CYP1C1 messenger RNA expression is inducible by benzo[a]pyrene in Fundulus heteroclitus embryos and adults

Toxicological Sciences

Volumn 93, Issue 2, 2006, Pages 331-340

  Wang, Lu ^a   Scheffler, Brian E ^b   Willett, Kristine L ^a  

^a UNIVERSITY OF MISSISSIPPI   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Benzo a pyrene; CYP1C1; Cytochrome P450; Embryos; Fundulus; Killifish

Indexed keywords

BENZO[A]PYRENE; COMPLEMENTARY DNA; CYTOCHROME P450; CYTOCHROME P450 1A; CYTOCHROME P450 1C1; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CARCINOGENESIS; CONTROLLED STUDY; EMBRYO; EYE; FEMALE; FISH; FUNDULUS HETEROCLITUS; GASTROINTESTINAL TRACT; GILL; GONAD; HEART; LIVER; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SPLEEN; TISSUE DISTRIBUTION;

AMINO ACID SEQUENCE; ANIMALS; BENZO(A)PYRENE; CLONING, MOLECULAR; CYTOCHROME P-450 ENZYME SYSTEM; EMBRYO, NONMAMMALIAN; FEMALE; FUNDULIDAE; MALE; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; SEX CHARACTERISTICS;

FUNDULUS; FUNDULUS HETEROCLITUS; STENOTOMUS CHRYSOPS; TELEOSTEI;

EID: 33748744373     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfl072     Document Type: Article

References (46)

1. Armstrong, P. B., and Child, J. S. (1965). Stages in the normal development of Fundulus heteroclitus. Biol. Bull. 128, 143-169.
2. Bello, S. M., Franks, D. G., Stegeman, J. J., and Hahn, M. E. (2001). Acquired resistance to Ah receptor agonists in a population of Atlantic killifish (Fundulus heteroclitus) inhabiting a marine superfund site: In vivo and in vitro studies on the inducibility of xenobiotic metabolizing enzymes. Toxicol. Sci. 60, 77-91.
3. Billiard, S. M., Querbach, K., and Hodson, P. V. (1999). Toxicity of retene to early life stages of two freshwater fish species. Environ. Toxicol. Chem. 18, 2070-2077.
4. Billiard, S. M., Timme-Laragy, A. R., Wassenberg, D. M., Cockman, C., and DiGiulio, R. T. (2006). The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons in zebrafish. Toxicol. Sci. 92(2), 526-536.
5. Buters, J. T., Quintanilla-Martinez, L., Schober, W., Soballa, V. J., Hintermair, J., Wolff, T., Gonzalez, F. J., and Greim, H. (2003). CYP1B1 determines susceptibility to low doses of 7,12-dimethylbenz(a)anthracene-induced ovarian cancers in mice: Correlation of CYP1B1-mediated DNA adducts with carcinogenicity. Carcinogenesis 24(2), 327-334.
6. Carlson, E. A., Li, Y., and Zelikoff, J. T. (2004). Benzo[a]pyrene-induced immunotoxicity in Japanese medaka (Oryzias latipes): Relationship between lymphoid CYP1A activity and humoral immune suppression. Toxicol. Appl. Pharmacol. 201, 40-52.
7. Celander, M., and Stegeman, J. J. (1997). Isolation of a cytochrome P450 3A cDNA sequence (CYP3A30) from the marine teleost Fundulus heteroclitus and phylogenetic analyses of CYP3A genes. Biochem. Biophys. Res. Commun. 236, 306-312.
8. Collier, T. K., Singh, S. V., Awasthi, Y. C., and Varanasi, U. (1992). Hepatic xenobiotic metabolizing enzymes in two species of benthic fish showing different prevalences of contaminant-associated liver neoplasms. Toxicol. Appl. Pharmacol. 113, 319-324.
9. El-kady, M. A. H., Mitsuo, R., Kaminishi, Y., and Itakura, T. (2004a). cDNA cloning, sequence analysis and expression of 3-methylcholanthrene-inducible cytochrome P450 1b1 in carp (Cyprinus carpio). Environ. Sci. 11(4), 231-240.
10. El-kady, M. A. H., Mitsuo, R., Kaminishi, Y., and Itakura, T. (2004b). Isolation of cDNA of novel cytochrome P450 1B gene, CYP1B2, from carp (Cyprinus carpio) and its induced expression in gills. Environ. Sci. 11(6), 345-354.
11. Godard, C. A., Goldsone, J. V., Said, M. R., Dickerson, R. L., Woodin, B. R., and Stegeman, J. J. (2005). The new vertebrate CYP1C family: Cloning of new subfamily members and phylogenetic analysis. Biochem. Biophys. Res. Commun. 331, 1016-1024.
12. Gotoh, O. (1992). Substrate recognition sites in cytochrome P450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences. J. Biol. Chem. 267(1), 83-90.
13. Hayes, C. L., Spink, D. C., Spink, B. C., Cao, J. Q., Walker, N. J., and Sutter, T. R. (1996). 17β-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A. 93, 9776-9781.
14. Hoffman, J. L., and Oris, J. T. (2006). Altered gene expression: A mechanism for reproductive toxicity in zebrafish exposed to benzo[a]pyrene. Aquat. Toxicol. 78, 332-340.
15. Incardona, J. P., Collier, T. K., and Scholz, N. L. (2004). Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 196, 191-205.
16. Itakura, T., El-kady, M. A. H., Mitsuo, R., and Kaminishi, Y. (2005). Complementary DNA cloning and constitutive expression of cytochrome P450 1C1 in the gills of carp (Cyprinus carpio). Environ. Sci. 12(2), 111-120.
17. Karchner, S. I., Franks, D. G., Powell, W. H., and Hahn, M. E. (2002). Regulatory interactions among three members of the vertebrate aryl hydrocarbon receptor family: AhR repressor, AhR1 and AhR2. J. Biol. Chem. 277(9), 6949-6959.
18. Karchner, S. I., Powell, W. H., and Hahn, M. E. (1999). Identification and functional characterization of two highly divergent aryl hydrocarbon receptors (AhR1 and AhR2) in the teleost Fundulus heteroclitus. J. Biol. Chem. 274(47), 33814-33824.
19. Kim, J. H., Stansbury, K. H., Walker, N. J., Trush, M. A., Strickland, P. T., and Sutter, T. R. (1998). Metabolism of benzo(a)pyrene and benzo(a)pyrene-7,8-diol by human cytochrome P450 1B1. Carcinogenesis 19(10), 1847-1853.
20. Leaver, M. J., and George, S. G. (2000). A cytochrome P4501B gene from a fish, Pleuronectes platessa. Gene 256, 83-91.
21. Leblanc, J., Couillard, C. M., and Brethes, J.-C. F. (1997). Modification of the reproduction period in mummichog (Fundulus heteroclitus) living downstream from a bleached kraft pulp mill in the Miramichi Estuary, New Brunswick, Canada. Can. J. Fish. Aquat. Sci. 54, 2564-2573.
22. Merson, R. R., Franks, D. G., Karchner, S. I., and Hahn, M. E. (2006). Development and characterization of polyclonal antibodies against the aryl hydrocarbon receptor protein family (AHR1, AHR2, and AHR repressor) of Atlantic killifish Fundulus heteroclitus. Comp. Biochem. Physiol. 142(Part C), 85-94.
23. Meyer, J. N., Nacci, D., and Di Giulio, R. T. (2002). Cytochrome P4501A (CYP1A) in killifish (Fundulus heteroclitus): Heritability of altered expression and relationship to survival in contaminated sediments. Toxicol. Sci. 68, 69-81.
24. Meyer, J. N., Smith, J. D., Winston, G. W., and Di Giulio, R. T. (2003). Antioxidant defenses in killifish (Fundulus heteroclitus) exposed to contaminated sediments and model prooxidants: Short-term and heritable responses. Aquat. Toxicol. 65, 377-395.
25. Morrison, H. G., Oleksiak, M. F., Cornell, N. W., Sogin, M. L., and Stegeman, J. J. (1995). Identification of cytochrome P-450 1A (CYP1A) genes from two teleost fish, toadfish (Opsanus tau) and scup (Stenotomus chrysops), and phylogenetic analysis of CYP1A genes. Biochem. J. 308, 97-104.
26. Morrison, H. G., Weil, E. J., Karchner, S. I., Sogin, M. L., and Stegeman, J. J. (1998). Molecular cloning of CYP1A from the estuarine fish Fundulus heteroclitus and phylogenetic analysis of CYP1 genes: Update with new species. Comp. Biochem. Physiol. 121C, 231-240.
27. Murray, G. I., Melvin, W. T., Greenlee, W. F., and Burke, M. D. (2001). Regulation, function and tissue-specific expression of cytochrome P450 CYP1B1. Annu. Rev. Pharmacol. Toxicol. 41, 297-316.
28. Nacci, D., Coiro, L., Kuhn, A., Champlin, D., Munns, W., Specker, J., and Cooper, K. (1998). Nondestructive indicator of ethoxyresorufin-O-deethylase activity in embryonic fish. Environ. Toxicol. Chem. 17(12), 2481-2486.
29. Nacci, D. E., Kohan, M., Pelletier, M., and George, E. (2002). Effects of benzo(a)pyrene exposure on a fish population resistant to the toxic effects of dioxin-like compounds. Aquat. Toxicol. 57, 203-215.
30. Nebert, D. W., and Gonzalez, F. J. (1987). P450 genes: Structure, evolution, and regulation. Annu. Rev. Biochem. 56, 945-993.
31. Oleksiak, M. F., Wu, S., Parker, C., Karchner, S. I., and Stegeman, J. J. (2000). Identification, functional characterization, and regulation of a new cytochrome P450 subfamily, the CYP2Ns. J. Biol. Chem. 275, 2312-2321.
32. Patel, M. R., Scheffler, B. E., Wang, L., and Willett, K. L. (2006). Effects of benzo(a)pyrene exposure on killifish (Fundulus heteroclitus) aromatase activities and mRNA. Aquat. Toxicol. 77, 267-278.
33. Payne, J. F., and Penrose, W. R. (1975). Induction of aryl hydrocarbon (benzo(a)pyrene) hydroxylase in fish by petroleum. Bull. Environ. Contam. Toxicol. 14, 112-116.
34. Powell, W. H., Karchner, S. I., Bright, R., and Hahn, M. E. (1999). Functional diversity of vertebrate ARNT proteins: Identification of ARNT2 as the predominant form of ARNT in the marine teleost, Fundulus heteroclitus. Arch. Biochem. Biophys. 361(1), 156-163.
35. Savas, U., Bhattacharyya, K. K., Christou, M., Alexander, D. L., and Jefcoate, C. R. (1994). Mouse cytochrome P-450EF, representative of a new 1B subfamily of cytochrome P-450s. Cloning, sequence determination, and tissue expression. J. Biol. Chem. 269, 14905-14911.
36. Shen, Z., Liu, J., Wells, R. L., and Elkind, M. M. (1994). cDNA cloning, sequence analysis, and induction by aryl hydrocarbons of a murine cytochrome P450 gene, Cyp1b1. DNA Cell Biol. 13(7), 763-769.
37. Shimada, T., Gillam, E. M., Oda, Y., Tsumura, F., Sutter, T. R., Guengerich, F. P., and Inoue, K. (1999a). Metabolism of benzo(a)pyrene to trans-7,8-dihydroxy-7,8-dihydrobenzo(a)pyrene by recombinant human cytochrome P4501B1 and purified liver epoxide hydrolase. Chem. Res. Toxicol. 12, 623-629.
38. Shimada, T., Watanabe, J., Kawajiri, K., Sutter, T. R., Guengerich, F. P., Gillam, E. M. J., and Inoue, K. (1999b). Catalytic properties of polymorphic human cytochrome P4501B1 variants. Carcinogenesis 20(8), 1607-1613.
39. Sutter, T. R., Tang, Y. M., Hayes, C. L., Wo, Y.-Y., Jabs, E. W., Li, X., Yin, H., Cody, C. W., and Greenlee, W. F. (1994). Complete cDNA sequence of a human dioxin-inducible mRNA identifies a new gene subfamily of cytochrome P450 that maps to chromosome 2. J. Biol. Chem. 269(18), 13092-13099.
40. Vogelbein, W. K., Fournie, J. W., Van Veld, P. A., and Huggett, R. J. (1990). Hepatic neoplasms in the mummichog Fundulus heteroclitus from a creosote-contaminated site. Cancer Res. 50, 5978-5986.
41. Wassenberg, D. M., and Di Giulio, R. T. (2004). Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environ. Health Perspect. 112, 1658-1664.
42. Willett, K., Steinberg, M. A., Thomsen, J., Narasimhan, T. K., Safe, S. H., McDonald, S. J., Beatty, K. B., and Kennicutt, M. C. (1995). Exposure of killifish to benzo(a)pyrene: Comparative metabolism, DNA adduct formation and aryl hydrocarbon (Ah) receptor agonist activities. Comp. Biochem. Physiol. 112B(1), 93-103.
43. Willett, K. L., Ganesan, S., Patel, M., Metzger, C., Quiniou, S., Waldbieser, G., and Scheffler, B. (2006). In vivo and in vitro CYP1B mRNA expression in channel catfish. Mar. Environ. Res. 62, S332-S336.
44. Willett, K. L., Wassenberg, D., Lienesch, L., Di Giulio, R. T., and Reichert, W. L. (2001). In vivo and in vitro inhibition of CYP1A-dependent activity in Fundulus heteroclitus by the polynuclear aromatic hydrocarbon (PAH) fluoranthene. Toxicol. Appl. Pharmacol. 177, 264-271.
45. Wirgin, I., and Waldman, J. R. (1998). Altered gene expression and genetic damage in North American fish populations. Mutat. Res. 399, 193-219.
46. Zhou, T., John-Alder, H. B., Weis, J. S., and Weis, P. (2000). Endocrine disruption: Thyroid dysfunction in mummichogs (Fundulus heteroclitus) from a polluted habitat. Mar. Environ. Res. 50(1-5), 393-397.