The spacious active site of a Y-family DNA polymerase facilitates promiscuous nucleotide incorporation opposite a bulky carcinogen-DNA adduct: Elucidating the structure-function relationship through experimental and computational approaches

Journal of Biological Chemistry

Volumn 279, Issue 35, 2004, Pages 36951-36961

  Perlow Poehnelt, Rebecca A ^a   Likhterov, Ilya ^a   Scicchitano, David A ^a   Geacintov, Nicholas E ^a   Broyde, Suse ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOASSAY; CARCINOGENS; DNA; ESCHERICHIA COLI; MOLECULAR DYNAMICS;

EUKARYOTIC SYSTEMS; NUCLEOTIDES;

ENZYMES;

CARCINOGEN; DNA; DNA POLYMERASE; NUCLEOTIDE; OLIGODEOXYNUCLEOTIDE; UNCLASSIFIED DRUG; Y FAMILY DNA POLYMERASE;

ARTICLE; CARCINOGENESIS; CHEMICAL CARCINOGENESIS; DNA DAMAGE; ENZYME ACTIVE SITE; ESCHERICHIA COLI; GENE MUTATION; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL;

BASE PAIRING; BENZO(A)PYRENE; BINDING SITES; CARCINOGENS; DNA; DNA ADDUCTS; DNA PRIMERS; DNA-DIRECTED DNA POLYMERASE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; NUCLEOTIDES; OLIGONUCLEOTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; TEMPERATURE;

ESCHERICHIA COLI; EUKARYOTA; INSERTION SEQUENCES; PROKARYOTA;

EID: 4344596952     PISSN: 00219258     EISSN: None     Source Type: Journal    
DOI: 10.1074/jbc.M404332200     Document Type: Article

References (108)

1. Boudsocq, F., Iwai, S., Hanaoka, F., and Woodgate, R. (2001) Nucleic Acids Res. 29, 4607-4616
2. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2001) Cell 107, 91-102
3. Suzuki, N., Ohashi, E., Kolbanovskiy, A., Geacintov, N. E., Grollman, A. P., Ohmori, H., and Shibutani, S. (2002) Biochemistry 41, 6100-6106
4. Rechkoblit, O., Zhang, Y., Guo, D., Wang, Z., Amin, S., Krzeminsky, J., Louneva, N., and Geacintov, N. E. (2002) J. Biol. Chem. 277, 30488-30494
5. Bresson, A., and Fuchs, R. P. (2002) EMBO J. 21, 3881-3887
6. Wagner, J., Etienne, H., Janel-Bintz, R., and Fuchs, R. P. (2002) DNA Repair (Amst) 1, 159-167
7. Shen, X., Sayer, J. M., Kroth, H., Ponten, I., O'Donnell, M., Woodgate, R., Jerina, D. M., and Goodman, M. F. (2002) J. Biol. Chem. 277, 5265-5274
8. Napolitano, R., Janel-Bintz, R., Wagner, J., and Fuchs, R. P. (2000) EMBO J. 19, 6259-6265
9. Pages, V., and Fuchs, R. P. (2002) Oncogene 21, 8957-8966
10. Kool, E. T. (1998) Biopolymers 48, 3-17
11. Kool, E. T. (2002) Annu. Rev. Biochem. 71, 191-219
12. Kool, E. T., Morales, J. C., and Guckian, K. M. (2000) Angew Chem. Int. Ed. Engl. 39, 990-1009
13. Steitz, T. (1999) J. Biol. Chem. 274, 17395-17398
14. Kunkel, T. A., and Bebenek, K. (2000) Annu. Rev. Biochem. 69, 497-529
15. Doublie, S., and Ellenberger, T. (1998) Curr. Opin. Struct. Biol. 8, 704-712
16. Doublie, S., Sawaya, M. R., and Ellenberger, T. (1999) Structure Fold Des 7, R31-35
17. Vaisman, A., Frank, E. G., McDonald, J. P., Tissier, A., and Woodgate, R. (2002) Mutat Res 510, 9-22
18. Kokoska, R. J., Bebenek, K., Boudsocq, F., Woodgate, R., and Kunkel, T. A. (2002) J. Biol. Chem. 277, 19633-19638
19. Gonzalez, M., and Woodgate, R. (2002) Bioessays 24, 141-148
20. Frank, E. G., Sayer, J. M., Kroth, H., Ohashi, E., Ohmori, H., Jerina, D. M., and Woodgate, R. (2002) Nucleic Acids Res. 30, 5284-5292
21. Duvauchelle, J. B., Blanco, L., Fuchs, R. P., and Cordonnier, A. M. (2002) Nucleic Acids Res. 30, 2061-2067
22. Boudsocq, F., Ling, H., Yang, W., and Woodgate, R. (2002) DNA Repair (Amst) 1, 343-358
23. Vaisman, A., and Woodgate, R. (2001) EMBO J. 20, 6520-6529
24. Baynton, K., and Fuchs, R. P. (2000) Trends Biochem. Sci 25, 74-79
25. Woodgate, R. (1999) Genes Dev. 13, 2191-2195
26. Ogi, T., Shinkai, Y., Tanaka, K., and Ohmori, H. (2002) Proc. Natl. Acad. Sci. U. S. A. 99, 15548-15553
27. Goodman, M. F. (2002) Annu. Rev. Biochem. 71, 17-50
28. Ohmori, H., Friedberg, E. C., Fuchs, R. P., Goodman, M. F., Hanaoka, F., Hinkle, D., Kunkel, T. A., Lawrence, C. W., Livneh, Z., Nohmi, T., Prakash, L., Prakash, S., Todo, T., Walker, G. C., Wang, Z., and Woodgate, R. (2001) Mol. Cell 8, 7-8
29. Goodman, M., and Tippin, B. (2000) Nat. Rev. Mol. Cell Biol. 1, 101-109
30. Weinberg, R. (1996) Sci. Am. 275, 62-70
31. Shcherbakova, P. V., Bebenek, K., and Kunkel, T. A. (2003) Sci. Aging Knowledge Environ. 2003, RE3
32. Perrin, J., Poirot, N., Liska, P., Hanras, C., Theinpont, A., and Felix, G. (1993) in Proc. 13th Int. Symp. Polynuclear Aromatic Hydrocarbons (Garrigues, P., and Lamotte, M., eds) pp. 337-346, Gordon and Breach Science Publishers, Langhorne, PA
33. Grimmer, G. (1993) in Proc. 13th Int. Symp. Polynuclear Aromatic Hydrocarbons (Garrigues, P., and Lamotte, M., eds) pp. 31-41, Gordon and Breach Science Publishers, Langhorne, PA
34. Grimmer, G., Jacob, J., Dettbarn, G., and Naujack, K. W. (1997) Int. Arch. Occup. Environ. Health 69, 231-239
35. Cook, J. W., Hewett, C. L., and Hieger, I. (1933) J. Chem. Soc. 395-405
36. Phillips, D. H. (1999) Mutat. Res. 443, 139-147
37. Denissenko, M. F., Pao, A., Tang, M., and Pfeifer, G. P. (1996) Science 274, 430-432
38. Denissenko, M. F., Pao, A., Pfeifer, G. P., and Tang, M. (1998) Oncogene 16, 1241-1247
39. Conney, A. (1982) Cancer Res. 42, 4875-4917
40. Buening, M. K., Wislocki, P. G., Levin, W., Yagi, H., Thakker, D. R., Akagi, H., Koreeda, M., Jerina, D. M., and Conney, A. H. (1978) Proc. Natl. Acad. Sci 75, 5358-5361
41. Meehan, T., and Straub, K. (1979) Nature 277, 410-412
42. Cheng, S., Hilton, B., Roman, J., and Dipple, A. (1989) Chem. Res. Toxicol. 2, 334-340
43. Cosman, M., de los Santos, C., Fiala, R., Hingerty, B. E., Singh, S. B., Ibanez, V., Margulis, L. A., Live, D., Geacintov, N. E., Broyde, S., and Patel, D. (1992) Proc. Natl. Acad. Sci. U. S. A. 89, 1914-1918
44. Fountain, M. A., and Krugh, T. R. (1995) Biochemistry 34, 3152-3161
45. Feng, B., Gorin, A., Hingerty, B. E., Geacintov, N. E., Broyde, S., and Patel, D. J. (1997) Biochemistry 36, 13769-13779
46. Cosman, M., Hingerty, B. E., Geacintov, N. E., Broyde, S., and Patel, D. J. (1995) Biochemistry 34, 15334-15350
47. Zhuang, P., Kolbanovskiy, A., Amin, S., and Geacintov, N. E. (2001) Biochemistry 40, 6660-6669
48. Hanrahan, C. J., Bacolod, M. D., Vyas, R. R., Liu, T., Geacintov, N. E., Loechler, E. L., and Basu, A. K. (1997) Chem. Res. Toxicol. 10, 369-377
49. Shukla, R., Geacintov, N. E., and Loechler, E. L. (1999) Carcinogenesis 20, 261-268
50. Shukla, R., Jelinsky, S., Liu, T., Geacintov, N. E., and Loechler, E. L. (1997) Biochemistry 36, 13263-13269
51. Shukla, R., Liu, T., Geacintov, N. E., and Loechler, E. L. (1997) Biochemistry 36, 10256-10261
52. Rodriguez, H., and Loechler, E. L. (1993) Carcinogenesis 14, 373-383
53. Rodriguez, H., and Loechler, E. L. (1993) Biochemistry 32, 1759-1769
54. Rodriguez, H., and Loechler, E. L. (1995) Mutat. Res. 326, 29-37
55. Shibutani, S., Bodepudi, V., Johnson, F., and Grollman, A. P. (1993) Biochemistry 32, 4615-4621
56. Alekseyev, Y. O., and Romano, L. J. (2000) Biochemistry 39, 10431-10438
57. Lipinski, L. J., Ross, H. L., Zajc, B., Sayer, J. M., Jerina, D. M., and Dipple, A. (1998) Int. J. Oncol. 13, 269-273
58. Hruszkewycz, A. M., Canella, K. A., Peltonen, K., Kotrappa, L., and Dipple, A. (1992) Carcinogenesis 13, 2347-2352
59. Moriya, M., Spiegel, S., Fernandes, A., Amin, S., Liu, T., Geacintov, N., and Grollman, A. P. (1996) Biochemistry 35, 16646-16651
60. Lenne-Samuel, N., Janel-Bintz, R., Kolbanovskiy, A., Geacintov, N., and Fuchs, R. (2000) Mol. Microbiol. 38, 299-307
61. Jelinsky, S. A., Liu, T., Geacintov, N. E., and Loechler, E. L. (1995) Biochemistry 34, 13545-13553
62. Fernandes, A., Liu, T., Amin, S., Geacintov, N. E., Grollman, A. P., and Moriya, M. (1998) Biochemistry 37, 10164-10172
63. Chiapperino, D., Kroth, H., Kramarczuk, I. H., Sayer, J. M., Masutani, C., Hanaoka, F., Jerina, D. M., and Cheh, A. M. (2002) J. Biol. Chem. 277, 11765-11771
64. Simhadri, S., Kramata, P., Zajc, B., Sayer, J., Jerina, D., Hinkle, D., and Wei, C. (2002) Mutat. Res. 508, 137
65. Zhang, Y., Yuan, F., Wu, X., Wang, M., Rechkoblit, O., Taylor, J. S., Geacintov, N. E., and Wang, Z. (2000) Nucleic Acids Res. 28, 4138-4146
66. Mackay, W., Benasutti, M., Drouin, E., and Loechler, E. L. (1992) Carcinogenesis 13, 1415-1425
67. Yin, J., Seo, K. Y., and Loechler, E. L. (2004) DNA Repair (Amst) 3, 323-334
68. Rechkoblit, O., Amin, S., and Geacintov, N. E. (1999) Biochemistry 38, 11834-11843
69. Alekseyev, Y., Dzantiev, L., and Romano, L. (2001) Biochemistry 40, 2282-2290
70. Alekseyev, Y. O., and Romano, L. J. (2002) Biochemistry 41, 4467-4479
71. Huang, X., Kolbanovskiy, A., Wu, X., Zhang, Y., Wang, Z., Zhuang, P., Amin, S., and Geacintov, N. E. (2003) Biochemistry 42, 2456-2466
72. Perlow, R. A., and Broyde, S. (2001) J. Mol. Biol. 309, 519-536
73. Perlow, R. A., and Broyde, S. (2002) J. Mol. Biol. 322, 291-309
74. Perlow, R. A., and Broyde, S. (2003) J. Mol. Biol. 327, 797-818
75. Ling, H., Boudsocq, F., Plosky, B. S., Woodgate, R., and Yang, W. (2003) Nature 424, 1083-1087
76. Ling, H., Sayer, J. M., Plosky, B. S., Yagi, H., Boudsocq, F., Woodgate, R., Jerina, D. M., and Yang, W. (2004) Proc. Natl. Acad. Sci. U. S. A. 13, 13
77. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2004) Mol. Cell 13, 751-762
78. Yang, W. (2003) Curr. Opin. Struct. Biol. 13, 23-30
79. Doublie, S., Tabor, S., Long, A., Richardson, C., and Ellenberger, T. (1998) Nature 391, 251-258
80. Franklin, M. C., Wang, J., and Steitz, T. A. (2001) Cell 105, 657-667
81. Huang, H., Chopra, R., Verdine, G., and Harrison, S. (1998) Science 282, 1669-1675
82. Kiefer, J., Mao, C., Braman, J., and Beese, L. (1998) Nature 391, 304-307
83. Li, Y., Korolev, S., and Waksman, G. (1998) EMBO J. 17, 7514-7525
84. Eom, S. H., Wang, J., and Steitz, T. A. (1996) Nature 382, 278-281
85. Sawaya, M., Prasad, R., Wilson, S., Kraut, J., and Pelletier, H. (1997) Biochemistry 36, 11205-11215
86. Pelletier, H., Sawaya, M. R., Wolfle, W., Wilson, S. H., and Kraut, J. (1996) Biochemistry 35, 12742-12761
87. Morales, J., and Kool, E. (1999) J. Am. Chem. Soc. 121, 2323-2324
88. Morales, J. C., and Kool, E. T. (2000) Biochemistry 39, 12979-12988
89. Geacintov, N. E., Cosman, M., Mao, B., Alfano, A., Ibanez, V., and Harvey, R. G. (1991) Carcinogenesis 12, 2099-2108
90. Pirogov, N., Shafirovich, V., Kolbanovskiy, A., Solntsev, K., Courtney, S. A., Amin, S., and Geacintov, N. E. (1998) Chem. Res. Toxicol. 11, 381-388
91. Mao, B., Xu, J., Li, B., Margulis, L. A., Smirnov, S., Ya, N. Q., Courtney, S. H., and Geacintov, N. E. (1995) Carcinogenesis 16, 357-365
92. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) Nucleic Acids Res. 28, 235-242
93. Xie, X. M., Geacintov, N. E., and Broyde, S. (1999) Biochemistry 38, 2956-2968
94. Pearlman, D. A., Case, D. A., Caldwell, J. W., Ross, W. S., Cheatham, T. E. I., DeBolt, S., Ferguson, D. M., Seibel, G. L., and Kollman, P. A. (1995) Comp. Phys. Comm. 91, 1-41
95. Hingerty, B., Ritchie, R., Ferrell, T., and Turner, J. (1985) Biopolymers 24, 427-439
96. Mezei, M. (1997) J. Comp. Chem. 18, 812-815
97. Jorgensen, W., Chandrasekhar, J., Madura, J., Impey, R., and Klein, M. (1983) J. Chem. Phys. 79, 926-935
98. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K., Ferguson, D., Spellmeyer, D., Fox, T., Caldwell, J., and Kollman, P. A. (1995) J. Am. Chem. Soc. 117, 5179-5197
99. Cheatham, T., Cieplak, P., and Kollman, P. (1999) J. Biomolec. Struct. Dynam. 16, 845-862
100. Darden, T. A., York, D., and Pedersen, L. (1993) J. Chem. Phys. 98, 10089-10092
101. Harvey, S. C., Tan, R. K.-Z., and Cheatham, T. E. (1998) J. Comp. Chem. 19, 726-740
102. Connolly, M. L. (1983) Science 221, 709-713
103. Kokoska, R. J., McCulloch, S. D., and Kunkel, T. A. (2003) J. Biol. Chem. 30, 30
104. Osheroff, W. P., Beard, W. A., Yin, S., Wilson, S. H., and Kunkel, T. A. (2000) J. Biol. Chem. 275, 28033-28038
105. Kannouche, P., Fernandez de Henestrosa, A. R., Coull, B., Vidal, A. E., Gray, C., Zicha, D., Woodgate, R., and Lehmann, A. R. (2002) EMBO J. 21, 6246-6256
106. Volk, D. E., Thiviyanathan, V., Rice, J. S., Luxon, B. A., Shah, J. H., Yagi, H., Sayer, J. M., Yeh, H. J., Jerina, D. M., and Gorenstein, D. G. (2003) Biochemistry 42, 1410-1420
107. Geacintov, N., Cosman, M., Hingerty, B., Amin, S., Broyde, S., and Patel, D. (1997) Chem. Res. Tox. 10, 111-146
108. Tan, J., Geacintov, N. E., and Broyde, S. (2000) Chem. Res. Toxicol. 13, 811-822