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Energetics, conformation, and recognition of DNA duplexes modified by monodentate Ru-II complexes containing terphenyl arenes

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Novakova, Olga, Malina, J. (Jaroslav), Suchankova, Tereza, Kasparkova, Jana, Bugarcic, Tijana, Sadler, P. J. and Brabec, V. (Viktor). (2010) Energetics, conformation, and recognition of DNA duplexes modified by monodentate Ru-II complexes containing terphenyl arenes. Chemistry - A European Journal, Vol.16 (No.19). pp. 5744-5754. ISSN 0947-6539

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Official URL: http://dx.doi.org/10.1002/chem.200903078

Abstract

We studied the thermodynamic properties, conformation, and recognition of DNA duplexes site-specifically modified by monofunctional adducts of Ru-II complexes of the type [Ru-II-(eta(6)-arene)(Cl)(en)](+), in which arene=para-, meta-, or orrho-terphenyl (complexes 1, 2, and 3, respectively) and en=1,2-diaminoethane. It has been shown (J. Med. Chem. 2008, 51, 5310) that 1 exhibits promising cytotoxic effects in human tumor cells, whereas 2 and 3 are much less cytotoxic; concomitantly with the high cytotoxicity of I. its DNA binding mode involves combined intercalative and monofunctional (coordination) binding modes, whereas less cytotoxic compounds 2 and 3 bind to DNA only through a monofunctional coordination to DNA bases. An analysis of conformational distortions induced in DNA by adducts of 1 and 2 revealed more extensive and stronger distortion and concomitantly greater thermodynamic destabilization of DNA by the adducts of nonintercalating 2. Moreover, affinity of replication protein A to the DNA duplex containing adduct of 1. was pronouncedly lower than to the adduct of 2. On the other hand, another damaged-DNA-binding protein, xeroderma pigmentosum protein A. did not recognize the DNA adduct of 1 or 2. Importantly, the adducts of 1 induced a considerably lower level of repair synthesis than the adducts of 2, which suggests enhanced persistence of the adducts of the more potent and intercalating 1 in comparison with the adducts of the less potent and nonintercalating 2. Also interestingly, the adducts of 1 inhibited DNA polymerization more efficiently than the adducts of 2, and they could also be bypassed by DNA polymerases with greater difficulty Results of the present work along with those previously published support the view that monodentate Run arene complexes belong to a class of anticancer agents for which structure pharmacological relationships might be correlated with their DNA-binding modes.

Item Type:

Journal Article

Subjects:

Q Science > QC Physics
Q Science > QD Chemistry
Q Science > QP Physiology

Divisions:

Faculty of Science > Chemistry

Library of Congress Subject Headings (LCSH):

Aromatic compounds -- Therapeutic use, Ruthenium compounds -- Therapeutic use, Calorimetry, Antineoplastic agents, DNA adducts, DNA-drug interactions

Journal or Publication Title:

Chemistry - A European Journal

Publisher:

Wiley - V C H Verlag GmbH & Co. KGaA

ISSN:

0947-6539

Official Date:

17 May 2010

Dates:

Date	Event
17 May 2010	Published

Volume:

Vol.16

Number:

No.19

Number of Pages:

Page Range:

pp. 5744-5754

Identification Number:

10.1002/chem.200903078

Status:

Peer Reviewed

Publication Status:

Published

Access rights to Published version:

Restricted or Subscription Access

Funder:

Czech Republic. Ministerstvo školství, mládeže a tělovýchovy [Czech Republic. Ministry of Education, Youth, and Sports], Akademie věd České republiky [Academy of Sciences of the Czech Republic] (ASCR), Grantová agentura České republiky [Grant Agency of the Czech Republic]

Grant number:

MSMT LC06030 (MSMT), 6198959216 (MSMT), ME08017 (MSMT), ME10066 (MSMT), OC08003 (MSMT), 0009018 (MSMT), KAN200200651 (ACSR), M200040901 (ACSR), AV0Z50040507 (ACSR), AV0Z500040702 (ACSR), IAA400040803 (ACSR), 301/09/H004 (GACR), P301/10/0598 (GACR)

References:

[1] R. E. Morris, R. E. Aird, P. D. Murdoch, H. M. Chen, J. Cummings,
N. D. Hughes, S. Parsons, A. Parkin, G. Boyd, D. I. Jodrell, P. J.
Sadler, J. Med. Chem. 2001, 44, 3616 –3621.
[2] R. Aird, J. Cummings, A. Ritchie, M. Muir, R. Morris, H. Chen, P.
Sadler, D. Jodrell, British J. Cancer 2002, 86, 1652 – 1657.
[3] Y. K. Yan, M. Melchart, A. Habtemariam, P. J. Sadler, Chem. Commun.(
Cambridge) 2005, 4764 –4776.
[4] S. J. Dougan, P. J. Sadler, Chimia 2007, 61, 704 – 715.
[5] V. Brabec, O. Novakova, Drug Resist. Updates 2006, 9, 111 –122.
[6] M. A. Jakupec, E. Reisner, A. Eichinger, M. Pongratz, V. B. Arion,
M. Galanski, C. G. Hartinger, B. K. Keppler, J. Med. Chem. 2005,
48, 2831 –2837.
[7] P. J. Dyson, G. Sava, Dalton Trans. 2006, 1929 – 1933.
[8] H. Chen, J. A. Parkinson, O. Novakova, J. Bella, F. Wang, A.
Dawson, R. Gould, S. Parsons, V. Brabec, P. J. Sadler, Proc. Natl.
Acad. Sci. USA 2003, 100, 14623 – 14628.
[9] O. Novakova, H. Chen, O. Vrana, A. Rodger, P. J. Sadler, V.
Brabec, Biochemistry 2003, 42, 11544 – 11554.
[10] O. Novakova, J. Kasparkova, V. Bursova, C. Hofr, M. Vojtiskova, H.
Chen, P. J. Sadler, V. Brabec, Chem. Biol. 2005, 12, 121 –129.
[11] M. Melchart, A. Habtemariam, O. Novakova, S. A. Moggach,
F. P. A. Fabbiani, S. Parsons, V. Brabec, P. J. Sadler, Inorg. Chem.
2007, 46, 8950 –8962.
[12] S. W. Magennis, A. Habtemariam, O. Novakova, J. B. Henry, S.
Meier, S. Parsons, I. D. H. Oswald, V. Brabec, P. J. Sadler, Inorg.
Chem. 2007, 46, 5059 –5068.
[13] T. Bugarcic, O. Novakova, A. Halamikova, L. Zerzankova, O.
Vrana, J. Kasparkova, A. Habtemariam, S. Parsons, P. J. Sadler, V.
Brabec, J. Med. Chem. 2008, 51, 5310 –5319.
[14] T. Bugarcic, A. Habtemariam, J. Stepankova, P. Heringova, J. Kasparkova,
R. J. Deeth, R. D. L. Johnstone, A. Prescimone, A. Parkin,
S. Parsons, V. Brabec, P. J. Sadler, Inorg. Chem. 2008, 47, 11470 –
11486.
[15] O. Novakova, A. A. Nazarov, C. G. Hartinger, B. K. Keppler, V.
Brabec, Biochem. Pharmacol. 2009, 77, 364 – 374.
[16] N. Poklar, D. S. Pilch, S. J. Lippard, E. A. Redding, S. U. Dunham,
K. J. Breslauer, Proc. Natl. Acad. Sci. USA 1996, 93, 7606 –7611.
[17] D. S. Pilch, S. U. Dunham, E. R. Jamieson, S. J. Lippard, K. J. Bres-
ACHTUNGTRENUNGlauer, J. Mol. Biol. 2000, 296, 803 – 812.
[18] C. Hofr, N. Farrell, V. Brabec, Nucleic Acids Res. 2001, 29, 2034 –
2040.
[19] C. Hofr, V. Brabec, J. Biol. Chem. 2001, 276, 9655 –9661.
[20] J. Malina, O. Novakova, B. K. Keppler, E. Alessio, V. Brabec, J.
Biol. Inorg. Chem. 2001, 6, 435 –445.
[21] C. Hofr, V. Brabec, Biopolymers 2005, 77, 222 –229.
[22] V. Bursova, J. Kasparkova, C. Hofr, V. Brabec, Biophys. J. 2005, 88,
1207 – 1214.
[23] V. Brabec, K. Stehlikova, J. Malina, M. Vojtiskova, J. Kasparkova,
Arch. Biochem. Biophys. 2006, 446, 1 –10.
[24] J. Malina, O. Novakova, M. Vojtiskova, G. Natile, V. Brabec, Biophys.
J. 2007, 93, 3950 –3962.
[25] O. Novakova, J. Malina, J. Kasˇparkova, A. Halamikova, V. Bernard,
F. Intini, G. Natile, V. Brabec, Chem. Eur. J. 2009, 15, 6211 –6221.
[26] H. K. Liu, S. J. Berners-Price, F. Y. Wang, J. A. Parkinson, J. J. Xu, J.
Bella, P. J. Sadler, Angew. Chem. 2006, 118, 8333 – 8336; Angew.
Chem. Int. Ed. 2006, 45, 8153 – 8156.
[27] P. E. Nielsen, J. Mol. Recognit. 1990, 3, 1–24.
[28] V. Brabec, M. Sip, M. Leng, Biochemistry 1993, 32, 11676 – 11681.
[29] H. Kostrhunova, V. Brabec, Biochemistry 2000, 39, 12639 –12649.
[30] S. M. Patrick, J. J. Turchi, Biochemistry 1998, 37, 8808 – 8815.
[31] K. M. Comess, J. N. Burstyn, J. M. Essigmann, S. J. Lippard, Biochemistry
1992, 31, 3975 –3990.
[32] Z. Suo, K. Johnson, J Biol Chem. 1998, 273, 27259 –27267.
[33] A. Vaisman, M. W. Warren, S. G. Chaney, J. Biol. Chem. 2001, 276,
18999 – 19005.
[34] E. Bassett, A. Vaisman, J. M. Havener, C. Masutani, F. Hanaoka,
S. G. Chaney, Biochemistry 2003, 42, 14197 – 14206.
[35] J. Kasparkova, O. Novakova, V. Marini, Y. Najajreh, D. Gibson, J.-
M. Perez, V. Brabec, J. Biol. Chem. 2003, 278, 47516 –47525.
[36] B. Moriarity, O. Novakova, N. Farrell, V. Brabec, J. Kasparkova,
Arch. Biochem. Biophys. 2007, 459, 264 –272.
[37] A. Alt, K. Lammens, C. Chiocchini, A. Lammens, J. C. Pieck, D.
Kuch, K. P. Hopfner, T. Carell, Science 2007, 318, 967 –970.
[38] Y. Jung, S. J. Lippard, Chem. Rev. 2007, 107, 1387 – 1407.
[39] V. Brabec, J. Kasparkova in Role of DNA Repair in Antitumor Effects
of Platinum Drugs (Eds.: N. Hadjiliadis, E. Sletten), Wiley,
New York, 2009, pp. 175 – 208.
[40] G. E. Plum, C. A. Gelfand, K. J. Breslauer in Physicochemical Approaches
to Structural Elucidation: Effects of 3,N4-Ethenodeoxycytidine
on Duplex Stability and Energetics (Eds.: B. Singer, H.
Bartsch), International Agency for Research on Cancer, Lyon, 1999,
pp. 169 –177.
[41] N. E. Geacintov, S. Broyde, T. Buterin, H. Naegeli, M. Wu, S. X.
Yan, D. J. Patel, Biopolymers 2002, 65, 202 – 210.
[42] Y. Maeda, K. Nunomura, E. Ohtsubo, J. Mol. Biol. 1990, 215, 321 –
329.
[43] M. T. Bjorndal, D. K. Fygenson, Biopolymers 2002, 65, 40– 44.
[44] J. M. Sturtevant, Proc. Natl. Acad. Sci. USA 1977, 74, 2236 –2240.
[45] R. S. Spolar, M. T. Record, Jr., Science 1994, 263, 777 – 784.
[46] P. J. Mikulecky, A. L. Feig, Nucleic Acids Res. 2004, 32, 3967 –3976.
[47] W. B. Peters, S. P. Edmondson, J. W. Shriver, Biochemistry 2005, 44,
4794 – 4804.
[48] Y. Zhang, Z. Xi, R. S. Hegde, Z. Shakked, D. M. Crothers, Proc.
Natl. Acad. Sci. USA 2004, 101, 8337 –8341.
[49] J. Malina, J. Kasparkova, G. Natile, V. Brabec, Chem. Biol. 2002, 9,
629 – 638.
[50] R. E. Dickerson, T. K. Chiu, Biopolymers 1997, 44, 361 – 403.
[51] S. M. Cohen, E. R. Jamieson, S. J. Lippard, Biochemistry 2000, 39,
8259 – 8265.
[52] M. Missura, T. Buterin, R. Hindges, U. Hubscher, J. Kasparkova, V.
Brabec, H. Naegeli, EMBO J. 2001, 20, 3554 – 3564.
[53] R. Dip, U. Camenisch, H. Naegeli, DNA Repair 2004, 3, 1409 – 1423.
[54] Y. Liu, Y. Liu, Z. Yang, C. Utzat, G. Wang, A. K. Basu, Y. Zou, Biochemistry
2005, 44, 7361 –7368.
[55] S. F. Bellon, S. J. Lippard, Biophys. Chem. 1990, 35, 179 –188.
[56] C. Iftode, Y. Daniely, J. A. Borowiec, Crit. Rev. Biochem. Mol. Biol.
1999, 34, 141 –180.
[57] Y. Zou, Y. Liu, X. Wu, S. M. Shell, J. Cell. Physiol. 2006, 208, 267 –
273.
[58] J. Kasparkova, J. Zehnulova, N. Farrell, V. Brabec, J. Biol. Chem.
2002, 277, 48076 –48086.
[59] V. Brabec, Prog. Nucleic Acid Res. Mol. Biol. 2002, 71, 1– 68.
[60] E. L. Mamenta, E. E. Poma, W. K. Kaufmann, D. A. Delmastro,
H. L. Grady, S. G. Chaney, Cancer Res. 1994, 54, 3500 – 3505.
[61] S. W. Johnson, P. B. Laub, J. S. Beesley, R. F. Ozols, T. C. Hamilton,
Cancer Res. 1997, 57, 850 – 856.
[62] U. Habscher, H. P. Nasheuer, J. E. Syvaoja, Trends Biochem. Sci.
2000, 25, 143 –147.
[63] W. C. Lam, E. J. C. Van der Schans, L. C. Sowers, D. P. Millar, Biochemistry
1999, 38, 2661 –2668.
[64] T. A. Steitz, J. Biol. Chem. 1999, 274, 17395 –17398.
[65] S. Lone, L. J. Romano, Biochemistry 2003, 42, 3826 – 3834.
[66] L. Ronconi, P. J. Sadler, Coord. Chem. Rev. 2007, 251, 1633 –1648.
[67] P. C. Bruijnincx, P. J. Sadler, Curr. Opin. Chem. Biol. 2008, 12, 197 –
206.
[68] N. P. Johnson, J.-L. Butour, G. Villani, F. L. Wimmer, M. Defais, V.
Pierson, V. Brabec, Prog. Clin. Biochem. Med. 1989, 6, 1–24.
[69] E. R. Jamieson, S. J. Lippard, Chem. Rev. 1999, 99, 2467 –2498.
[70] E. Alessio, G. Mestroni, A. Bergamo, G. Sava, Curr. Top. Med.
Chem. 2004, 4, 1525 – 1535.
[71] V. Brabec, J. Reedijk, M. Leng, Biochemistry 1992, 31, 12397 –
12402.
[72] C. J. Jones, R. D. Wood, Biochemistry 1993, 32, 12096 –12104.
[73] I. L. Hermanson-Miller, J. J. Turchi, Biochemistry 2002, 41, 2402 –
2408.
[74] J. L. Manley, A. Fire, A. Cano, P. A. Sharp, M. L. Gefter, Proc. Natl.
Acad. Sci. USA 1980, 77, 3855 – 3859.
[75] J. T. Reardon, A. Vaisman, S. G. Chaney, A. Sancar, Cancer Res.
1999, 59, 3968 –3971.
[76] V. Brabec, M. Leng, Proc. Natl. Acad. Sci. USA 1993, 90, 5345 –
5349.
[77] O. Novakova, J. Kasparkova, J. Malina, G. Natile, V. Brabec, Nucleic
Acids Res. 2003, 31, 6450 –6460.