The Library

Combined theoretical and computational study of interstrand DNA guanine–guanine cross-linking bytrans-[Pt(pyridine)2] derived from the photoactivated prodrugtrans,trans,trans-[Pt(N3)2(OH)2(pyridine)2]

Tools

Tai, Hui-Chung, Brodbeck, Ralf, Kasparkova, Jana, Farrer, Nicola J., Brabec, V. (Viktor), Sadler, P. J. and Deeth, Robert J.. (2012) Combined theoretical and computational study of interstrand DNA guanine–guanine cross-linking bytrans-[Pt(pyridine)2] derived from the photoactivated prodrugtrans,trans,trans-[Pt(N3)2(OH)2(pyridine)2]. Inorganic Chemistry, Vol.51 (No.12). pp. 6830-6841. ISSN 0020-1669

Preview

Text
WRAP_Tai_488_InorgChem_2012_Tai_diposit.pdf - Accepted Version
Download (2266Kb) | Preview

Official URL: http://dx.doi.org/10.1021/ic3005745

Abstract

Molecular modeling and extensive experimental studies are used to study DNA distortions induced by binding platinum(II)-containing fragments derived from cisplatin and a new class of photoactive platinum anticancer drugs. The major photoproduct of the novel platinum(IV) prodrug trans,trans,trans-[Pt(N3)2(OH)2(py)2] (1) contains the trans-{Pt(py)2}2+ moiety. Using a tailored DNA sequence, experimental studies establish the possibility of interstrand binding of trans-{Pt(py)2}2+ (P) to guanine N7 positions on each DNA strand. Ligand field molecular mechanics (LFMM) parameters for Pt–guanine interactions are then derived and validated against a range of experimental structures from the Cambridge Structural Database, published quantum mechanics (QM)/molecular mechanics (MM) structures of model Pt–DNA systems and additional density-functional theory (DFT) studies. Ligand field molecular dynamics (LFMD) simulation protocols are developed and validated using experimentally characterized bifunctional DNA adducts involving both an intra- and an interstrand cross-link of cisplatin. We then turn to the interaction of P with the DNA duplex dodecamer, d(5′-C1C2T3C4T5C6G7T8C9T10C11C12-3′)·d(5′-G13G14A15G16A17C18G19A20G21A22G23G24-3′) which is known to form a monofunctional adduct with cis-{Pt(NH3)2(py)}. P coordinated to G7 and G19 is simulated giving a predicted bend toward the minor groove. This is widened at one end of the platinated site and deepened at the opposite end, while the P–DNA complex exhibits a global bend of 67° and an unwinding of 20°. Such cross-links offer possibilities for specific protein–DNA interactions and suggest possible mechanisms to explain the high potency of this photoactivated complex.

Item Type:

Journal Article

Subjects:

Q Science > QD Chemistry
Q Science > QP Physiology

Divisions:

Faculty of Science > Chemistry

Library of Congress Subject Headings (LCSH):

DNA-protein interactions, Molecular dynamics -- Simulation methods, G proteins, Antineoplastic agents, Cisplatin, DNA adducts

Journal or Publication Title:

Inorganic Chemistry

Publisher:

American Chemical Society

ISSN:

0020-1669

Official Date:

2012

Dates:

Date	Event
2012	Published

Volume:

Vol.51

Number:

No.12

Page Range:

pp. 6830-6841

Identification Number:

10.1021/ic3005745

Status:

Peer Reviewed

Publication Status:

Published

Access rights to Published version:

Restricted or Subscription Access

Funder:

Overseas Research Students Awards Scheme (ORSAS), University of Warwick Postgraduate Research Scholarship, Engineering and Physical Sciences Research Council (EPSRC), European Research Council (ERC), Grantová agentura České republiky [Grant Agency of the Czech Republic] (GACR), Advantage West Midlands (AWM)

Grant number:

EP/F042159 (EPSRC), 247450 (ERC), P301/10/0598 (GACR)

References:

(1) Wong, E.; Giandomenico, C. Chem. Rev. 1999, 99, 2451.
(2) Kelland, L. Nat. Rev. Cancer 2007, 7, 573.
(3) Blindauer, C. A.; Harvey, I.; Bunyan, K. E.; Stewart, A. J.; Sleep, D.; Harrison, D. J.; Berezenko, S.;
Sadler, P. J. J. Biol. Chem. 2009, 284, 23116.
(4) Deubel, D. V.; Lau, J. K. C. Chem. Commun. 2006, 2451.
(5) Reedijk, J. Platinum Met. Rev. 2008, 52, 2.
(6) Jamieson, E. R.; Lippard, S. J. Chem. Rev. 1999, 99, 2467.
(7) Baik, M. H.; Friesner, R. A.; Lippard, S. J. J. Am. Chem. Soc. 2003, 125, 14082.
(8) Mantri, Y.; Lippard, S. J.; Baik, M. H. J. Am. Chem. Soc. 2007, 129, 5023.
(9) Deubel, D. V. J. Am. Chem. Soc. 2006, 128, 1654.
(10) Reedijk, J. Chem. Rev. 1999, 99, 2499.
(11) Jung, Y.; Lippard, S. J. Chem. Rev. 2007, 107, 1387.
(12) Fuertes, M.; Alonso, C.; Perez, J. Chem. Rev. 2003, 103, 645.
(13) Bradley, L. J. N.; Yarema, K. J.; Lippard, S. J.; Essigmann, J. M. Biochemistry 1993, 32, 982.
(14) Coste, F.; Malinge, J.; Serre, L.; Shepard, W.; Roth, M.; Leng, M.; Zelwer, C. Nucleic Acids Res. 1999,
27, 1837.
(15) Gelasco, A.; Lippard, S. J. Biochemistry 1998, 37, 9230.
(16) Elizondo-Riojas, M. A.; Kozelka, J. J. Mol. Biol. 2001, 314, 1227.
(17) Zhu, Y. Y.; Wang, Y.; Chen, G. J. Nucleic Acids Res. 2009, 37, 5930.
(18) Teletchea, S.; Skauge, T.; Sletten, E.; Kozelka, J. Chem. Eur. J. 2009, 15, 12320.
(19) Barnham, K. J.; Bernersprice, S. J.; Frenkiel, T. A.; Frey, U.; Sadler, P. J. Angew. Chem. Int. Ed. 1995,
34, 1874.
(20) Parkinson, J. A.; Chen, Y.; Murdoch, P. D.; Guo, Z. J.; Berners-Price, S. J.; Brown, T.; Sadler, P. J.
Chem. Eur. J. 2000, 6, 3636.
(21) Chen, Y.; Parkinson, J. A.; Guo, Z. J.; Brown, T.; Sadler, P. J. Angew. Chem. Int. Ed. 1999, 38, 2060.
(22) Farrer, N. J.; Woods, J. A.; Salassa, L.; Zhao, Y.; Robinson, K. S.; Clarkson, G.; Mackay, F. S.; Sadler,
P. J. Angew. Chem. Int. Ed. 2010, 8905.
(23) Natile, G.; Coluccia, M. Coord. Chem. Rev. 2001, 216, 383.
(24) Mackay, F. S.; Woods, J. A.; Heringova, P.; Kasparkova, J.; Pizarro, A. M.; Moggach, S. A.; Parsons,
S.; Brabec, V.; Sadler, P. J. Proc. Natl. Acad. Sci. USA 2007, 104, 20743.
(25) Wu, B.; Davey, C. A. Chem. Biol. 2008, 15, 1023.
(26) Ober, M.; Lippard, S. J. J. Am. Chem. Soc 2008, 130, 2851.
(27) Ober, M.; Lippard, S. J. J. Am. Chem. Soc. 2007, 129, 6278.
(28) Galea, A. M.; Murray, V. Chem. Biol. Drug Design 2010, 75, 578.
(29) Allen, M.; Tildesley, D. Computer simulation of liquids; Oxford University Press, USA, 1990.
(30) Hambley, T. W.; Jones, A. R. Coord. Chem. Rev. 2001, 212, 35.(31) Burton, V. J.; Deeth, R. J.; Kemp, C. M.; Gilbert, P. J. J. Am. Chem. Soc. 1995, 117, 8407.
(32) Deeth, R. J. Coord. Chem. Rev. 2001, 212, 11.
(33) Deeth, R.; Anastasi, A.; Diedrich, C.; Randell, K. Coord. Chem. Rev. 2009, 253, 795.
(34) Piquemal, J. P.; Williams-Hubbard, B.; Fey, N.; Deeth, R. J.; Gresh, N.; Giessner-Prettre, C. J.
Comput. Chem. 2003, 24, 1963.
(35) Woodley, S. M.; Battle, P. D.; Catlow, C. R. A.; Gale, J. D. J. Phys. Chem. B 2001, 105, 6824.
(36) Deeth, R. J. Chem. Commun. 2006, 2551.
(37) Chval, Z.; Sip, M. J. Phys. Chem. B 1998, 102, 1659.
(38) Anastasi, A.; Deeth, R. J. J. Chem. Theory. Comput. 2009, 5, 2339.
(39) Noll, D. M.; Mason, T. M.; Miller, P. S. Chem. Rev. 2006, 106, 277.
(40) E.J. Baerends, et al. Amsterdam Density Functional 2007.01, SCM, Vrije Universiteit, Amsterdam,
The Netherlands: Amsterdam, 2007.
(41) Becke, A. Phys. Rev. A 1988, 38, 3098.
(42) Perdew, J. Phys. Rev. B 1986, 33, 8822.
(43) Grimme, S. J. Comp. Chem. 2004, 25, 1463.
(44) van Lenthe, E.; Ehlers, A.; Baerends, E. J. Chem. Phys. 1999, 110, 8943.
(45) Chirlian, L. E.; Francl, M. M. J. Comput. Chem. 1987, 8, 894.
(46) Frisch, M.; Trucks, G.; Schlegel, H.; Scuseria, G.; Robb, M.; Cheeseman, J.; Montgomery Jr, J.;
Vreven, T.; Kudin, K.; Burant, J. In Gaussian 2003; Revision B. 05, Gaussian, Inc.: Pittsburgh, PA, 2003.
(47) Hay, P. J.; Wadt, W. R. J. Chem. Phys. 1985, 82, 299.
(48) Ehlers, A.; Böhme, M.; Dapprich, S.; Gobbi, A.; Höllwarth, A.; Jonas, V.; Köhler, K.; Stegmann, R.;
Veldkamp, A.; Frenking, G. Chem. Phys. Lett. 1993, 208, 111.
(49) Figgis, B. N.; Hitchman, M. A. Ligand field theory and its applications; Wiley-VCH: New York [etc.],
2000.
(50) Deeth, R. J.; Foulis, D. L. PCCP 2002, 4, 4292.
(51) Deeth, R. J.; Fey, N.; Williams-Hubbard, B. J. J. Comp. Chem. 2005, 26, 123.
(52) A copy of DommiMOE can be obtained from the authors. Certain conditions apply.
(53) Halgren, T. A. J. Comput. Chem. 1996, 17, 490.
(54) Halgren, T. A. J. Comput. Chem. 1996, 17, 520.
(55) Halgren, T. A. J. Comput. Chem. 1996, 17, 553.
(56) Halgren, T. A.; Nachbar, R. B. J. Comput. Chem. 1996, 17, 587.
(57) Halgren, T. A. J. Comput. Chem. 1996, 17, 616.
(58) Pearlman, D. A.; Case, D. A.; Caldwell, J. W.; Ross, W. S.; Cheatham, T. E.; DeBolt, S.; Ferguson, D.;
Seibel, G.; Kollman, P. Comput. Phys. Commun. 1995, 91, 1.
(59) Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. J.
Comput. Chem. 1983, 4, 187.
(60) Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. J. Comput. Phys. 1977, 23, 327.
(61) Smith, W.; Yong, C. W.; Rodger, P. M. Mol. Sim. 2002, 28, 385.(62) DL_POLY_LF implements the standard molecular form of LFMM as described in reference 61. Stress
tensor components are computed for all interactions except the d-electron energy.
(63) Lovejoy, K. S.; Todd, R. C.; Zhang, S. Z.; McCormick, M. S.; D'Aquino, J. A.; Reardon, J. T.; Sancar,
A.; Giacomini, K. M.; Lippard, S. J. Proc. Natl. Acad. Sci. USA 2008, 105, 8902.
(64) Brabec, V.; Reedijk, J.; Leng, M. Biochemistry 1992, 31, 12397.
(65) Kasparkova, J.; Zehnulova, J.; Farrell, N.; Brabec, V. J. Biol. Chem. 2002, 277, 48076.
(66) Kasparkova, J.; Novakova, O.; Marini, V.; Najajreh, Y.; Gibson, D.; Perez, J.-M.; Brabec, V. J. Biol.
Chem. 2003, 278, 47516.
(67) Leng, M.; Locker, D.; Giraud-Panis, M. J.; Schwartz, A.; Intini, F. P.; Natile, G.; Pisano, C.;
Boccarelli, A.; Giordano, D.; Coluccia, M. Mol. Pharmacol. 2000, 58, 1525.
(68) Comess, K. M.; Costello, C. E.; Lippard, S. J. Biochemistry 1990, 29, 2102.
(69) Lemaire, M. A.; Schwartz, A.; Rahmouni, A. R.; Leng, M. Proc. Natl. Acad. Sci. USA 1991, 88, 1982.
(70) Brabec, V.; Leng, M. Proc. Natl. Acad. Sci. USA 1993, 90, 5345.
(71) Kasparkova, J.; Mellish, K. J.; Qu, Y.; Brabec, V.; Farrell, N. Biochemistry 1996, 35, 16705.
(72) Zakovska, A.; Novakova, O.; Balcarova, Z.; Bierbach, U.; Farrell, N.; Brabec, V. Eur. J. Biochem.
1998, 254, 547.
(73) Brabec, V.; Neplechova, K.; Kasparkova, J.; Farrell, N. J. Biol. Inorg. Chem. 2000, 5, 364.
(74) Bancroft, D. P.; Lepre, C. A.; Lippard, S. J. J. Am. Chem. Soc. 1990, 112, 6860.
(75) Draganescu, A.; Tullius, T. D. In Met. Ions Biol. Syst.; Sigel, A., Sigel, H., Eds.; Marcel Dekker, Inc.:
New York, 1996; Vol. 33, p 453.
(76) Maxam, A. M.; Gilbert, W. Methods Enzymol. 1980, 65, 499.
(77) Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D.
C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. J. Am. Chem. Soc. 1995, 117, 5179.
(78) Allen, F. Acta Crystallogr. Sect. B: Struct. Sci. 2002, 58, 380.
(79) Sherman, S.; Gibson, D.; Wang, A.; Lippard, S. Science 1985, 230, 412.
(80) Coll, M.; Sherman, S.; Gibson, D.; Lippard, S.; Wang, A. J. Biomol. Struct. Dynamics 1990, 8, 315.
(81) Gkionis, K.; Platts, J. J. Biol. Inorg. Chem. 2009, 14, 1165.
(82) Deeth, R. J.; Diedrich, C. J. Biol. Inorg. Chem. 2010, 15, 117.
(83) Spiegel, K.; Rothlisberger, U.; Carloni, P. J. Phys. Chem. B 2004, 108, 2699.
(84) Deeth, R. J. Inorg. Chem. 2007, 46, 4492.
(85) Deeth, R. J.; Randell, K. Inorg. Chem. 2008, 47, 7377.
(86) Lavery, R.; Moakher, M.; Maddocks, J.; Petkeviciute, D.; Zakrzewska, K. Nucleic Acids Res. 2009, 37,
5917.
(87) Kartalou, M.; Essigmann, J. M. Mutation Research 2001, 478, 1.
(88) Rohs, R.; West, S. M.; Sosinsky, A.; Liu, P.; Mann, R. S.; Honig, B. Nature 2009, 461, 1248.