Dose-dependent differences in the mutational profiles of (-)- (1R,2S,3S,4R)-3,4-dihydroxy-1,2-epoxy-1,2,3,4-tetrahydrobenzo[c]phenanthrene and its less carcinogenic enantiomer

Cancer Research

Volumn 56, Issue 16, 1996, Pages 3695-3703

  Wei, S J Caroline ^a   Chang, Richard L ^a   Cui, Xiao X ^a   Merkler, Kathleen A ^a   Wong, Ching Quo ^a   Yagi, Haruhiko ^b   Jerina, Donald M ^b   Conney, Allan H ^a  

^a RUTGERS UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZO[C]PHENANTHRIDINE DERIVATIVE; CARCINOGEN; COMPLEMENTARY DNA; MESSENGER RNA; PHOSPHORIBOSYLTRANSFERASE;

ANIMAL CELL; ARTICLE; CARCINOGENICITY; CELL STRAIN V 79; CELL SURVIVAL; CHINESE HAMSTER; CYTOTOXICITY; DOSE RESPONSE; ENANTIOMER; GENE AMPLIFICATION; GENE SEQUENCE; MUTATION RATE; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BASE SEQUENCE; CRICETINAE; DNA ADDUCTS; DOSE-RESPONSE RELATIONSHIP, DRUG; EXONS; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; MOLECULAR SEQUENCE DATA; MUTAGENS; PHENANTHRENES; STEREOISOMERISM;

EID: 0029760996     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Wei, S-J. C., Chang, R L., Wong, C. Q., Bhachech, N., Cui, X. X., Hennig, E., Yagi, H., Sayer, J. M , Jerina, D. M., Preston, B. D., and Conney, A. H. Dose-dependent differences in the profile of mutations induced by an ultimate carcinogen from benzo[a]pyrene Proc. Natl. Acad. Sci. USA, 88: 11227-11230, 1991.
2. Wei, S-J. C., Chang, R L., Bhachech, N., Cui, X. X , Merkler, K. A., Wong, C Q., Hennig, E., Yagi, H., Jerina, D. M., and Conney, A H. Dose-dependent differences in the profile of mutations induced by (+)- 7R,8S-dihydroxy-9S,10R-epoxy-7,8,9,10-tetrahydrobenzo(a)pyrene in the coding region of the hypoxanthine (guanine) phosphoribosyltransferase gene in Chinese hamster V-79 cells. Cancer Res., 53: 3294-3301, 1993
3. Wei, S-J. C., Chang, R. L., Hennig, E , Cut, X X., Merkler, K A , Wong, C. Q., Yagi, H , Jerina, D. M., and Conney, A H. Mutagenic selectivity at the HPRT locus in V-79 cells: comparison of mutations caused by bay-region benzo[a]pyrene 7,8-diol-9,10-epoxide enantiomers with high and low carcinogenic activity. Carcinogenesis (Lond), 15: 1729-1735, 1994.
4. Meehan, T, and Straub, K. Double-stranded DNA stereoselectively binds benzo-(a)pyrene diol epoxide. Nature (Lond), 277: 410-412, 1977.
5. Sayer, J M., Chadha, A., Agareal, S. K., Yeh, H. J. C , Yagi, H , and Jerina, D M Covalent nucleoside adducts of benzo[d]pyrene 7,8-diol 9,10-epoxides: structural reinvestigation and characterization of a novel adenosine adduct on the ribose moiety. J. Org. Chem., 56: 20-29, 1991
6. Jenna, D. M., Chadha, A., Cheh, A. M , Schurdak, M. E., Wood, A W., and Sayer, J M. Covalent bonding of bay-region diol epoxides to nucleic acids. In: C. M Witmer, R. Snyder, D J. Jollow, G. F Kalf, J. J. Kocsis, and I G. Sipes (eds.), Biological Reactive Intermediates IV. Molecular and Cellular Effects and Their Impact on Human Health, pp. 533-553. New York: Plenum Publishing Corp., 1991
7. Cheng, S. C , Hilton, B. D., Roman, J. M., and Dipple, A. DNA adducts from carcinogenic and noncarcinogenic enantiomers of benzo[a]pyrene dihydrodiol epoxide. Chem. Res. Toxicol , 2, 334-340, 1989
8. Andersson, B., Fält, S., and Lambert, B Strand specificity for mutations induced by (+)-anti BPDE in the hprt gene in human T-lymphocytes. Mutation Res., 269 129-140, 1992.
9. Hennig, E E., Conney, A. H., and Wei, S-J. C. Characterization of hprt splicing mutations induced by the ultimate carcinogenic metabolite of benzo[a]pyrene in Chinese hamster V-79 cells Cancer Res., 55: 1550-1558, 1995.
10. Rodriguez, H., and Loechler, E. L. Mutagenesis by (+)-anti-diol epoxide of benzo-[a]pyrene: what controls mutagenic specificity? Biochemistry, 32: 1759-1768, 1993
11. Yang, J-L., Maher, V. M , and McCormick, J. J. Kinds of mutations formed when a shuttle vector containing adducts of benzo[a]pyrene-7,8-diol-9,10-epoxide replicates in COS7 cells Mol. Cell Biol , 7: 1267-1270, 1987.
12. Yang, J-L , Maher, V. M , and McCormick, J. J Kinds of mutations formed when a shuttle vector containing adducts of (±)-7β,8α-dihydroxy-9α, 10α-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene replicates in human cells Proc Natl. Acad Sci USA, 84 3787-3791, 1987.
13. Carothers, A M , and Grunberger, D. DNA base changes in benzo[a]pyrene diol epoxide-induced dihydrofolate reductase mutants of Chinese hamster ovary cells. Carcinogenesis (Lond.), 11: 189-192, 1990.
14. Chen, R-H , Maher, V. M., and McCormick, J. J Effect of excision repair by diploid human fibroblasts on the kinds and locations of mutations induced by (±)-7β,8α-dihydroxy-9α,10α-epoxy-7,8,9,10- tetrahydrobenzo[a]pyrene in ïhe coding region of the HPRT gene. Proc. Natl. Acad Sci USA, 87: 8680-8684, 1990
15. Chen, R-H., Maher, V. M., and McCormick, J J. Lack of a cell cycle-dependent strand bias for mutations induced in the HPRT gene by (±)-7β,8α-dihydroxy-9α,10α-epoxy-7,8,9,10- tetrahydrobenzo[a]pyrene in excision repair-deficient human cells. Cancer Res., 51: 2587-2592, 1991.
16. Yang, J-L , Chen, R-H., Maher, V. M., and McCormick, J J Kinds and location of mutations induced by (±)-7β,8α-dihydroxy-9α,10α-epoxy-7,8,9,10- tetrahydrobenzo[a]pyrene in the coding region of the hypoxanthine (guanine) phosphoribosyltransferase gene in diploid human fibroblasts Carcinogenesis (Lond.), 12: 71-75, 199L
17. Wood, A. W., Chang, R L , Levin, W , Thakker, D. R , Yagi, H., Sayer, J. M , Jerina, D. M , and Conney, A. H Mutagenicity of the enantiomers of the diastereomeric bay-region benzo(c)phenanthrene 3,4-diol-1,2-epoxides in bacterial and mammalian cells Cancer Res., 44, 2320-2324, 1984.
18. Levin, W., Chang, R L , Wood, A. W., Thakker, D R , Yagi, H , Jerina, D. M., and Conney, A H. Tumorigenicity of optical isomers of the diastereomeric bay-region 3,4-diol-1,2-epoxides of benzo(c)phenanthrene in murine tumor models. Cancer Res , 46: 2257-2261, 1986.
19. Dipple, A., Pigott, M A., Agarwal, S. K., Yagi, H , Saver, J. M , and Jerina, D. M. Optically active benzo[c]phenanthrene diol epoxides bind extensively to adenine in DNA. Nature (Lond), 327: 535-536, 1987.
20. Jerina, D. M., Sayer, J. M , Agarwal, S. K , Yagi, H , Levin, W , Wood, A. W., Conney, A. H , Pruess-Schwartz, D , Baird, W M , Pigott, M A , and Dipple, A. Reactivity and tumorigenicity of bay-region diol epoxides derived from polycycilc aromatic hydrocarbons In: J J. Kocsis, D. J. Jollow, C. M Wilmer, J O. Nelson, and R. Snyder (eds.). Biological Reactive Intermediates III, pp. 11-30 New York: Plenum Publishing Corp., 1986.
21. Bigger, C. A. H , Strandberg, J., Yagi, H , Jerina, D. M., and Dipple, A. Mutagenic specificity of a potent carcinogen, benzo[c]phenanthrene (4R,3S)-dihydrodiol (2S,1R)-epoxide, which reacts with adenine and guanine in DNA. Proc Natl. Acad. Sci. USA, 86: 2291-2295, 1989.
22. Bigger, C A. H., St. John, J., Yagi, H., Jenna, D. M , and Dipple, A. Mutagenic specificities of four stereoisomeric benzo(c]phenanthrene dihydrodiol epoxides. Proc. Nail. Acad. Sci USA, 89: 368-372, 1992
23. Yagi, H., Thakker, D R., Utah, Y , Croisy-Delcey, M., and Jerina, D M. Synthesis and assignment of absolute configuration to the trans 3,4-dihydrodiol and 3,4-diol-1,2-epoxides of benzo[c]phenanthrene. Tetrahedron Lett., 24: 1349-1352, 1983.
24. Wei, S C., Chang, R. L., Cut, X., Merkler, K., Wong, C Q , Yagi, H , Jenna, D. M., and Conney, A. H, Effects of dose on the mutation profiles of (-)-(1R,2S,3S,4R)-3,4-dihydroxy-1 2-epoxy-1,2,3,4-tetrahydrobenzo[c]phenanthrene ((-)-B[c]PhDE) and its less carcinogenic enantiomer ((+)-B[c]PhDE) Proc. Am Assoc. Cancer Res., 35: 147, 1994.
25. Wood, A. W., Goode, R. L., Chang, R L., Levin, W , Conney, A. H. Yagi, H , Danselte, P. M., and Jerina, D. M Mutagenic and cytotoxic activity of benzo-[a]pyrene 4,5-, 7,8-, and 9,10-oxides and the six corresponding phenols. Proc Natl. Acad Sci. USA, 72: 3176-3180, 1975.
26. Yang, J-L., Maher, V. M., and McCormick, J. J. Amplification and direct nucleotide sequencing of cDNA from the lysate of low numbers of diploid human cells Gene (Amst.), 83: 347-354, 1989
27. Jansen, J. G., Vrieling, H., van Zeeland, A. A., and Mohn, G. R The gene encoding hypoxanthine-guanine phosphoribosyltransferase as target for mutational analysis: PCR cloning and sequencing of the cDNA from the rat Mutat. Res., 266: 105-116, 1992.
28. Jerina, D. M , Yagi, H., Thakker, D R., Karle, J. M., Mah, H. D., Boyd, D. R., Gadaginamath, G., Wood, A. W., Buening, M., Chang, R. L , Levin, W , and Conney, A. H. Stereoselective metabolic activation of polycyclic aromatic hydrocarbons. In: Y Cohen (ed) Advances in Pharmacology and Therapeutics, Vol. 9 Toxicology, pp. 53-62. Oxford: Pergamon Press, 1979.
29. Thakker, D. R , Yagi, H , Levin, W , Wood, A. W., Conney, A. H., and Jenna, D M Polycyclic aromatic hydrocarbons: metabolic activation to ultimate carcinogens. In: M W. Anders (ed.) Bioacuvation of Foreign Compounds, pp. 177-242 New York. Academic Press, 1985.
30. Jenna, D. M., Sayer, J. M , Yagi, H , van Bladeren, P. J., Thakker, D. R., Levin, W., Chang, R L , Wood, A. W , and Conney, A. H. Stereoselective metabolism of polycyclic aromatic hydrocarbons to carcinogenic metabolites. In: A. R. Boobis, J. Caldwell, F. De Matteis, and C R. Elcombe (eds), Microsomes and Drug Oxidations, pp 310-319. London. Taylor and Francis Ltd., 1985.
31. Lehr, R E , Kumar, S., Levin, W., Wood, A. W , Chang, R. L , Conney, A. H , Yagi, H., Sayer, J. M., and Jerina, D M The bay-region theory of polycyclic aromatic hydrocarbon Carcinogenesis In: R G Harvey (ed.) Polycyclic Hydrocarbons and Carcinogenesis (ACS symposium Series No. 283), pp 63-84 Washington, DC: American Chemical Society, 1985.
32. Dipple, A Reactive metabolites of carcinogens and their interactions with DNA In: P Politzer and F. J J Martin (eds.). Chemical Carcinogens: Activation Mechanisms, Structural and Electronic Factors, and Reactivity. Bioactive Molecules, Vol. 5, pp. 32-62 Amsterdam: Elsevier, 1988
33. Wood, A W., Chang, R. L., Levin, W., Yagi, H., Thakker, D R., Jenna, D. M and Conney, A. H. Differences in mutagenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides. Biochem. Biophys. Res. Commun., 77, 1389-1396, 1977
34. Wood, A W , Chang, R. J., Levin, W., Yagi, H., Tada, M , Vyas, K. P., Jenna, D. M., and Conney, A H Mutagemcity of the optical isomers of the diastereomeric bay-region chrysene 1,2-diol-3,4-epoxides in bacterial and mammalian cells Cancer Res., 42, 2972-2976, 1982.
35. Wood, A. W., Chang, R L , Levin, W , Yagi, H , Thakker, D R., van Bladeren, P J., Jenna, D. M., and Conney, A. H. Mutagenicity of the enantiomers of the diastereomeric bay-region benz[a]anthracene 3,4-diol-1,2-epoxides in bacterial and mammalian cells. Cancer Res., 43: 5821-5825, 1983.
36. Buening, M K , Wislocki, P. G., Levin, W., Yagi, H., Thakker, D R., Akagi, H., Koreeda, M., Jerina, D. M., and Conney, A. H. Tumorigenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides in newborn mice: exceptional activity of (+)-7β,8α-dihydroxy-9α,10α-epoxy-7,8,9,10- tetrahydrobereo[a]pyrene. Proc. Natl. Acad. Sci. USA, 75: 5358-5361, 1978.
37. Slaga, T. J., Bracken, W. J , Gleason, G., Levin, W., Yagi, H., Jerina, D. M., and Conney, A. H. Marked differences in the skin tumor-initiating activities of the optical enantiomers of the diastereomeric benzo(a)pyrene 7,8-diol-9,30-epoxides Cancer Res., 39: 67-71, 1979
38. Chang, R. L , Levin, W , Wood, A. W., Yagi, H., Tada, M., Vyas, K. P., Jerina, D M., and Conney, A H Tumorigenicity of enantiomers of chrysene 1,2-dihydrodiol and of the diastereomeric bay-region chrysene 1,2-dio]-3,4-epoxides on mouse skin and in newborn mice. Cancer Res., 43: 192-196, 1983.
39. Levin, W., Chang, R. L., Wood, A. W., Yagi, H., Thakker, D. R., Jenna, D. M., and Conney, A. H High stereoselectivity among the optical isomers of the diastereomeric bay-region diol-epoxides of benz[a]anthracene in the expression of tumorigenic activity in murine tumor models. Cancer Res., 44: 929-933, 1984.
40. Hoffmann, D., and Wynder, E. L. A study of tobacco carcinogenesis. XI. Tumor initiators, tumor accelerators and tumor promoting activity of condensate fractions. Cancer (Phila.), 27: 848-864, 1971.
41. Lunde, G , and Bjorseth, A. Polycyclic aromatic hydrocarbons in long-range transported aerosols Nature (Lond.), 268: 518-519, 1977.
42. Pruess-Schwartz, D., Baird, W. M , Yagi, H , Jerina, D. M., Pigott, M. A., and Dipple, A Stereochemical specificity in the metabolic activation of benzo(c)phenanthrene to metabolites that covalently bind to DNA in rodent embryo cell cultures Cancer Res., 47: 4032-4037, 1987
43. Conney, A. H , Chang, R. L., Jerina, D. M., and Wei, S-J. C. Studies on the metabolism of benzo[a]pyrene and dose-dependent differences in the mutagenic profile of its ultimate carcinogenic metabolite. Drug Metab Rev., 26: 125-163, 1994
44. Cosman, M., Laryea, A., Fiala, R., Hingerty, B. E , Amin, S , Geacintov, N. E., Broyde, S., and Patel, D. J. Solution conformation of the (-)-trans-anti-benzo[c-]phenanthrene-dA ([BPh]dA) adduct opposite dT m a DNA duplex: intercalation of the covalently attached benzo[c]phenanthrenyl ring to the 3′-side of the adduct site and comparison with the (+)-trans-anti-[BPh]dA opposite dT stereoisomer Biochemistry, 34 1295-1307, 1995
45. Cosman, M., Fiala, R , Hingerty, B. E., Laryea, A., Lee, H., Harvey, R. G , Amin, S., Geacintov, N. E., Broyde, S., and Patel, D. Solution conformation of the (+)-trans-anti-[BPh]dA adduct opposite dT in a DNA duplex: intercalation of the covalently attached benzo[c]phenanthrene to the 5′-side of the adduct site without disruption of the modified base pair. Biochemistry. 32: 12488-12497, 1993.
46. Ronai, Z. A., Gradia, S., El-Bayoumy, K , Amin, S., and Hecht, S S. Contrasting incidence of ras mutations in rat mammary and mouse skin tumors induced by anti-benzo[c]phenanthrene-3,4-diol-1,2-epoxide Carcinogenesis (Lond.), 15: 2113-2116, 1994.
47. Carothers, A. M., Urlaub, G., Mucha, J., Harvej, R G., Chasm, L. A., and Grunberger, D. Splicing mutations in the CHO DHFR gene preferentially induced by (±)-3α,4β-dihydroxy-1α,2α-epoxy-1,2,3,4- tetrahydrobenzo[c]phenanthrene. Proc Natl Acad Sci. USA, 87, 5464-5468, 1990.
48. Carothers, A M., Mucha, J., and Grunberger, D. DNA strand-specific mutations induced by (±)-3α,4β-dihydroxy-1α,2α-epox)-1,2,3,4- tetrahydrobenzo[c]phenanthrene in the dihydrofolate reductase gene Proc. Natl Acad. Sci. USA, 88: 5749-5753, 1991.
49. Carothers, A. M., Zhen, W , Mucha, J , Zhang, Y-J., Santella, R M , Grunberger, D., and Bohr, V A. DNA strand-specific repair of (±)-3α,4β-dihydroxy-1α,2α-epoxy-1,2,3,4- tetrahydrobenzo[c]phenanthrene adducts in the hamster dihydrofolate reductase gene Proc. Natl. Acad. Sci. USA, 89 11925-11929, 1992.
50. Parris, C M , Levy, D D., Jessee, J , and Seidman, M M. Proximal and distal effects of sequence context on ultraviolet mutational hotspois in a shuttle vector replicated in xeroderma cells J Mol. Biol., 236: 491-502, 1994.