DNA cleavage by the antitumor agent 3-amino-1,2,4-benzotriazine 1,4-dioxide (SR4233): Evidence for involvement of hydroxyl radical

Journal of the American Chemical Society

Volumn 118, Issue 14, 1996, Pages 3380-3385

  Daniels, J Scott ^a   Gates, Kent S ^a,b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; TIRAPAZAMINE;

ARTICLE; DNA CLEAVAGE; DRUG ACTIVATION; REACTION ANALYSIS;

EID: 0029959898     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja9510774     Document Type: Article

References (81)

1. (a) Remers, W A In Textbook of Organic, Medicinal and Pharmaceutical Chemistry; Delgado, J. W., Remers, W. A., Eds.; Lippincott: Philadelphia, PA, 1991; pp 313-358.
2. (b) Kane, S. A ; Hecht, S. M. Prog. Nucleic Acids Res. Mol. Biol. 1994, 49, 313-352.
3. (c) Henderson, D.; Hurley, L. H. Nature (Med) 1995, 1, 525-527
4. (a) Hockel, M.; Schlenger, K., Knoop, C.; Vaupel, P. Cancer Res. 1991, 51, 6098-6102.
5. (b) Mueller-Klieser, W., Vaupel, P ; Manz, R.; Schimdseder, R. Int. J. Radiat. Oncol. Biol. Phys. 1981, 7, 1397-1404
6. (c) Vaupel, P., Schlenger, K ; Knoop, C.; Hockel, M. Cancer Res. 1991, 51, 3316-3322.
7. (a) Gatenby, R. A.; Kessler, H. B.; Rosenblum, J. S.; Coia, L. R.; Moldofsky, P. J., Hartz, W. H., Broder, G. J Int. J. Radiat. Oncol Biol. Phys. 1988, 14, 831-838.
8. (b) Overgaard, J., Hansen, H. S.; Jorgenson, K., Hansen, M. H Int. J. Radiat. Oncol. Biol. Phys. 1986, 12, 515-521.
9. (c) Bush, R. S., Jenkin, R D., Allt, W E C.; Beale, F A.; Bean, H.; Denbo, A. J.; Pringle, J. F Br. J. Cancer 1978, 37, Suppl. III, 302-306.
10. (d) Hockel, M., Knoop, C.; Schlenger, K ; Vorndran, B., Baubmann, E ; Mitze, M., Knapstein, P G.; Vaupel, P Radiother. Oncol 1993, 26, 45-50
11. (a) Kennedy, K. A. Anticancer Drug Res. 1987, 2, 181-194.
12. (b) Sartorelli, A. C. Cancer Res. 1988, 48, 775-778.
13. (c) Tannock, I ; Guttman, P Br J. Cancer 1981, 42, 245-248.
14. (a) Adams, G. E Radiation Res. 1992, 132, 129-139.
15. (b) Palmer, B. D., Wilson, W. R.; Atwell, G. J., Schultz, D.; Xu, X. Z.; Denny, W. A. J. Med. Chem. 1994, 37, 2175-2184.
16. Zeman, E. M.; Brown, J. M.; Lemmon, M. J.; Hirst, V. K.; Lee, W W. Int. J. Radiat. Oncol. Biol. Phys. 1986, 12, 1239-1242.
17. Zeman, E. M., Baker, M. A.; Lemmon, M. J.; Pearson, C. I.; Adams, J. A ; Brown, J. M.; Lee, W. W.; Tracy, M. Int. J. Radiat. Onc. Biol. Phys 1989, 16, 977-981.
18. Brown, J. M. Br. J. Cancer 1993, 67, 1163-70.
19. Fitzsimmons, S A., Lewis, A. D ; Riley, R. J., Workman, P Carcinogenesis 1994, 15, 1503-1510.
20. Studies involving electrochemical reduction of 1: (a) Tocher, J H., Edwards, D I. Free Radical Res. 1994, 21, 277-283. (b) Tocher, J. H., Virk, N S.; Edwards, D. I. Biochem. Pharmacol. 1990, 39, 781-786.
21. Studies involving electrochemical reduction of 1: (a) Tocher, J H., Edwards, D I. Free Radical Res. 1994, 21, 277-283. (b) Tocher, J. H., Virk, N S.; Edwards, D. I. Biochem. Pharmacol. 1990, 39, 781-786.
22. Baker, M. A.; Zeman, E. M.; Hirst, V. K.; Brown, J. M. Cancer Res. 1988, 48, 5947-5952.
23. Biedermann, K A., Wang, J.; Graham, R. P.; Brown, J. M. Br. J. Cancer 1991, 63, 358-362.
24. Costa, A. K.; Baker, M. A.; Brown, J. M.; Trudell, J. R. Cancer Res. 1989, 49, 925-929.
25. Brown, J. M. In Selective Activation of Drugs by Redox Processes, Breccia, A., Adams, G. E., Fielden, E. M., Wardman, P., Eds.; Plenum Press: Fermo, Italy, 1991; pp 137-148.
26. Lloyd, R. V.; Duling, D. R.; Rumyantseva, G. V.; Mason, R. P.; Bridson, P. K. Mol. Pharmacol. 1991, 40, 440-445.
27. Walton, M. I.; Workman, P. Biochem. Pharmacol. 1990, 39, 1735-1742.
28. Laderoute, K ; Rauth, A. M. Biochem. Pharmacol. 1986, 35, 3417-3420.
29. Fridovich, I. Acc. Chem. Res. 1972, 5, 321-326.
30. (a) Von Sonntag, C.; Hagen, U.; Schon-Bopp, A.; Schulte-Frolinde, D. Adv. Radiat. Biol. 1981, 9, 109-142.
31. (b) Stubbe, J.; Kozarich, J. W. Chem. Rev. 1987, 87, 1107-1136.
32. (c) Tullius, T. D.; Dombroski, B. A.; Churchill, M. E. A ; Kam, L. Methods Enzymol. 1987, 155, 537-558.
33. For examples, see: (a) Nicolaou, K. C.; Dai, W.-M., Angew. Chem. Int. Ed. Engl. 1991, 30, 1387-1416. (b) Pratviel, G.; Bernadou, J.; Meunier, B. Angew. Chem., Int. Ed. Engl. 1995, 34, 746-769. (c) Giese, B.; Beyrich-Graf, X.; Burger, J.; Kesselheim, C.; Senn, M.; Schafer, T. Angew. Chem., Int. Ed. Engl. 1993, 32, 1742-1743.
34. For examples, see: (a) Nicolaou, K. C.; Dai, W.-M., Angew. Chem. Int. Ed. Engl. 1991, 30, 1387-1416. (b) Pratviel, G.; Bernadou, J.; Meunier, B. Angew. Chem., Int. Ed. Engl. 1995, 34, 746-769. (c) Giese, B.; Beyrich-Graf, X.; Burger, J.; Kesselheim, C.; Senn, M.; Schafer, T. Angew. Chem., Int. Ed. Engl. 1993, 32, 1742-1743.
35. For examples, see: (a) Nicolaou, K. C.; Dai, W.-M., Angew. Chem. Int. Ed. Engl. 1991, 30, 1387-1416. (b) Pratviel, G.; Bernadou, J.; Meunier, B. Angew. Chem., Int. Ed. Engl. 1995, 34, 746-769. (c) Giese, B.; Beyrich-Graf, X.; Burger, J.; Kesselheim, C.; Senn, M.; Schafer, T. Angew. Chem., Int. Ed. Engl. 1993, 32, 1742-1743.
36. Laderoute, K.; Wardman, P.; Rauth, A. M. Biochem. Pharmacol. 1988, 37, 1487-1495
37. 18
38. Graf, E.; Mahoney, J. R.; Bryant, R. G.; Eaton, J. W. J. Biol. Chem. 1984, 259, 3620-3624.
39. Mason, J. C.; Tennant, G., J. Chem. Soc. B 1970, 911-916.
40. Omission of the xanthine oxidase substrate xanthine from the reaction mixture removes the source of reducing equivalents for the reduction of 1 by xanthine oxidase.
41. 11 Poor cleavage by 3 may be due primarily to the fact that the compound is not efficiently reduced by the xanthine-xanthine oxidase enzyme system used in these studies (J S. Daniels, K. S. Gates, unpublished data); however, we suggest that the small amount of observed DNA cleavage by the mono-N-oxide 3 may proceed by a hydroxyl radical-liberating mechanism analogous to pathway a in Scheme 1
42. (a) Kappen, L S.; Goldberg, I. H. Nucleic Acids Res. 1978, 5, 2959-2967
43. (b) Riordan, C G.; Wei, P. J. Am. Chem. Soc. 1994, 116, 2189-2190.
44. (c) Cheng, C. C., Rokita, S. E.; Burrows, C. J. Angew. Chem., Int. Ed. Engl. 1993, 32, 277-278.
45. For reaction rates of various scavengers with hydroxyl radical, see: Buxton, G. V., Greenstock, C L.; Phillip, W.; Ross, A B J. Phys. Chem. Ref. Data 1988, 17, 513-886.
46. Pogozelski, W. K.; McNeese, T. J.; Tullius, T. D. J. Am. Chem. Soc. 1995, 117, 6428-6433.
47. (a) Steiner, M G , Babbs, C. F. Arch. Biochem. Biophys. 1990, 278, 478-481.
48. (b) Dixon, W T ; Norman, R O. C.; Buley, A. L. J. Chem. Soc. 1964, 3625-3634.
49. (c) Lagercrantz, C., Forshult, S. Acta Chem. Scand. 1969, 23, 811-817.
50. (d) Klein, S. M.; Cohen, G.; Cederbaum, A. I. Biochemistry 1981, 20, 6006-6012
51. Fukui, S.; Hanasaki, Y.; Ogawa, S. J. Chromatogr. 1993, 630, 187-193.
52. 30 however, the authors recognize that methanesulfinic acid could conceivably result from a direct reaction between radical 2 and DMSO.
53. For example see: Burkhoff, A. M.; Tullius, T. D. Nature 1988, 331, 455-457.
54. 29 that DNA cleavage by the iron-EDTA system used in our study yields DNA-cleavage products indistinguishable from those formed by radiolytically-generated hydroxyl radical.
55. (a) Luo, Y ; Han, Z.; Chin, S. M.; Linn, S Proc. Natl. Acad. Sci U.S.A. 1994, 91, 12438-12442.
56. (b) Wink, D. A.; Nims, R. W.; Saavedra, J. E ; Utermahlen, W. E., Jr ; Ford, P. C Proc. Natl Acad Sci. U.S.A 1994, 91, 6604-6608.
57. (a) Sawyer, D. T., Kang, C.; Llobet, A.; Redman, C. J. Am. Chem. Soc. 1993, 115, 5817-5818
58. (b) Yamazaki, I.; Piette, L H. J. Am. Chem. Soc. 1991, 113, 7588-7593.
59. Halliwell, B.; Gutteridge, J. M. C. Methods Enzymol. 1990, 186, 1-85
60. (a) Bomford, C K., Kunkler, I. H., Sherriff, S B. Walter and Miller's Textbook of Radiotherapy Radiation Physics, Therapy, and Oncology, Churchill Livingston: Edinburgh, 1993
61. (b) Hall, E. J. Int. J. Radiation Oncol. Biol. Phys. 1994, 30, 1019-1028
62. (c) Armal, P. R., Strniste G. F., Wallace, S. S. Radiation Res. 1977, 69, 328-338
63. Of course, the possibility exists that, when produced in vivo, radical 2 reacts with non-nucleic acid components of the cell and the resulting radicals lead to DNA cleavage.
64. Denny, W A. In Cancer Chemotherapeutic Agents; Foye, W. O , Ed., American Chemical Society Washington, DC, 1995, pp 483-500.
65. (a) Nagai, K , Carter, B J., Xu, J., Hecht, S M J Am Chem. Soc. 1991, 113, 5099-5100.
66. (b) Nagai, K.; Hecht, S. M J. Biol. Chem. 1991, 266, 23994-24002
67. Barton, D. H. R., Crich, D., Motherwell, W. B Tetrahedron 1985, 41, 3901-3924.
68. (a) Newcomb, M., Glenn, A. G. J. Am. Chem. Soc. 1989, 111, 275-277.
69. (b) Venkatesan, H.; Greenberg, M. M. J. Org. Chem. 1995, 60, 1053-1059.
70. (c) Boivin, J ; Crépon, E.; Zard, S. Z. Tetrahedron Lett. 1990, 31, 6869-6872.
71. (d) Barton, D. H. R., Jaszberenyi, J. Cs.; Morrell, A. I. Tetrahedron Lett. 1991, 32, 311-314.
72. (e) Adam, W.; Ballmaier, D.; Epe, B., Grimm, G. N.; Saha-Moller, C. R. Angew. Chem., Int. Ed. Engl. 1995, 34, 2156-2158.
73. (f) Aveline, B. M.; Kochevar, I. E.; Redmond, R. W. J. Am Chem. Soc. 1996, 118, 289-290
74. Monge, A.; Palop, J. A ; de Ceráin, A. L.; Senador, V.; Martinez-Crespo, F J., Sainz, Y.; Narro, S.; Garcia, E.; de Miguel, C.; González, M., Hamilton, E.; Barker, A. J.; Clarke, E. D.; Greenhow, D. T. J. Med. Chem. 1995, 38, 1786-1792.
75. Sakata, N.; Moriya, Y ; Hori, M. J. Antibiotics 1987, 40, 558-560.
76. (a) Behki, R. M.; Lesley, S. M. J. Bacteriology 1972, 109, 250-261.
77. (b) Hollstein, U.; Butler, P. L. Biochemistry 1972, 109, 250-261.
78. Suter, W., Rosselet, A ; Knusel, F. Antimicrob. Agents Chemother. 1978, 13, 770-783.
79. Sambrook, J.; Fritsch, E. F ; Maniatis, T. Molecular Cloning: A Laboratory Manual; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1989
80. Bauer, W.; Vinograd, J. J. Mol. Biol. 1968, 33, 141-171.
81. Lynch, R.; Fridovich, I. Biochim. Biophys. Acta 1979, 571, 195-200.