padmanava ^a   Havener, Jody ^a   Boysen, Gunnar ^b   Swenberg, James A ^b,c   Campbell, Sharon L ^a,c   Chaney, Stephen G ^a,c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b IL   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

cisplatin; DNA adducts; NMR; oxaliplatin; solution structure

Indexed keywords

ADENINE; CISPLATIN; CYTOSINE; DNA; GUANINE; OXALIPLATIN; PROTON;

ARTICLE; BASE PAIRING; CALCULATION; CONFORMATION; CROSS LINKING; DNA SEQUENCE; DRUG STRUCTURE; ENERGY; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; SIMULATION;

EID: 4143141245     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.06.066     Document Type: Article

References (66)

1. M.H. Greene Is cisplatin a human carcinogen J. Nature Cancer Inst. 84 1992 306 312
2. B.J.S. Sanderson, L.R. Ferguson, and W.A. Denny Mutagenic and carcinogenic properties of platinum-based anticancer drugs Mutat. Res-Fundam. Mol. Mech. Mut. 355 1996 59 70
3. S.W. Johnson, R.F. Ozols, and T.C. Hamilton Mechanisms of drug resistance in ovarian cancer Cancer 71 1993 644 649
4. B.T. Hill Drug resistance: an overview of the current state of the art Int. J. Oncol. 9 1996 197 203
5. M. Kartalou, and J.M. Essigmann Mechanisms of resistance to cisplatin Mutat. Res. 478 2001 23 43
6. S.G. Chaney, and A. Vaisman Specificity of platinum-DNA adduct repair J. Inorg. Biochem. 77 1999 71 81
7. O. Rixe, W. Ortuzar, M. Alvarez, R. Parker, E. Reed, K. Paull, and T. Fojo Oxaliplatin, tetraplatin, cisplatin, and carboplatin: spectrum of activity in drug-resistant cell lines and in the cell lines of the National Cancer Institute's Anticancer Drug Screen panel Biochem. Pharmacol. 52 1996 1855 1865
8. Y. Kidani Oxaliplatin Drugs Future 14 1989 529 532
9. W.R. Leopold, R.P. Batzinger, E.C. Miller, J.A. Miller, and R.H. Earhardt Mutagenicity, tumorigenicity, and electrophilic reactivity of the stereoisomeric platinum(II) complexes of 1, 2-diaminocyclohexane Cancer Res. 41 1981 4368 4377
10. S. Aebi, B. Kurdihaidar, R. Gordon, B. Cenni, H. Zheng, and D. Fink Loss of DNA mismatch repair in acquired resistance to cisplatin Cancer Res. 56 1996 3087 3090
11. D. Fink, S. Nebel, S. Aebi, H. Zheng, B. Cenni, and A. Nehme The role of mismatch repair in platinum drug resistance Cancer Res. 56 1996 4881 4886
12. D. Fink, H. Zheng, S. Nebel, P.S. Norris, S. Aebi, and T.-P. Lin In vitro and in vivo resistance to cisplatin in cells that have lost DNA mismatch repair Cancer Res. 57 1997 1841 1845
13. J.T. Drummond, A. Anthoney, R. Brown, and P. Modrich Cisplatin and adriamycin resistance are associated with MutL alpha and mismatch repair deficiency in an ovarian tumor cell line J. Biol. Chem. 271 1996 19645 19648
14. A. Nehme, R. Baskaran, S. Aebi, D. Fink, S. Nebel, B. Cenni, and J.Y.J. Wang Differential induction of c-Jun NH2-terminal kinase and c-Abl kinase in DNA mismatch repair-proficient and deficient cells exposed to cisplatin Cancer Res. 57 1997 3253 3257
15. A. Nehme, R. Baskaran, S. Nebel, D. Fink, S.B. Howell, J.Y.J. Wang, and R.D. Christen Induction of JNK and c-Abl signalling by cisplatin and oxaliplatin in mismatch repair-proficient and -deficient cells Br. J. Cancer 79 1999 1104 1110
16. A. Vaisman, M. Varchenko, A. Umar, T.A. Kunkel, J.I. Risinger, and J.C. Barrett The role of hMLH1, hMSH3, and hMSH6 defects in cisplatin and oxaliplatin resistance: correlation with replicative bypass of platinum-DNA adducts Cancer Res. 58 1998 3579 3585
17. Z.Z. Zdraveski, J.A. Mello, C.K. Farinelli, J.M. Essigmann, and M.G. Marinus MutS preferentially recognizes cisplatin- over oxaliplatin-modified DNA J. Biol. Chem. 277 2002 1255 1260
18. G.R. Gibbons, W.K. Kaufmann, and S.G. Chaney Role of DNA replication in carrier-ligand-specific resistance to platinum compounds in L1210 cells Carcinogenesis 12 1991 2253 2257
19. E.L. Mamenta, E.E. Poma, W.K. Kaufmann, D.A. Delmastro, H.L. Grady, and S.G. Chaney Enhanced replicative bypass of platinum-DNA adducts in cisplatin-resistant human ovarian carcinoma cell lines Cancer Res. 54 1994 3500 3505
20. A. Vaisman, S.E. Lim, S.M. Patrick, W.C. Copeland, D.C. Hinkle, J.J. Turchi, and S.G. Chaney Effect of DNA polymerases and high mobility group protein 1 on the carrier ligand specificity for translesion synthesis past platinum-dna adducts Biochemistry 38 1999 11026 11039
21. A. Vaisman, and S.G. Chaney The efficiency and fidelity of translesion synthesis past cisplatin and oxaliplatin GpG adducts by human DNA polymerase beta J. Biol. Chem. 275 2000 13017 13025
22. A. Vaisman, C. Masutani, F. Hanaoka, and S.G. Chaney Efficient translesion replication past oxaliplatin and cisplatin GpG adducts by human DNA polymerase eta Biochemistry 39 2000 4575 4580
23. J.M. Havener, S.A. McElhinny, E. Bassett, M. Gauger, D.A. Ramsden, and S.G. Chaney Translesion synthesis past platinum DNA adducts by human DNA polymerase mu Biochemistry 42 2003 1777 1788
24. M. Wei, S.M. Cohen, A.P. Silverman, and S.J. Lippard Effects of spectator ligands on the specific recognition of intrastrand platinum-DNA cross-links by high mobility group box and TATA-binding proteins J. Biol. Chem. 276 2001 38774 38780
25. X. Zhai, H. Beckmann, H.-M. Jantzen, and J.M. Essigmann Cisplatin-DNA adducts inhibit ribosomal RNA synthesis by hijacking the transcription factor human upstream binding factor Biochemistry 37 1998 16307 16315
26. J.C. Huang, D.B. Zamble, J.T. Reardon, S.J. Lippard, and A. Sancar HMG-domain proteins specifically inhibit the repair of the major DNA adduct of the anticancer drug cisplatin by human excision nuclease Proc. Natl Acad. Sci. USA 91 1994 10394 10398
27. M.M. Mcanulty, and S.J. Lippard The HMG-domain protein Ixr1 blocks excision repair of cisplatin-DNA adducts in yeast Mutat. Res.-DNA Repair 362 1996 75 86
28. J.S. Hoffmann, D. Locker, G. Viliani, and M. Leng HMG1 protein inhibits the translesion synthesis of the major DNA cisplatin adduct by cell extracts J. Mol. Biol. 270 1997 539 543
29. D.K. Treiber, X.Q. Zhai, H.M. Jantzen, and J.M. Essigmann Cisplatin-DNA adducts are molecular decoys for the ribosomal RNA transcription factor hUBF (human upstream binding factor) Proc. Natl Acad. Sci. USA 91 1994 5672 5676
30. J.D. Page, I. Husain, A. Sancar, and S.G. Chaney Effect of the diaminocyclohexane carrier ligand on platinum adduct formation, repair, and lethality Biochemistry 29 1990 1016 1024
31. M.M. Jennerwein, A. Eastman, and A.R. Khokhar Characterization of adducts produced in DNA by isomeric 1, 2-diaminocyclohexaneplatinum(II) complexes Chem.-Biol. Interact. 70 1989 39 49
32. J.M. Woynarowski, W.G. Chapman, C. Napier, M.C.S. Herzig, and P. Juniewicz Sequence- and region-specificity of oxaliplatin adducts in naked and cellular DNA Mol. Pharmacol. 54 1998 770 777
33. A. Eastman The formation, isolation and characterization of DNA adducts produced by anticancer platinum complexes Pharmacol. Ther. 34 1987 155 166
34. P.M. Takahara, C.A. Frederick, and S.J. Lippard Crystal structure of the anticancer drug cisplatin bound to duplex DNA J. Am. Chem. Soc. 118 1996 12309 12321
35. B. Spingler, D.A. Whittington, and S.J. Lippard 2.4 crystal structure of an oxaliplatin 1,2-d(GpG) intrastrand cross-link in a DNA dodecamer duplex Inorg. Chem. 40 2001 5596 5602
36. M.H. Lamers, A. Perrakis, J.H. Enzlin, H.H.K. Winterwerp, N. de Wind, and T.K. Sixma The crystal structure of DNA mismatch repair protein MutS binding to a G center dot T mismatch Nature 407 2000 711 717
37. G. Obmolova, C. Ban, P. Hsieh, and W. Yang Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA Nature 407 2000 703 710
38. U.M. Ohndorf, M.A. Rould, Q. He, C.O. Pabo, and S.J. Lippard Basis for recognition of cisplatin-modified DNA by high-mobility-group proteins Nature 399 1999 708 712
39. M.R. Sawaya, R. Prasad, S.H. Wilson, J. Kraut, and H. Pelletier Crystal structures of human DNA polymerase beta complexed with gapped and nicked DNA: evidence for an induced fit mechanism Biochemistry 36 1997 11205 11215
40. F. Herman, J. Kozelka, V. Stoven, E. Guittet, J.P. Girault, T. Huynh-Dinh, and J. Igolen A d(GpG)-platinated decanucleotide duplex is kinked An extended NMR and molecular mechanics study Eur. J. Biochem. 194 1990 119 133
41. D. Yang, S.S.G.E. van Bloom, J. Reedijk, J.H. van Bloom, and A.H.J. Wang Structure and isomerization of an intrastrand cisplatin-cross-linked octamer DNA duplex by NMR analysis Biochemistry 34 1995 12912 12920
42. A. Gelasco, and S.J. Lippard NMR solution structure of a DNA dodecamer duplex containing a cis-diammineplatinum(II) dGpG intrastrand cross-link, the major adduct of the anticancer drug cisplatin Biochemistry 37 1998 9230 9239
43. L.G. Marzilli, J.S. Saad, Z. Kuklenyik, K.A. Keating, and Y. Xu Relationship of solution and protein-bound structures of DNA duplexes with the major intrastrand cross-link lesions formed on cisplatin binding to DNA J. Am. Chem. Soc. 123 2001 2764 2770
44. M.A. Elizondo-Riojas, and J. Kozelka Unrestrained 5 ns molecular dynamics simulation of a cisplatin-DNA 1, 2-GG adduct provides a rationale for the NMR features and reveals increased conformational flexibility at the platinum binding site J. Mol. Biol. 314 2001 1227 1243
45. G.J. Bubley, B.P. Ashburner, and B.A. Teicher Spectrum of cis-diamminedichloroplatinum(II)-induced mutations in a shuttle vector propagated in human cells Mol. Carcinog. 4 1991 397 406
46. J.G. de Boer, and B.W. Glickman Sequence specificity of mutations induced by the antitumor drug cisplatin in the CHO aprt gene Carcinogenesis 10 1989 1363 1367
47. J.G. de Boer, and B.W. Glickman Mutations recovered in the chinese hamster aprt gene after exposure to carboplatin - a comparison with cisplatin Carcinogenesis 13 1992 15 17
48. M.J. Pillaire, A. Margot, G. Villani, A. Sarasin, M. Defais, and A. Gentil Mutagenesis in monkey cells of a vector containing a single d(GPG) cis-diamminedichloroplatinum(II) adduct placed on codon 13 of the human H-ras proto-oncogene Nucl. Acids Res. 22 1994 2519 2524
49. D.S. Pilch, S.U. Dunham, E.R. Jamieson, S.J. Lippard, and K.J. Breslauer DNA sequence context modulates the impact of a cisplatin 1,2-d(GpG) intrastrand cross-link on the conformational and thermodynamic properties of duplex DNA J. Mol. Biol. 296 2000 803 812
50. A. Eastman Reevaluation of the interactions of cis- diamminedichloro(ethylenediamine)platinum(II) with DNA Biochemistry 25 1986 3912 3915
51. Wuthrich, K. (1986) NMR of Proteins and Nucleic Acids Wiley New York.
52. 1H resonances in oligonucleotides by two-dimensional NMR spectroscopy FEBS Letters 208 1986 94 98
53. X. Chen, J.A. McDowell, R. Kierzek, T.R. Krugh, and D.H. Turner Nuclear magnetic resonance spectroscopy and molecular modeling reveal that different hydrogen bonding patterns are possible for G.U pairs: one hydrogen bond for each G.U pair in r(GGCGUGCC)(2) and two for each G.U pair in r(GAGUGCUC)(2) Biochemistry 39 2000 8970 8982
54. Wijmenga, S. S., Mooren, M. M. W. & Hilbers, C. W. (1993) NMR of nucleic acids, from spectrum to structure. In NMR of Macromolecules. A Practical Approach (Roberts, G. C. K., ed), pp. 217-288, Oxford University Press, New York
55. R.J. Isaacs, and H.P. Spielmann Relationship of DNA structure to internal dynamics: correlation of helical parameters from NOE-based NMR solution structures of d(GCGTACGC)(2) and d(CGCTAGCG)(2) with (13)C order parameters implies conformational coupling in dinucleotide units J. Mol. Biol. 307 2001 525 540
56. X.J. Lu, and W.K. Olson 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures Nucl. Acids Res. 31 2003 5108 5121
57. A. Barbic, and D.M. Crothers Comparison of analyses of DNA curvature J. Biomol. Struct. Dyn. 21 2003 89 97
58. S.L. Lam, I.L. Nang, X. Cui, and H.C. Nang Random coil proton chemical shifts of deoxyribonucleic acids J. Biomol. NMR 24 2002 329 337
59. A. Travers Recognition of distorted DNA structures by HMG domains Curr. Opin. Struct. Biol. 10 2000 102 109
60. 1H resonances of protein side chains contacting DNA J. Magn. Reson. 135 1998 87 92
61. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
62. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallog. sect. D. 54 1998 905 921
63. E.D. Scheeff, J.M. Briggs, and S.B. Howell Molecular modeling of the intrastrand guanine-guanine DNA adducts produced by cisplatin and oxaliplatin Mol. Pharmacol. 56 1999 633 643
64. J. Kuszewski, C. Schwieters, and G.M. Clore Improving the accuracy of NMR structures of DNA by means of a database potential of mean force describing base-base positional interactions J. Am. Chem. Soc. 123 2001 3903 3918
65. R. Koradi, M. Billeter, and K. Wuthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 51 55
66. X.J. Lu, Z. Shakked, and W.K. Olson A-form conformational motifs in ligand-bound DNA structures J. Mol. Biol. 300 2000 819 840