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Evidence for a Common Molecular Basis for Sequence Recognition of N3-Guanine and N3-Adenine DNA Adducts Involving the Covalent Bonding Reaction of (+)-CC-1065  

Park, Hyun-Ju (College of Pharmancy, Sungkunkwan University)
Publication Information
Archives of Pharmacal Research / v.25, no.1, 2002 , pp. 11-24 More about this Journal
Abstract
The antitumor antibiotic (+)-CC-1065 can alkylate N3 of guanine in certain sequences. A previous high-field $^1H$ NMR study on the$(+)-CC-1065d[GCGCAATTG*CGC]_2$ adduct ($^*$ indicates the drug alkylation site) showed that drag modification on N3 of guanine results in protonation of the cross-strand cytosine [Park, H-J.; Hurley, L. H. J. Am. Chem. Soc.1997, 119,629]. In this contribution we describe a further analysis of the NMR data sets together with restrained molecular dynamics. This study provides not only a solution structure of the (+)-CC-1065(N3- guanine) DNA duplex adduct but also new insight into the molecular basis for the sequence- specific interaction between (+)-CC-1065 and N3-guanine in the DNA duplex. On the basis of NOESY data, we propose that the narrow minor groove at the 7T8T step and conformational kinks at the junctions of 16C17A and 18A19T are both related to DNA bending in the drugDNA adduct. Analysis of the one-dimensional $^1H$ NMR (in $H_2O$) data and rMD trajectories strongly suggests that hydrogen bonding linkages between the 8-OH group of the (+)-CC-1065 A-sub-unit and the 9G10C phosphate via a water molecule are present. All the phenomena observed here in the (+)-CC-1065(N3-guanine) adduct at 5'$-AATTG^*$are reminiscent of those obtained from the studies on the (+)-CC-1065(N3-adenine) adduct at $5, suggesting that (+)-CC-1065 takes advantage of the conformational flexibility of the 5'-TPu step to entrap the bent structure required for the covalent bonding reaction. This study reveals a common molecular basis for (+)-CC-1065 alkylation at both $5 and $5, which involves a trapping out of sequence-dependent DNA conformational flexibility as well as sequence-dependent general acid and general base catalysis by duplex DNA.
Keywords
(+)-CC-1065; N3-guanine or adenine adduct; Common molecular basis; DNA conformational flexibility; Catalysis by duplex DNA;
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1 Lin, C. H. Use of High-Field NMR in Combination with StableIsotope Labeled Oligomers to Probe the Reaction of (+)-CC-1065 with DNA. Ph.D. dissertation, The University of Texas at Austin, Austin, TX, August (1991)
2 Asai, A., Nagamura, S., and Saito, H. A Novel Property of Duocar-mycin and Its Analogs for Covalent Reaction with DNA. J. Am. Chem. Soc., 116, 4171-4177 (1994)   DOI   ScienceOn
3 Barber, A. M. and Zhurkin, V. B. CAP binding sites reveal pyrimidine-purine pattern characteristic of DNA bending. J. Biomol. Struct. Dyn., 8, 213-232 (1990)   DOI   PUBMED   ScienceOn
4 Boger, D. L., Ishizaki, T, and Zarrinmayeh, H. Isolation and characterization of the duocarmycin-adenine DNA adduct. J. Am. Chem. Soc., 113, 6645-6649 (1991)   DOI
5 Boger, D. L. and Mesini, P. DNA Alkylation Properties of CC1065 and Duocarmycin Analogs Incorporating the 2,3,10, 10a-Tetrahydrocyclopropa[d]benzo[f]quinol-5-one Alkylation Subunit: Identification of Subtle Structural Features That Contribute to the Regioselectivity of the Adenine N3 Alkylation Reaction. J. Am. Chem. Soc., 117, 11647-11655 (1995)   DOI
6 Chuprina, V. P., Lipanov, A. A, Fedoroff, O., Kim, S. G., Kintanar, A., and Reid, B. R. Sequence effects on local DNA topology. Proc. Natl. Acad. Sci. U.S.A., 88, 9087-9091 (1991)   DOI   ScienceOn
7 Churchill, M. E., Jones, D. N., Glaser, T., Hefner, H., Searles, M. A., and Travers, A. A. HMG-D is an architecture-specific protein that preferentially binds to DNA containing the dinucleotide TG. EMBO Journal, 14, 1264-1275(1995)
8 Colson, A. -O., Besler, B., and Sevilla, M. D. Ab initio molecular orbital calculations on DNA base pair radical ions: effect of base pairing on proton-transfer energies, electron affinities, and ionization potentials. J. Phys. Chem., 96, 9787-9794 (1992)   DOI
9 Hassan, M. A. and Calladine, C. R. Two distinct modes of protein-induced bending in DNA. J. Mol. Biol., 282, 331-343 (1998)   DOI   ScienceOn
10 Hutter, M. and Clark, T. On the Enhanced Stability of the Guanine-Cytosine Base-Pair Radical Cation. J. Am. Chem. Soc., 118, 7574-7577 (1996)   DOI   ScienceOn
11 Jencks, W. P. (chapter 3) in Catalysis in Chemistry and Enzymology, Dover, New York, (1987)
12 Katahira, M., Sugeta, H., and Kyogoku, Y. A new model for the bending of DNAs containing the oligo(dA) tracts based on NMR observations. Nucleic Acids Res., 18, 613-618 (1990)   DOI   ScienceOn
13 Kintanar, A., Klevit, R. E., and Reid, B. R. Two-dimensional NMR investigation of a bent DNA fragment: assignment of the proton resonances and preliminary structure analysis. Nucleic Acids Res., 15, 5845-5862 (1987)   DOI   ScienceOn
14 Lam, S. L. and Au-Yeung, S. C. SeqJence-specific local structural variations in solution structures of d$(CGXX`CG)_2$ and d$(CAXX`TG)_2$ self-complementary deoxyribonucleic acids. J. Mol. Biol., 266, 745-60 (1997)   DOI   ScienceOn
15 Lamm, G. and Pack, G.R. Acidic domains around nucleic acids. Proc. Natl. Acad. Sci. U.S.A., 87, 9033-9036 (1990)   DOI   ScienceOn
16 Reynolds, V. L., McGovren, J. P, and Hurley, L. H. The chemistry, mechanism of action and biological properties of CC-1065, a potent antitumor antibiotic. J. Antibiot., 39, 319-334 (1986)   DOI   PUBMED
17 Lee, C. S., Sun, D., Kizu, R., and Hurley, L. H. Determination of the structural features of (+)-CC-1065 that are responsible for bending and winding of DNA. Chem. Res. Toxicol., 4, 203-213 (1991)   DOI   ScienceOn
18 Lin, C. H. and Hurley, L. H. Determination of the major tautomeric form of the covalently modified adenine in the (+)-CC-1065-DNA adduct by 1H and 15N NMR studies. Biochemistry, 29, 9503-9507 (1990)   DOI   ScienceOn
19 Needham-VanDevanter, D. R., Hurley, L. H., Reynolds, V. L., Theriault, N. Y., Krueger, W. C., and Wierenga, W. Characterization of an adduct between CC-1065 and a defined oligodeoxynucleotide duplex. Nucleic Acids Res., 12, 6159-6168 (1984)   DOI   ScienceOn
20 Warpehoski, M. A., Gebhard, I., Kelly, R. C., Krueger, W. C., Li, L. H., McGovren, J. P., Prairie, M. D., Wicnienski, N., and Wierenga, W. Stereoelectronic factors influencing the biological activity and DNA interaction of synthetic antitumor agents modeled on CC-1065. J. Med. Chem., 31, 590-603 (1988)   DOI   PUBMED
21 Warpehoski, M. A. and Hurley, L. H. Sequence selectivity of DNA covalent modification. Chem. Res. Toxicol., 1, 315-333 (1988)   DOI   ScienceOn
22 Warpehoski, M. In Advances in DNA Sequence Specific Agents, Vol. 1; Hurley, L. H., Ed.; JAI Press Inc.: Greenwich, CT, pp 217245 (1992)
23 Warpehoski, M. A., Harper, D. E., Mitchell, M. A., and Monroe T. J. Reversibility of the covalent reaction of CC-1065 and analogues with DNA. Biochemistry, 31, 2502-2508 (1992)   DOI   ScienceOn
24 Nagaich, A. K., Bhattacharyya, D., Brahmachari, S. K., and Bansal, M. CA/TG sequence at the 5' end of oligo(A)-tracts strongly modulates DNA curvature. J. Biol Chem., 269, 7824-7833 (1994)   PUBMED
25 Baird, R. and Winstein, S. Neighboring carbon and hydrogen. LI. Dienones from Ar1q-3 participation. Isolation and behavior of spiro[2,5]octa-1,4-dien-3-one. J. Am. Chem. Soc., 85, 567-578 (1963)   DOI
26 Boger, D. L., Han, N., Tarby, C. M., Boyce, C. W., Cai, H., Jin, Q., and Kitos, P. A. Synthesis, Chemical Properties, and Preliminary Evaluation of Substituted CBI Analogs of CC1065 and the Duocarmycins Incorporating the 7-Cyano-1,2, 9,9a-tetra-hydrocyclopropa[c]benz[e]indol-4-0ne Alkylation Subunit: Hammett Quantitation of the Magnitude of Electronic Effects on Functional Reactivity. J. Org. Chem., 61, 4894-4912 (1996)   DOI   ScienceOn
27 Reynolds, V. L., Molineux, I. J., Kaplan, D. J., Swenson, D. H., and Hurley, L. H. Reaction of the antitumor antibiotic CC1065 with DNA Location of the site of thermally induced strand breakage and analysis of DNA sequence specificity. Biochemistry, 24, 6228-6237 (1985)   DOI   ScienceOn
28 Lee, S. -J., Park, H. -J., and Hurley, L. H. Unpublished results
29 Sugiyama, H., Ohmori, K., Chan, K. L., Hosoda, M., Asai, A., Saito, H., and Saito, I. A novel guanine N3 alkylation by antitumor antibiotic duocarmycin A. Tetrahedron Lett., 34, 2179-2182 (1993)   DOI   ScienceOn
30 Katahira, M., Sugeta, H., Kyogoku, Y., Fujii, S., Fujisawa, R., and Tomita, K. One- and two-dimensional NMR studies on the conformation of DNA containing the oligo(dA)oligo(dT) tract. Nucleic Acids Res., 16, 8619-8632 (1988)   DOI   ScienceOn
31 McNamara, P. T., Bolshoy, A., Trifonov, E. N., and Harrington, R. E. Sequence-dependent kinks induced in curved DNA J. Biomol. Struct. Dyn., 8, 529-538 (1990)   DOI   PUBMED   ScienceOn
32 Martin, D. G., Biles, C., Gerpheide, S. A., Hanka, L. J., Krueger, W. C., McGovren, J. P., Mizsak, S. A., Neil, G. L., Stewart, J. C., and Visser, J. CC-1065 (NSC 298223), a potent new antitumor agent improved production and isolation, characterization and antitumor activity. J. Antibiot., 34, 1119-1125 (1981)   DOI   PUBMED
33 Borgias, B. A., Gochin, M., Kerwood, D. J., and James T L. Relaxation matrix analysis of 2D NMR data. Prog. Nucl. Magn. Reson. Spectrosc., 22, 83100 (1990)
34 Lee, C. -S. and Gibson, N. W. DNA interstrand cross-links induced by the cyclopropylpyrroloindole antitumor agent bizelesin are reversible upon exposure to alkali. Biochemistry, 32, 9108-9114 (1993)   DOI   ScienceOn
35 Borgias, B. A., Thomas, P. D., and James, T.L. Complete Relaxation Analysis (CORMA). University of California, San Francisco, (1989)
36 Hanka, L. J., Dietz, A., Gerpheide, S. A., Kuentzel, S. L., and Martin, D. G. CC-1065 (NSC-298223), a new antitumor antibiotic. Production, in vitro biological activity, microbiological assays and taxonomy of the producing microorganism. J. Antibiot., 31, 1211-1217 (1978)   DOI   PUBMED
37 Hurley, L. H., Warpehoski, M. A., Lee, C. -S., McGovren, J. P, and Scahill, T. A.; Kelly, K. C., Wicnienski, N. A., Gebhard, I., Bradford, V. S. Sequence specificity of DNA alkylation by the unnatural enantiomer of CC-1065 and its synthetic analogs. J. Am. Chem. Soc., 112 ,4633-4649 (1990)   DOI
38 Lin, C. H., Hill, G. C., and Hurley, L. H. Characterization of a 12mer duplexd(GGCGGAGTTAGG).d(CCTAACTCCGCC) containing a highly reactive (+)-CC-1065 sequence by 1Hand 31P NMR, hydroxyl-radical footprinting, and NOESY restrained molecular dynamics calculations. Chem. Res. Toxicol., 5, 167-182 (1992)   DOI   ScienceOn
39 Sun, D., Lin, C. H., and Hurley, L. H. A-tract and (+)-CC-1065 induced bending of DNA. Comparison of structural features using non-denaturing gel analysis, hydroxyl-radical footprinting, and high-field NMR. Biochemistry, 32, 4487-4495 (1993)   DOI   ScienceOn
40 Han, F. X. and Hurley, L. H. A model for the T-antigen-induced structural alteration of the SV40 replication origin based upon experiments with specific probes for bent, straight, and unwound DNA. Biochemistry, 35, 7993-8001 (1996)   DOI   ScienceOn
41 Schowen, R. L. (chapter 2), and Maggiora, G. and Christoffersen, R. (chapter 3), in Transition States of Biochemical Processes, eds. Gandour, R. and Schowen, R. L., Plenum, New York, (1978)
42 Park, H. -J. and Hurley, L. H. Covalent Modification of N3 of Guanine by (+)-CC-1065 Results in Protonation of the Cross-Strand Cytosine. J. Am. Chem. Soc., 119, 629-630 (1997)   DOI   ScienceOn
43 Colominas, C., Luque, F. J., and Orozco, M. Tautomerism and Protonation of Guanine and Cytosine. Implications in the Formation of Hydrogen-Bonded Complexes. J. Am. Chem. Soc., 118, 6811-6821 (1996)   DOI   ScienceOn
44 Mergny, J. -L., Lacroix, L., Han, X., Leroy, J -L., and Helene, C. Intramolecular Folding of Pyrimidine Oligodeoxynucleotides into an i-DNA Motif. J. Am. Chem. Soc., 117, 8887-8898 (1995)   DOI   ScienceOn
45 Boger, D. L. and Garbaccio, R. M., Jin, Q. Synthesis and Evaluation of CC-1065 and Duocarmycin Analogs Incorporating the Iso-CI and Iso-CBI Alkylation Subunits: Impact of Relocation of the C-4 Carbonyl. J. Org. Chem., 62, 8875-8891 (1997)   DOI   ScienceOn
46 Hurley, L. H., Reynolds, V. L., Swenson, D. H., Petzold, G. L., and Scahill, T. A. Reaction of the antitumor antibiotic CC1065 with DNA: structure of a DNA adduct with DNA sequence specificity. Science, 226, 843-844 (1984)   DOI   PUBMED
47 Nadeau, J. G. and Crothers, D. M. Structural basis for DNA bending. Proc. Natl. Acad. Sci. U.S.A., 86, 2622-2626 (1989)   DOI   ScienceOn
48 Sugiyama, H., Lian, C., Isomura, M., Saito, I., and Wang, A. H. Distamycin A modulates the sequence specificity of DNA alkylation by duocarmycin A Proc. Natl Acad. Sci. U.S.A., 93, 14405-14410 (1996)   DOI   ScienceOn
49 Sun, D., Hurley, L. H. Cooperative bending of the 21-base-pair repeats of the SV40 viral early promoter by human Sp1. Biochemistry, 33, 9578-9587 (1994)   DOI   ScienceOn
50 Lin, C. H. and Patel, D. J. SOlution structure of the covalent duocarmycin A-DNA duplex complex. J. Mol. Biol., 248, 162-179 (1995)   DOI   ScienceOn
51 Mujeeb, A, Kerwin, S. M., Kenyon, G. L., and James, T L. Solution structure of a conserved DNA sequence from the HIV-1 genome: restrained molecular dynamics simulation with distance and torsion angle restraints derived from two-dimensional NMR spectra. Biochemistry, 32, 13419-13431 (1993)   DOI   ScienceOn
52 Radhakrishnan, I., Gao, X., Santos, C. d. I., Live, D., and Patel, D. J. NMR structural studies of intramolecular (Y+)$_n$(R+)$_n$(Y-)$_n$DNA triplexes in solution: imino and amino proton and nitrogen markers of G.TA base triple formation. Biochemistry, 30, 9022-9030 (1991)   DOI   ScienceOn
53 Robinson, H. and Wang, A. H. 5'-CGA sequence is a strong motif for homo base-paired parallel-stranded DNA duplex as revealed by NMR analysis. Proc. Natl. Acad. Sci. U.S.A., 90, 5224-5228 (1993)   DOI   ScienceOn
54 Takahashi, I., Takahashi, K., Ichimura, M., Morimoto, M., Asano, K., Kawamoto, I., Tomita, F., and Nakano, H. Duocarmycin A, a new antitumor antibiotic from Streptomyces. J. Antibiot., 41, 1915-1917 (1988)   DOI   PUBMED
55 Warpehoski, M. A. and Harper, D. E. Acid-Dependent Electrophilicity of Cydopropylpyrroloindoles. Nature's Masking Strategy for a Potent DNA Alkylator. J. Am. Chem. Soc., 116, 7573-7580 (1994)   DOI   ScienceOn
56 Yuan, Y. -C., Seaman, F. C., Hurley, L. H. Unpublishec results
57 Hassan, M. A. and Calladine, C. R. Propeller-twisting of basepairs and the conformational mobility of dinucleotide steps in DNA. J. Mol. Biol., 259, 95-103 (1996)   DOI   ScienceOn
58 Mitchell, M. A., Weiland, K. L., Aristoff, P.A., Johnson, P. D., and Dooley, T P. Sequence-selective guanine reactivity by duocarmycin A. Chem. Res. Toxicol., 6, 421-424 (1993)   DOI   ScienceOn
59 Pearlman, D. A., Case, D. A., Caldwell, J. W., Ross, W. S., Cheatham, T. E., Ferguson, D. M., Seibel, G. L., Singh, C., Weiner, P. K., and Kollman, P. A AMBER 4.1, University of California: San Francisco, (1995)
60 Ichimura, M., Ogawa, T., Katsumata, S., Takahashi, K., Takahashi, I., and Nakano, H. Duocarmycins, new antitumor antibiotics produced by Streptomyces; producing organisms and improved production. J. Antibiot., 44, 1045-1053 (1991)   DOI   PUBMED
61 Weisz, K., Shafer, R. H., Egan, W., anc James, T. L. Solution structure of the octamer motif in immunoglobulin genes via restrained molecular dynamics calculations. Biochemistry, 33, 354-366 (1994)   DOI   ScienceOn
62 Lin, C. H., Beale, J. M., and Hurley, L. H. Structure of 곧 (+)-CC-1065-DNA adduct: critical role of ordered water molecules and implications for involvement of phosphate catalysis in the covalent reaction. Biochemistry, 30, 3597-3602 (1991)   DOI   ScienceOn
63 Radhakrishnan, I., Patel, D. J., Priestly, E. S., Nash, H. M., and Dervan, P. B. NMR structural studies on a nonnatural deoxyribonucleoside which mediates recognition of GC base pairs in pyrimidine-purine-pyrimidine DNA triplexes. Biochemistry, 32, 11228-11234 (1993)   DOI   ScienceOn
64 Hurley, L. H. and Draves, P. H. In Molecular Aspects of Anticancer DrugDNA Interactions; Vol. 2; Neidle, S., Waring, M. J., Eds.; The Macmillan Press Ltd., London, pp 89133 (1993)
65 Boger, D. L. and Turnbull, P. Synthesis and Evaluation of CC1065 and Duocarmycin Analogs Incorporating the 1,2,3,4, 11, 11a-Hexahydrocyclopropa[c]naphtho[2,1-b]azepin-6-one (CNA) Alkylation Subunit: Structural Features that Govern Reactivity and Reaction Regioselectivity. J. Org. Chem., 62, 5849-5863 (1997)   DOI   ScienceOn
66 Krueger, W. C. and Prairie, M. D. A circular dichroism study of the binding of CC-1065 to B and Z form poly(dl-5BrdC). poly(dl-5BrdC). Chem. -Biol. Interact., 62, 281-295 (1987)   DOI   ScienceOn
67 Santos, C. d. I., Rosen, M., and Patel, D. NMR studies of DNA (R+)n.(Y-)n.(Y+)n triple helices in solution: imino and amino proton markers of T.A.T and C.G.C+ base-triple formation. Biochemistry, 28, 7282-7289 (1989).   DOI   ScienceOn
68 Asai, A., Nagamura, S., Saito, H., Takahashi, I., and Nakano,H. The reversible DNA-alkylating activity of duocarmycin and its analogues. Nucleic Acids Res., 22, 88-93 (1994)   DOI   ScienceOn
69 Warpehoski, M. A. and Harper, D. E. Enzyme-like Rate Acceleration in the DNA Minor Groove. Cyclopropylpyrroloindoles as Mechanism-Based Inactivators of DNA. J. Am. Chem. Soc., 117, 2951-2952 (1995)   DOI   ScienceOn
70 Yamamoto, K., Sugiyama, H., and Kawarishi, S. Concerted DNA recognition and novel site-specific alkylation by duocarmycin A with distamycin A. Biochemistry, 32, 1059-1066 (1993)   DOI   ScienceOn
71 Schultz, S. C., Shields, G. C., and Steitz, T. A. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science, 253, 1001-1007 (1991)   DOI   PUBMED   ScienceOn
72 Kim, S. -G. and Reid, B. R. Solution structure of the TnAn DNA duplex GCCGTIAACGCG containing the Hpal restriction site. Biochemistry, 31, 12103-12116 (1992)   DOI   ScienceOn
73 Rohozinski, J., Hancock, J. M., and Keniry, M. A. Polycytosine regions contained in DNA hairpin loops interact via a fourstranded, parallel structure similar to the i-motif. Nucleic Acids Res., 22, 4653-4659 (1994)   DOI   ScienceOn
74 Lin, C. H. and Sun, D., Hurley, L. H. (+)-CC-1065 produces bending of DNA that appears to resemble adenine/thymine tracts. Chem. Res. Toxicol., 4, 21-26 (1991)   DOI   ScienceOn
75 Krueger, W. C., Li, L. H., Moscowitz, A.., Prairie, M. D., Petzold, G., and Swenson, D. H. Binding of CC-1065 to poly- and oligonucleotides. Biopolymers, 24, 1549-1572 (1985)   DOI   ScienceOn