Induction of cytochrome P450 1 genes and stress response genes in developing zebrafish exposed to ultraviolet radiation

Aquatic Toxicology

Volumn 98, Issue 1, 2010, Pages 74-82

  Behrendt, Lars ^a   Jönsson, Maria E ^a,b   Goldstone, Jared V ^a   Stegeman, John J ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

CYP1A; Cytochrome P450; SOD; Ultraviolet radiation; UVA; UVB; Zebrafish

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; CYCLINE; CYTOCHROME P450; CYTOCHROME P450 1A; CYTOCHROME P450 1B1; CYTOCHROME P450 1C1; CYTOCHROME P450 1C2; CYTOCHROME P450 1D1; UNCLASSIFIED DRUG;

CYTOCHROME; EMBRYO; EMBRYONIC DEVELOPMENT; FERTILIZATION (REPRODUCTION); FISH; GENE EXPRESSION; MORTALITY; PHYSIOLOGICAL RESPONSE; RADIATION DAMAGE; RADIATION EXPOSURE; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO MORTALITY; GENE EXPRESSION; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; RADIATION EXPOSURE; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION; ULTRAVIOLET RADIATION; UPREGULATION;

ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; STRESS, PHYSIOLOGICAL; ULTRAVIOLET RAYS; ZEBRAFISH;

DANIO RERIO; MAMMALIA;

EID: 77953683036     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.01.008     Document Type: Article

References (50)

1. Bittinger M.A., Nguyen L.P., Bradfield C.A. Aspartate aminotransferase generates proagonists of the aryl hydrocarbon receptor. Mol. Pharmacol. 2003, 64:550-556.
2. Black A.T., Gray J.P., Shakarjian M.P., Laskin D.L., Heck D.E., Laskin J.D. Distinct effects of ultraviolet B light on antioxidant expression in undifferentiated and differentiated mouse keratinocytes. Carcinogenesis 2008, 29:219-225.
3. Brash D.E. Sunlight and the onset of skin cancer. Trends Genet. 1997, 13:410-414.
4. Brash D.E., Rudolph J.A., Simon J.A., Lin A., McKenna G.J., Baden H.P., Halperin A.J., Ponten J. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:10124-10128.
5. Browman H.I., Vetter R.D., Rodriguez C.A., Cullen J.J., Davis R.F., Lynn E., St Pierre J.F. Ultraviolet (280-400nm)-induced DNA damage in the eggs and larvae of Calanus finmarchicus G. (Copepoda) and Atlantic cod (Gadus morhua). Photochem. Photobiol. 2003, 77:397-404.
6. Charron R.A., Fenwick J.C., Lean D.R., Moon T.W. Ultraviolet-B radiation effects on antioxidant status and survival in the zebrafish, Brachydanio rerio. Photochem. Photobiol. 2000, 72:327-333.
7. Choung B.Y., Byun S.J., Suh J.G., Kim T.Y. Extracellular superoxide dismutase tissue distribution and the patterns of superoxide dismutase mRNA expression following ultraviolet irradiation on mouse skin. Exp. Dermatol. 2004, 13:691-699.
8. Chowdhury G., Dostalek M., Hsu E.L., Nguyen L.P., Stec D.F., Bradfield C.A., Guengerich F.P. Structural identification of Diindole agonists of the aryl hydrocarbon receptor derived from degradation of indole-3-pyruvic acid. Chem. Res. Toxicol. 2009, 22:1905-1912.
9. Dahms, H.U., Lee, J.S., 2009. UV radiation in marine ectotherms: molecular effects and responses. Aquat. Toxicol, Epub December 4.
10. Diani-Moore S., Labitzke E., Brown R., Garvin A., Wong L., Rifkind A.B. Sunlight generates multiple tryptophan photoproducts eliciting high efficacy CYP1A induction in chick hepatocytes and in vivo. Toxicol. Sci. 2006, 90:96-110.
11. Dong Q., Svoboda K., Tiersch T.R., Monroe W.T. Photobiological effects of UVA and UVB light in zebrafish embryos: evidence for a competent photorepair system. J. Photochem. Photobiol. B 2007, 88:137-146.
12. Engeszer R.E., Patterson L.B., Rao A.A., Parichy D.M. Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 2007, 4:21-40.
13. Essers J., Theil A.F., Baldeyron C., van Cappellen W.A., Houtsmuller A.B., Kanaar R., Vermeulen W. Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol. 2005, 25:9350-9359.
14. Fritsche E., Schafer C., Calles C., Bernsmann T., Bernshausen T., Wurm M., Hubenthal U., Cline J.E., Hajimiragha H., Schroeder P., et al. Lightening up the UV response by identification of the arylhydrocarbon receptor as a cytoplasmatic target for ultraviolet B radiation. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:8851-8856.
15. Goerz G., Barnstorf W., Winnekendonk G., Bolsen K., Fritsch C., Kalka K., Tsambaos D. Influence of UVA and UVB irradiation on hepatic and cutaneous P450 isoenzymes. Arch. Dermatol. Res. 1996, 289:46-51.
16. Grubbs F.E. Procedures for detecting outlying observations in samples. Technometrics 1969, 11:1-21.
17. Häder D.P., Kumar H.D., Smith R.C., Worrest R.C. Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem. Photobiol. Sci. 2007, 6:267-285.
18. Hakkinen J., Vehniainen E., Oikari A. High sensitivity of northern pike larvae to UV-B but no UV-photoinduced toxicity of retene. Aquat. Toxicol. 2004, 66:393-404.
19. Hall P.A., McKee P.H., Menage H.D., Dover R., Lane D.P. High levels of p53 protein in UV-irradiated normal human skin. Oncogene 1993, 8:203-207.
20. Hunter J.R., Taylor J.H., Moser H.G. Effect of ultraviolet irradiation on eggs and larvae on the northern anchovy, Engraulis mordax, and the Pacific mackerel, Scomber japonicus, during the embryonic stage. Photochem. Photobiol. 1979, 29:325-338.
21. Isoherranen K., Peltola V., Laurikainen L., Punnonen J., Laihia J., Ahotupa M., Punnonen K. Regulation of copper/zinc and manganese superoxide dismutase by UVB irradiation, oxidative stress and cytokines. J. Photochem. Photobiol. B 1997, 40:288-293.
22. Jönsson M.E., Franks D.G., Woodin B.R., Jenny M.J., Garrick R.A., Behrendt L., Hahn M.E., Stegeman J.J. The tryptophan photoproduct 6-formylindolo[3,2-b]carbazole (FICZ) binds multiple AHRs and induces multiple CYP1 genes via AHR2 in zebrafish. Chem. Biol. Interact. 2009, 181:447-454.
23. Katiyar S.K., Matsui M.S., Mukhtar H. Ultraviolet-B exposure of human skin induces cytochromes P450 1A1 and 1B1. J. Invest. Dermatol. 2000, 114:328-333.
24. Katsumi S., Kobayashi N., Imoto K., Nakagawa A., Yamashina Y., Muramatsu T., Shirai T., Miyagawa S., Sugiura S., Hanaoka F., et al. In situ visualization of ultraviolet-light-induced DNA damage repair in locally irradiated human fibroblasts. J. Invest. Dermatol. 2001, 117:1156-1161.
25. Kocarek T.A., Schuetz E.G., Guzelian P.S. Transient induction of cytochrome P450 1A1 mRNA by culture medium component in primary cultures of adult rat hepatocytes. In Vitro Cell Dev. Biol. 1993, 29A:62-66.
26. Lambertini L., Surin K., Ton T.V., Clayton N., Dunnick J.K., Kim Y., Hong H.H., Devereux T.R., Sills R.C. Analysis of p53 tumor suppressor gene, H-ras protooncogene and proliferating cell nuclear antigen (PCNA) in squamous cell carcinomas of HRA/Skh mice following exposure to 8-methoxypsoralen (8-MOP) and UVA radiation (PUVA therapy). Toxicol. Pathol. 2005, 33:292-299.
27. Laub L.B., Jones B.D., Powell W.H. Responsiveness of a Xenopus laevis cell line to the aryl hydrocarbon receptor ligands 6-formylindolo[3,2-b]carbazole (FICZ) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Chem. Biol. Interact. 2010, 183:202-211.
28. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2DeltaDeltaCT method. Methods 2001, 25:402-408.
29. Maeda T., Chua P.P., Chong M.T., Sim A.B., Nikaido O., Tron V.A. Nucleotide excision repair genes are upregulated by low-dose artificial ultraviolet B: evidence of a photoprotective SOS response?. J. Invest. Dermatol. 2001, 117:1490-1497.
30. McCurley A.T., Callard G.V. Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol. Biol. 2008, 9:102.
31. McKenzie R.L., Aucamp P.J., Bais A.F., Bjorn L.O., Ilyas M. Changes in biologically-active ultraviolet radiation reaching the Earth's surface. Photochem. Photobiol. Sci. 2007, 6:218-231.
32. Moore J.O., Palep S.R., Saladi R.N., Gao D., Wang Y., Phelps R.G., Lebwohl M.G., Wei H. Effects of ultraviolet B exposure on the expression of proliferating cell nuclear antigen in murine skin. Photochem. Photobiol. 2004, 80:587-595.
33. Mukai M., Tischkau S.A. Effects of tryptophan photoproducts in the circadian timing system: searching for a physiological role for aryl hydrocarbon receptor. Toxicol. Sci. 2007, 95:172-181.
34. Nair S., Kekatpure V.D., Judson B.L., Rifkind A.B., Granstein R.D., Boyle J.O., Subbaramaiah K., Guttenplan J.B., Dannenberg A.J. UVR exposure sensitizes keratinocytes to DNA adduct formation. Cancer Prev. Res. (Phila Pa) 2009, 2:895-902.
35. (NCAR/ACD) National Center for Atmospheric Research Tropospheric Ultraviolet & Visible Radiation Model 2009, NCAR/ACD TUV.
36. Nguyen L.P., Hsu E.L., Chowdhury G., Dostalek M., Guengerich F.P., Bradfield C.A. d-amino acid oxidase generates agonists of the aryl hydrocarbon receptor from d-tryptophan. Chem. Res. Toxicol. 2009, 22:1897-1904.
37. Oberg M., Bergander L., Hakansson H., Rannug U., Rannug A. Identification of the tryptophan photoproduct 6-formylindolo[3,2-b]carbazole, in cell culture medium, as a factor that controls the background aryl hydrocarbon receptor activity. Toxicol. Sci. 2005, 85:935-943.
38. Pence B.C., Naylor M.F. Effects of single-dose ultraviolet radiation on skin superoxide dismutase, catalase, and xanthine oxidase in hairless mice. J. Invest. Dermatol. 1990, 95:213-216.
39. Punnonen K., Lehtola K., Autio P., Kiistala U., Ahotupa M. Chronic UVB irradiation induces superoxide dismutase activity in human epidermis in vivo. J. Photochem. Photobiol. B 1995, 30:43-48.
40. Rowland F.S. Stratospheric ozone depletion. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2006, 361:769-790.
41. Salo D.C., Pacifici R.E., Lin S.W., Giulivi C., Davies K.J. Superoxide dismutase undergoes proteolysis and fragmentation following oxidative modification and inactivation. J. Biol. Chem. 1990, 265:11919-11927.
42. Setlow R.B. The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc. Natl. Acad. Sci. U.S.A. 1974, 71:3363-3366.
43. Tedetti M., Sempere R., Vasilkov A., Charriere B., Nerini D., Miller W.L., Kawamura K., Raimbault P. High penetration of ultraviolet radiation in the south east Pacific waters. Geophys. Res. Lett. 2007, 34:L12610.
44. Vega M.P., Pizarro R.A. Oxidative stress and defence mechanisms of the freshwater cladoceran Daphnia longispina exposed to UV radiation. J. Photochem. Photobiol. B 2000, 54:121-125.
45. Vehniainen E.R., Hakkinen J., Oikari A. Photoinduced lethal and sublethal toxicity of retene, a polycyclic aromatic hydrocarbon derived from resin acid, to coregonid larvae. Environ. Toxicol. Chem. 2003, 22:2995-3000.
46. Wei Y.D., Bergander L., Rannug U., Rannug A. Regulation of CYP1A1 transcription via the metabolism of the tryptophan-derived 6-formylindolo[3,2-b]carbazole. Arch. Biochem. Biophys. 2000, 383:99-107.
47. Wei Y.D., Rannug U., Rannug A. UV-induced CYP1A1 gene expression in human cells is mediated by tryptophan. Chem. Biol. Interact. 1999, 118:127-140.
48. Wincent E., Amini N., Luecke S., Glatt H., Bergman J., Crescenzi C., Rannug A., Rannug U. The suggested physiologic aryl hydrocarbon receptor activator and cytochrome P4501 substrate 6-formylindolo[3,2-b]carbazole is present in humans. J. Biol. Chem. 2009, 284:2690-2696.
49. Zagarese H.E., Williamson C.E. The implications of solar UV radiation exposure for fish and fisheries. Fish Fisheries 2001, 2:250-260.
50. Zeng X.R., Jiang Y., Zhang S.J., Hao H., Lee M.Y. DNA polymerase delta is involved in the cellular response to UV damage in human cells. J. Biol. Chem. 1994, 269:13748-13751.