Identification of a CYP3A-like gene and CYPs mRNA expression modulation following exposure to benzo[a]pyrene in the bivalve mollusk Chlamys farreri

Marine Environmental Research

Volumn 94, Issue , 2014, Pages 7-15

  Tian, Shuangmei ^a   Pan, Luqing ^a   Zhang, Hui ^a  

^a Ocean University of China   (China)

Author keywords

Benzo a pyrene; Chlamys farreri; CYP3A like; CYPs expression; Ecotoxicology; MRNA; Pollution effects

Indexed keywords

BENZO [A] PYRENE; CHLAMYS FARRERI; CYP3A-LIKE; CYPS EXPRESSION; ECO-TOXICOLOGY; MRNA; POLLUTION EFFECTS;

BIOCHEMISTRY; MOLLUSCS; NUCLEIC ACIDS; PYRENE; SHELLFISH;

GENE EXPRESSION;

BENZO[A]PYRENE; CYTOCHROME P450 3A; MESSENGER RNA; POLYCYCLIC AROMATIC HYDROCARBON;

BIVALVE; DNA; ECOTOXICOLOGY; GENE EXPRESSION; GENOTOXICITY; METABOLISM; PAH; POLLUTION EFFECT; PYRENE; RNA; STEROID; XENOBIOTICS;

ARTICLE; BINDING SITE; CHLAMYS FARRERI; CONTROLLED STUDY; CYP3A LIKE GENE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; GENE EXPRESSION; GENE IDENTIFICATION; GENOTOXICITY; LIPID PEROXIDATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PHYLOGENY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SEQUENCE ALIGNMENT; STEROID METABOLISM; XENOBIOTIC METABOLISM;

BIVALVIA; CHLAMYS FARRERI; PECTINIDAE;

BENZO[A]PYRENE; B[A]P; CHLAMYS FARRERI; CYP3A-LIKE; CYPS EXPRESSION; ECOTOXICOLOGY; MRNA; PAHS; POLLUTION EFFECTS; POLYCYCLIC AROMATIC HYDROCARBONS;

AMINO ACID SEQUENCE; ANIMALS; BENZO(A)PYRENE; CYTOCHROME P-450 CYP3A; DNA DAMAGE; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; OVARY; OXIDATIVE STRESS; PECTINIDAE; PHYLOGENY; RNA, MESSENGER; SEQUENCE ALIGNMENT; WATER POLLUTANTS, CHEMICAL;

EID: 84893010847     PISSN: 01411136     EISSN: 18790291     Source Type: Journal    
DOI: 10.1016/j.marenvres.2013.11.001     Document Type: Article

References (67)

1. Barouki R., Morel Y. Repression of cytochrome P450 1A1 gene expression by oxidative stress: mechanisms and biological implications. Biochem. Pharmacol. 2001, 61:511-516.
2. Benedetti M., Martuccio G., Fattorini D., Canapa A., Barucca M., Nigro M., Regoli F. Oxidative and modulatory effects of trace metals on metabolism of polycyclic aromatic hydrocarbons in the Antarctic fish Trematomus bernacchii. Aquat. Toxicol. 2007, 85:167-175.
3. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 1976, 72:248-254.
4. Butler R.A., Kelley M.L., Olberding K.E., Gardner G.R., Van Beneden R.J. Aryl hydrocarbon receptor (AHR)-independent effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on softshell clam (Mya arenaria) reproductive tissue. Comp. Biochem. Physio. Part C Toxicol. Pharmacol. 2004, 138:375-381.
5. Canova S., Degan P., Peters L.D., Livingstone D.R., Voltan R., Venier P. Tissue dose, DNA adducts, oxidative DNA damage and CYP1A-immunopositive proteins in mussels exposed to waterborne benzo[a]pyrene. Mutat. Res. 1998, 399:17-30.
6. Celander M.C., Moore M.J., Stegeman J.J. Cellular localization of CYP3A proteins in various tissues from pilot whale (Globicephala melas). Environ. Toxicol. Pharmacol. 2000, 8:245-253.
7. Ching E.W.K., Siu W.H.L., Lam P.K.S., Xu L., Zhang Y., Richardson B., Wu R.S.S. DNA adduct formation and DNA strand breaks in green-lipped mussels (P. viridis) exposed to benzo[a]pyrene: dose- and time-dependent relationships. Mar. Pollut. Bull. 2001, 42:603-610.
8. Chipman J.K., Livingstone D.R., Marsh J.W. Mechanism of xenobiotic activation in marine invertebrates. Role Enzymes Xenobiot. Toxic. 1991, 19:751-755.
9. Cubero-Leon E., Puinean A.M., Labadie P., Ciocan C., Itoh N., Kishida M., Osada M., Minier C., Hill E.M., Rotchell J.M. Two CYP3A-like genes in the marine mussel Mytilus edulis: mRNA expression modulation following short-term exposure to endocrine disruptors. Mar. Environ. Res. 2012, 74:32-39.
10. Daniel F.B., Haas D.L., Santi L. Quantitation of chemically induced DNA strand breaks in human cells via an alkaline unwinding assay. Anal. Biochem. 1985, 144:390-402.
11. Danielson P.B. The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. Curr. Drug Metab. 2002, 3:561-597.
12. Danielson P.B., Foster J.L., Mchill M.M., Smith M.K., Fogleman J.C. Induction by alkaloids and phenobarbital of family 4 cytochrome P450s in Drosophila: evidence for involvement in host plant utilization. Mol. Gen. Genet. 1998, 259:54-59.
13. Della Torre C., Corsi I., Nardi F., Perra G., Tomasino M.P., Focardi S. Transcriptional and post-transcriptional response of drug-metabolizing enzymes to PAHs contamination in red mullet (Mullus barbatus, Linnaeus, 1758): a field study. Mar. Environ. Res. 2010, 70(1):95-101.
14. Denison M.S., Pandini A., Nagy S.R., Baldwin E.P., Bonati L. Ligand binding and activation of the Ah receptor. Chem.-Biol. Interac. 2002, 141:3-24.
15. Gagné F., Blaise C., Hellou J. Endocrine disruption and health effects of caged mussels, Elliptio complanata, placed downstream from a primary-treated municipal effluent plume for one year. Comp. Biochem. Physiol. Part C 2004, 138(1):33-44.
16. Guo H., Bao Z., Du H., Zhang L., Wang S., Sun L., Mou X., Hu X. Identification of cytochrome P450 (CYP) genes in Zhikong scallop (Chlamys farreri). J. Ocean Univ. Ch. 2013, 12(1):97-102.
17. Hahn M.E. Aryl hydrocarbon receptors: diversity and evolution. Chem.-Biol. Interac. 2002, 141:131-160.
18. Hegelund T., Celander M.C. Hepatic versus extrahepatic expression of CYP3A30 and CYP3A56 in adult kill fish (Fundulus heteroclitus). Aquat. Toxicol. 2003, 6(4):277-291.
19. Horiguchi T., Nishikawa T., Ohta Y., Shiraishi H., Morita M. Retinoid X receptor gene expression and protein content in tissues of the rock shell Thais clavigera. Aquat. Toxicol. 2007, 84:379-388.
20. Jing-Jing M., Lu-qing P., Jing L., Lin Z. Effects of benzo[a]pyrene on DNA damage and histological alterations in gonad of scallop Chlamys farreri. Mar. Environ. Res. 2009, 67:47-52.
21. Jørgensen A., Rasmussen L.J., Andersen O. Characterisation of two novel CYP4 genes from the marine polychaete Nereis virens and their involvement in pyrene hydroxylase activity. Biochem. Biophys. Res. Commun. 2005, 336:890-897.
22. Kirischian N.L., Wilson J.Y. Phylogenetic and functional analyses of the cytochrome P450 family 4. Mol. Phylogenet. Evol. 2011, 62:458-471.
23. Kullman S.W., Hinton D.E. Identification, characterization, and ontogeny of a second cytochrome P4503A gene from the fresh water teleost medaka (Oryzias latipes). Mol. Reprod. Dev. 2001, 58:149-158.
24. Kumagai T., Suzuki H., Sasaki T., Sakaguchi S., Miyairi S., Yamazoe Y., Nagata K. Polycyclic aromatic hydrocarbons activate CYP3A4 gene transcription through human pregnane X receptor. Drug Metab. Pharmacol. 2012, 27:200-206.
25. Lee S.J., Wang-Buhler J.L., Cok I., Yu T.S., Yang Y.H., Miranda C.L., Lech J., Buhler D.R. Cloning, sequencing, and tissue expression of CYP3A27, a new member of the CYP3A subfamily from embryonic and adult rainbow trout livers. Arch. Biochem. Biophys. 1998, 360:53-61.
26. Li B., Bisgaarda H.C., Forbes V.E. Identification and expression of two novel cytochrome P450 genes, belonging to CYP4 and a new CYP331 family, in the polychaete Capitella capitata sp. I. Biochem. Biophys. Res. Commun. 2004, 325:510-517.
27. Liu N., Pan L., Miao J., Xu C., Zhang L. Molecular cloning and sequence analysis and the response of a aryl hydrocarbon receptor homologue gene in the clam Ruditapes philippinarum exposed to benzo(a)pyrene. Comp. Biochem. Physio. Part C 2010, 152:279-287.
28. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-delta delta C) method. Methods 2001, 25:402-408.
29. Manoli E., Samara C. Polycyclic aromatic hydrocarbons in natural waters: sources, occurrence and analysis. TrAC-Trend. Anal. Chem. 1999, 18:417-428.
30. Martinez P.G., Livingstone D.R. Benzo[a]pyrene-dione-stimulated oxyradical production by microsomes of digestive gland of the common mussel, M. edulis L. Mar. Environ. Res. 1995, 39:185-189.
31. Mecocci P., Fanó G., Fulle S., MacGarvey U., Shinobu L., Polidori M.C., Cherubini A., Vecchiet J., Senin U., Beal M.F. Age-dependent increases in oxidative damage to DNA, lipids, and proteins in human skeletal muscle. Free Radic. Biol. Med. 1999, 26:303-308.
32. Miao J., Pan L., Liu N., Xu C., Zhang L. Molecular cloning of CYP4 and GSTpi homologues in the scallop Chlamys farreri and its expression in response to benzo[a]pyrene exposure. Mar. Genom. 2011, 4:99-108.
33. Monari M., Cattani O., Serrazanetti G.P., Selli A., Pagliuca G., Zironi E., O'Hara S.C.M., Livingstone D.R. Effect of exposure to benzo[a]pyrene on SODs, CYP1A1/1A2- and CYP2E1 immunopositive proteins in the blood clam Scapharca inaequivalvis. Mar. Environ. Res. 2007, 63:200-218.
34. Monari M., Foschi J., Matozzo V., Marin M.G., Fabbri M., Rosmini R., Serrazanetti G.P. Investigation of EROD, CYP1A immunopositive proteins and SOD in haemocytes of Chamelea gallina and their role in response to B[a]P. Comp. Biochem. Physiol. Part C 2009, 149:382-392.
35. Morel Y., Barouki R. Down-regulation of cytochrome P450 1A1 gene promoter by oxidative stress. J. Biol. Chem. 1998, 273(41):26969-26976. Critical contribution of nuclear factor 1.
36. Nebert D.W., Russell D.W. Clinical importance of the cytochromes P450. The Lancet 2002, 360:1155-1162.
37. Nishikawa J., Mamiya S., Kanayama T., Nishikawa T., Shiraishi F., Horiguchi T. Involvement of the retinoid X receptor in the development of imposex caused by organotins in gastropods. Environ. Sci. Technol. 2004, 38:6271-6276.
38. Pan L., Liu N., Xu C., Miao J. Identification of a novel P450 gene belonging to the CYP4 family in the clam Ruditapes philippinarum, and analysis of basal- and benzo(a)pyrene-induced mRNA expression levels in selected tissues. Environ. Toxicol. Pharmacol. 2011, 32:390-398.
39. Pan L.Q., Miao J.J., Wang J., Liu J. AHH activity, tissue dose and DNA damage in different tissues of the scallop Chlamys farreri exposed to benzo[a]pyrene. Environ. Pollut. 2008, 153:192-198.
40. Peters L.D., Nasci C., Livingstone D.R. Immunochemical investigations of cytochrome P450 forms/epitopes (CYP1A, 2B, 2E, 3A and 4A) in digestive gland of Mytilus spp. Comp. Biochem. Physiol. Part C 1998, 121:361-369.
41. Porte C., Biosca X., Sole M., Albaiges J. The integrated use of chemical analysis, cytochrome P450 and stress proteins in mussels to assess pollution along the Galician coast (NW, Spain). Environ. Pollut. 2001, 112:261-268.
42. Qin H., Powell-Coffman J.A. The Caenorhabditis elegans aryl hydrocarbon receptor, AHR-1, regulates neuronal development. Dev. Biol. 2004, 270:64-75.
43. Qiu Y.W., Zhou J.L., Maskaoui K., Hong H.S., Wang Z.D. Distribution of polycyclic aromatic hydrocarbons in water and sediments from Daya Bay and their ecological hazard assessment. J. Tropic. Oceangr. 2004, 23:72-80.
44. Rewitz K.F., Kjellerup C., Jørgensen A., Petersen C., Andersen O. Identification of two Nereis virens (Annelida: Polychaeta) cytochromes P450 and induction by xenobiotics. Comp. Biochem. Physiol. C. 2004, 138:89-96.
45. Rewitz K.F., Styrishave B., Lbner-Olesen A., Anderson O. Marine invertebrate cytochrome P450: emerging insights from vertebrate and insect analogies. Comp. Biochem. Physiol. C 2006, 143:363-381.
46. Schirmer K., Dixon D.G., Greenberg B.M., Bols N.C. Ability of 16 priority PAHs to be directly cytotoxic to a cell line from the rainbow trout gill. Toxicology 1998, 127:129-141.
47. Scott J.A., Collins F.H., Feyereisen R. Diversity of cytochrome P450 genes in the mosquito, Anopheles albimanus. Biochem. Biophys. Res. Commun. 1994, 205:1452-1459.
48. Shaw J.P., Large A.T., Livingstone D.R., Doyotte A., Renger J., Chipman J.K., Peters L.D. Elevation of cytochrome P450-immunopositive protein and DNA damage in mussels (Mytilus edulis) transplanted to a contaminated site. Mar. Environ. Res. 2002, 54:505-509.
49. Shaw J.P., Peters L.D., Chipman J.K. CYP1A- and CYP3A-immunopositive protein levels in digestive gland of the mussel Mytilus galloprovincialis from the Mediterranean Sea. Mar. Environ. Res. 2004, 58:649-653.
50. Snyder M.J. Cytochrome P450 enzymes belonging to the CYP4 family from marine invertebrates. Biochem. Biophys. Res. Comm. 1998, 249:187-190.
51. Sole M., Livingstone D.R. Components of the cytochrome P450-dependent monooxygenase system and 'NADPH-independent benzo[a]pyrene hydroxylase' activity in a wide range of marine invertebrate species. Comp. Biochem. Physio. Part C 2005, 141:20-31.
52. Stegeman J.J. Benzo(a)pyrene oxidation and microsomal enzyme activity in the mussel Mytilus edulis and other bivalve mollusc species from the Western North Atlantic. Mar. Biol. 1985, 89(1):21-30.
53. Stegeman J.J., Lech J.J. Cytochrome P-450 monooxygenase systems in aquatic species: carcinogen metabolism and biomarkers for carcinogen and pollutant exposure. Environ. Health Perspect. 1991, 90:101-109.
54. Sternberg R.M., Hotchkiss A.K., Leblanc G.A. Synchronized expression of retinoid X receptor mRNA with reproductive tract recrudescence in an imposex-susceptible mollusc. Environ. Sci. Technol. 2008, 42:1345-1351.
55. Tian S., Pan L., Sun X. An investigation of endocrine disrupting effects and toxic mechanisms modulated by benzo [a] pyrene in female scallop Chlamys farreri. Aquat. Toxicol. 2013, 144:162-171.
56. US Environmental Protection Agency (EPA): Method 8100, Rev.0, Polynuclear Aromatic Hydrocarbons Compendium Method TO-13: the Determination of Benzo[a]pyrene (B[a]P) and Other Polynuclear Aromatic Hydrocarbons (PAHs) in Ambient Air Using Gas Chromatographic (GC) and High Performance Liquid Chromatographic (HPLC) Analysis 1998, Available from:. http://www.epa.gov/epahome/index.
57. Verslycke T., Goldstone J., Stegeman J.J. Isolation and phylogeny of 4 novel CYP3A genes from the ascidian Ciona intestinalis. Mar. Environ. Res. 2006, 62:S75.
58. Verslycke T., Goldstone J.V., Stegeman J.J. Isolation and phylogeny of novel cytochrome P450 genes from tunicates (Ciona spp.): a CYP3 line in early deuterostomesα. Mol. Phylogenet. Evol. 2006, 40:760-771.
59. Wills E.D. Evaluation of lipid peroxidation in lipids and biological membranes. Biochem. Toxicol: a Practical Approach 1987, 127-152. IRL Press, Washington. K. Snell, B. Mullock (Eds.).
60. Won E.J., Rhee J.S., Shin K.H., Jung J.H., Shim W.J., Lee Y.M., Lee J.S. Expression of three novel cytochrome P450 (CYP) and antioxidative genes from the polychaete, Perinereis nuntia exposed to water accommodated fraction (WAF) of Iranian crude oil and Benzo[a]pyrene. Mar. Environ. Res. 2013, 90:75-84.
61. Wootton A.N., Herring C., Spry J.A., Wiseman A., Livingstone D.R., Goldfarb P.S. Evidence for the existence of cytochrome P450 genes families (CYP1A, 3A, 4A, 11A) and modulation of gene expression (CYP1A) in the mussel Mytilus spp. Mar. Environ. Res. 1995, 39:21-26.
62. Yadetie F., Butcher S., Førde H.E., Campsteijn C., Bouquet J.M., Karlsen O.A., Denoeud F., Metpally R., Thompson E.M., Manak J.R., Gok søyr A., Chourrout D. Conservation and divergence of chemical defense system in the tunicate Oikopleura dioica revealed by genome wide response to two xenobiotics. BMC Genomics 2012, 2(13):55.
63. Zanette J., Goldstone J.V., Bainy A.C., Stegeman J.J. Identification of CYP genes in Mytilus (mussel) and Crassostrea(oyster) species: first approach to the full complement of cytochrome P450 genes in bivalves. Mar. Environ. Res. 2010, 69:S1-S3.
64. Zanette J., Jenny M.J., Goldstone J.V., Parente T., Woodin B.R., Bainy A.C., Stegeman J.J. Identification and expression of multiple CYP1-like and CYP3-like genes in the bivalve mollusk Mytilus edulis. Aquat. Toxicol. 2013, 128-129:101-112.
65. Zhang Y., Song J., Yuan H., Xu Y., He Z., Duan L. Biomarker responses in the bivalve (Chlamys farreri) to exposure of the environmentally relevant concentrations of lead, mercury, copper. Environ. Toxicol. Pharmacol. 2010, 30(1):19-25.
66. Zheng S., Chen B., Qui X., Lin K., Yu X. Three novel cytochrome P450 genes identified in the marine polychaete Perinereis nuntia and their transcriptional responses to xenobiotics. Aquat. Toxicol. 2013, 134-135:11-22.
67. Zheng S., Qui X., Chen B., Yu X., Lin K., Bian M., Liu Z., Huang H., Yu W. Toxicity evaluation of benzo[a]pyrene on the polychaete Perinereis nuntia using subtractive cDNA libraries. Aquat. Toxicol. 2011, 105:279-291.