DNA damage and transcriptional changes induced by tributyltin (TBT) after short in vivo exposures of Chironomus riparius (Diptera) larvae

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 158, Issue 2, 2013, Pages 57-63

  Morales, Mónica ^a   Martínez Paz, Pedro ^a   Ozáez, Irene ^a   Martínez Guitarte, José Luis ^a   Morcillo, Gloria ^a  

^a UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

Author keywords

Ecdysone responsive genes; Endocrine disruptors; Hsp70; Nuclear receptor genes; Vitellogenin

Indexed keywords

DNA; ECDYSONE RECEPTOR; ECDYSTEROID; ESTROGEN RECEPTOR; HEAT SHOCK PROTEIN 70; TRIBUTYLTIN; VITELLOGENIN;

ANIMAL EXPERIMENT; ARTICLE; CHIRONOMUS RIPARIUS; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; DOWN REGULATION; GENE EXPRESSION; GENOTOXICITY; IN VIVO STUDY; LARVA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

CHIRONOMUS RIPARIUS; DIPTERA; HEXAPODA;

EID: 84886905941     PISSN: 15320456     EISSN: 18781659     Source Type: Journal    
DOI: 10.1016/j.cbpc.2013.05.005     Document Type: Article

References (59)

1. Antizar-Ladislao, B., 2008. Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review. Environ. Int. 34, 292-308. (Pubitemid 351232963)
2. Baken, K.A., Pennings, J.L.A., de Vries, A., Breit, T.M., van Steeg, H., van Loveren, H., 2006. Gene expression profiling of bis(tri-n-butyltin)oxide (TBTO) induced immunotoxicity in mice and rats. J. Immunotoxicol. 3, 227-244. (Pubitemid 44915798)
3. Castro, L.F., Lima, D., Machado, A., Melo, C., Hiromori, Y., Nishikawa, J., Nakanishi, T., Reis-Henriques, M.A., Santos, M.M., 2007. Imposex induction is mediated through the Retinoid X receptor signaling pathway in thneogastropod Nucella lapillus. Aquat. Toxicol. 85, 57-66. (Pubitemid 47419050)
4. Fent, K., 1996. Ecotoxicology of organotin compounds. Crit. Rev. Toxicol. 26, 3-117.
5. Ferraro, M.V.M., Fenocchio, A.S., Mantovani, M.S., Ribeiro, C.D., Cestari, M.M., 2004. Mutagenic effects of tributyltin and inorganic lead (Pb II) on the fish H. malabaricus as evaluated using the comet assay and the piscine micronucleus and chromosome aberration tests. Genet. Mol. Biol. 27, 103-107. (Pubitemid 38578877)
6. Gilbert, L.I., Warren, J.T., 2005. A molecular genetic approach to the biosynthesis of the insect steroid molting hormone. Vitam. Horm. 73, 31-57. (Pubitemid 43589059)
7. Gupta, S.C., Shrama, A., Mishra, M., Mishra, R.K., Chowdhuri, D.K., 2010. Heat shock proteins in toxicology: how close and how far? Life Sci. 86, 377-384.
8. Hagger, J.A., Depledge, M.H., Galloway, T.S., 2005. Toxicity of tributyltin in the marine mollusc Mytilus edulis. Mar. Pollut. Bull. 51, 811-816. (Pubitemid 41608835)
9. Hahn, T., Schulz, R., 2002. Ecdysteroid synthesis and imaginal disc development in the midge Chironomus riparius as biomarkers for endocrine effects of tributyltin. Environ. Toxicol. Chem. 21, 1052-1057. (Pubitemid 36091444)
10. Hannas, B.R., Wang, Y.H., Thomson, S., Kwon, G., Li, H., LeBlanc, G.A., 2011. Regulatin and dysregulation of vitellogenin mRNA accumulation in daphnids (Daphnia magna). Aquat. Toxicol. 101, 351-357.
11. Hirano, M., Ishibashi, H., Yamauchi, R., Kim, J.W., Arizono, K., 2008. Expression analysis of the ecdysone receptor and ultraspiracle through molting period in mysid crustacean, Americamysis bahia. In: Murakami, Y., Nakayama, K., Kitamura, S.I., Iwata, H., Tanabe, S. (Eds.), Interdisciplinary studies on environmental chemistry: Biological responses to chemical pollutans. Terraub, Tokyo, pp. 303-310.
12. Iguchi, T., 2007. Endocrine disrupting organotin compounds are potent inducers of imposex in gastropods and adipogenesis in vertebrates. Mol. Cell. Toxicol. 3, 1-10.
13. Jha, A.N., Hagger, J.A., Hill, S.J., 2000. Tributyltin induces cytogenetic damage in the early life stages of the marine mussel, Mytilus edulis. Environ. Mol. Mutagen. 35, 343-350. (Pubitemid 30434611)
14. Karim, F.D., Thummel, C.S., 1992. Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J. 11, 4083-4093.
15. Keay, J., Bridgham, J.T., Thornton, J.W., 2006. The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. Endocrinology 147, 3861-3869. (Pubitemid 44079391)
16. Koelle, M.R., Talbot, W.S., Segraves, W.A., Bender, M.T., Cherbas, P., Hogness, D.S., 1991. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67, 59-77. (Pubitemid 121001425)
17. Köhler, H.R., Kloas, W., Schirling, M., Lutz, I., Reye, A.L., Langen, J.S., Triebskorn, R., Nagel, R., Schönfelder, 2007. Sex steroid receptor evolution and signaling in aquatic invertebrates. Ecotoxicology 16, 131-146.
18. Lezzi, M., Bergman, T., Mouillet, J.F., Henrich, V.C., 1999. The ecdysone receptor puzzle. Arch. Insect Biochem. Physiol. 41, 99-106. (Pubitemid 129558087)
19. Lilley, T.M., Ruokolainen, L., Pikkarainen, A., Laine, V.N., Kilpimaa, J., Rantala, M.J., Nikinmaa, M., 2012. Impact of tributyltin on immune response and life history traits of Chironomus riparius: single and multigeneration effects and recovery to pollution. Environ. Sci. Technol. 46, 7382-7389.
20. Lima, D., Reis-Hemriques, M.A., Silva, R., Santos, A.I., Castro, L.F.C., Santos, M.M., 2011. Tributyltin-induced imposex in marine gastropods involves tissue specific modulation of the retinoid X receptor. Aquat. Toxicol. 101, 221-227.
21. Marinkovic, M., de Bruijn, K., Asselman, M., Bogaert, M., Jonker, M.J., Kraak, M.H.S., Admiraal, W., 2012. Response of the nonbiting midge Chironomus riparius to multigeneration toxicant exposure. Environ. Sci. Technol. 46, 12105-12111.
22. Marinkovic, M., de Leeuw, W.C., Ensink, W.A., de Jong, M., Breit, T.M., Admiraal, W., Kraak, M.H.S., Jonker, M.J., 2012. Gene expression patterns and life cycle responses of toxicant exposed chironomids. Environ. Sci. Technol. 46, 12679-12686.
23. Martínez-Guitarte, J.L., Planelló, R., Morcillo, G., 2007. Characterization and expression during development and under environmental stress of the genes encoding ribosomal proteins L11 and L13 in Chironomus riparius. Comp. Biochem. Physiol. B 147, 590-596. (Pubitemid 46929094)
24. Martinez-Guitarte, J.L., Planelló, R., Morcillo, G., 2012. Overexpression of long noncoding RNAs following exposure to xenobiotics in the aquatic midge Chironomus riparius. Aquat. Toxicol. 110-111, 84-90.
25. Martínez-Paz, P., Morales, M., Martínez-Guitarte, J.L., Morcillo, G., 2012. Characterization of a cytochrome P450 gene (CYP4G) and modulation under different exposures to xenobiotics (tributyltin, nonylphenol, bisphenol A) in Chironomus riparius aquatic larvae. Comp. Biochem. Physiol. C 155, 333-343.
26. Micael, J., Reis-Henriques, M.A., Carvalho, A.P., Santos, M.M., 2007. Genotoxic effects of binary mixtures of xenoandrogens (tributyltin, triphenyltin) and a xenoestrogen (ethinylestradiol) in a partial life-cycle test with Zebrafish (Danio rerio). Environ. Int. 33, 1035-1039. (Pubitemid 47483902)
27. Morales, M., Planelló, R., Martínez-Paz, P., Herrero, O., Cortés, E., Martínez-Guitarte, J.L., Morcillo, G., 2011. Characterization of Hsp70 gene in Chironomus riparius: expression in response to endocrine disrupting pollutants as a marker of ecotoxicological stress. Comp. Biochem. Physiol. C 153, 150-158.
28. Morcillo, Y., Janer, G., O'Hara, S.C., Livingstone, D.R., Porte, C., 2004. Interaction of tributyltin with hepatic cytochrome P450 and uridine diphosphate-glucuronosyl transferase systems of fish: in vitro studies. Environ. Toxicol. Chem. 23, 990-996. (Pubitemid 38418649)
29. Mortensen, A.S., Arukwe, A., 2007. Modulation of xenobiotic biotransformation system and hormonal responses in Atlantic salmon (Salmo salar) after exposure to tributyltin (TBT). Comp. Biochem. Physiol. C 145, 3431-3441.
30. Nair, P.M.G., Choi, J., 2012. Modulation of the mRNA expression of ecdysone receptor gene in aquatic midge, Chironomus riparius upon exposure to nonylphenol and silver nanoparticles. Environ. Toxicol. Pharmacol. 33, 98-106.
31. Nakanishi, T., 2008. Endocrine disruption induced by organotin compounds; organotins function as a powerful agonist for nuclear receptors rather the aromatase inhibitor. J. Toxicol. Sci. 33, 269-276.
32. Nishikawa, J., Mamiya, S., Kanayama, T., Nishikawa, T., Shiraishi, F., Horiguchi, T., 2004. Involvement of the retinoid X receptor in the development of imposex caused by organotins in gastropods. Environ. Sci. Technol. 38, 6271-6276. (Pubitemid 39578639)
33. Nolen, E.A.A., Morimoto, R.I., 2002. Chaperoning signalling pathways: molecular chaperones as stress-sensing heat shock proteins. J. Cell Sci. 115, 2809-2816.
34. Nowak, C., Vogt, C., Pfenninger, M., Schwenk, K., Oehlmann, J., Streit, B., Oetken, M., 2009. Rapid genetic erosion in pollutant-exposed experimental chironomid populations. Environ. Pollut. 157, 881-886.
35. OECD, 2001. Guideline for testing of chemicals, sedimentwater chironomid toxicity test using spiked sediment. 218.
36. Ozáez, I., Martínez-Guitarte, J.L., Morcillo, G., 2013. Effects of in vivo exposure to UV filters (4-MBC, OMC, BP-3, 4-HB, OC, OD-PABA) on endocrine signaling genes in the insect Chironomus riparius. Sci. Total. Environ. 456-457, 120-126.
37. Park, K., Kwak, I.S., 2010. Molecular effects of endocrine-disrupting chemicals on the Chironomus riparius estrogen-related receptor gene. Chemosphere 79, 934-941.
38. Park, K., Kim, R., Park, J.J., Shin, H.C., Lee, J.S., Cho, H.S., Lee, Y.G., Kim, J., Kwak, I.S., 2012. Ecotoxicological evaluation of tributyltin toxicity to the equilateral venus clam, Gomphina veneriformis (Bivalvia: Veneridae). Fish Shellfish Immunol. 32, 426-433.
39. Pascoal, S., Carvalho, G., Vasieva, O., Hughes, R., Cossins, A., Fang, Y., Ashelford, K., Olohan, L., Barroso, C., Mendo, S., Creer, S., 2013. Transcriptome and in vitro tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus. Mol. Ecol. 22, 1589-1608.
40. Planelló, R., Martínez-Guitarte, J.L., Morcillo, G., 2008. The endocrine disruptor bisphenol A increases the expression of HSP70 and ecdysone-receptor genes in the aquatic larvae of Chironomus riparius. Chemosphere 71, 1870-1876.
41. Planelló, R., Martínez-Guitarte, J.L., Morcillo, G., 2010. Effect of acute exposure to cadmium on the expression of heat-shock and hormone-nuclear receptor genes in the aquatic midge Chironomus riparius. Sci. Total. Environ. 408, 1598-1603.
42. Planelló, R., Herrero, O., Martínez-Guitarte, J.L., Morcillo, G., 2011. Comparative effects of butyl benzyl phthalate (BBP) and di-2-ethylhexyl phthalate (DEHP) on the aquatic larvae of Chironomus riparius based on gene expression assays related to the endocrine system, the stress response and ribosomes. Aquat. Toxicol. 105, 62-70.
43. Rauch, P., Grebe, M., Elke, C., Spindler, K.D., Spindler-Barth, M., 1998. Ecdysteroid receptor and ultraspiracle from Chironomus tentans (Insecta) are phosphoproteins and are regulated differently by molting hormone. Insect Biochem. Mol. Biol. 28, 265-275. (Pubitemid 28313404)
44. Ryan, J.A., Hightower, L.E., 1998. Heat shock proteins: molecular biomarkers of effects. In: Puga, A., Wallale, K.B. (Eds.), Molecular Biology of the Toxic Response. Hamilton Printing Co., Castlton, New York, pp. 449-466.
45. Sheng, Z., Xu, J., Palli, S.R., 2011. Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum. J. Biol. Chem. 286, 41924-41936.
46. Shimazaki, Y., Kitano, T., Oshima, Y., Inuoe, S., Imada, N., Honjo, T., 2003. Tributyltin causes masculinization in fish. Environ. Toxicol. Chem. 22, 141-144. (Pubitemid 35471331)
47. Singh, N.P., McCoy, M.T., Tice, R.R., Schneider, E.L., 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175, 184-191.
48. Stange, D., Sieratowicz, A., Oehlmann, J., 2012. Imposex development in Nucella lapillus. Evidence for the involvement of retinoid X receptor and androgen signaling pathways in vivo. Aquat. Toxicol. 106-107, 20-24.
49. Stenberg, R., Gooding, M., Hotchkiss, A., Le Blanc, G., 2010. Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs. Ecotoxicology 19, 4-23.
50. Thornton, J.W., Need, E., Crews, D., 2003. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301, 1714-1717. (Pubitemid 37174363)
51. Thummel, C.S., 1996. Flies on steroids-Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet. 12, 306-310. (Pubitemid 26258356)
52. Tyler, C.R., Van Aerle, R., Hutchinson, T.H., Maddix, S., Trip, H., 1999. An in vivo testing system for endocrine disruptors in fish early stages using induction of vitellogenin. Environ. Toxicol. Chem. 18, 337-347. (Pubitemid 29058979)
53. US-EPA, 1996. Chironomid sediment toxicity test, ecological effects tests guidelines. EPA 712-C-96-313. Government Printing Office, Washington DC, USA.
54. Verhaegen, Y., Parmentier, K., Swevers, L., Renders, E., Rougé, P., De Coen, W., Cooreman, K., Smagghe, G., 2011. The heterodimeric ecdysteroid receptor complex in the brown shrimp Crangon crangon: EcR and RXR isoform characteristics and sensitivity towards the marine pollutant tributyltin. Gen. Comp. Endocrinol. 172, 158-169.
55. Vogt, C., Nowak, C., Diego, J.B., Oetken, M., Schwenk, K., Oehlmann, J., 2007. Multigeneration studies with Chironomus riparius-effects of low tributyltin concentrations on life history parameters and genetic diversity. Chemosphere 67, 2192-21200.
56. Wang, Y.H., LeBlanc, G.A., 2009. Interactions of methyl farnesoate and related compounds with a crustacean retinoid X receptor. Mol. Cell. Endocrinol. 309, 109-116.
57. Wang, Y.H., Wang, G., LeBlanc, G.A., 2007. Cloning and characterization of the retinoid X receptor from a primitive crustacean Daphnia magna. Gen. Comp. Endocrinol. 150, 209-318.
58. Wang, Y.H., Kwon, G., Li, H., LeBlanc, G.A., 2011. Tributyltin synergizes with 20- hydroxyecdysone to produce endocrine toxicity. Toxicol. Sci. 123, 71-79.
59. Yao, T.O., Forman, B.M., Jiang, Z., Cherbas, L., Chen, J.D., McKeown, M., Cherbas, P., Evans, R.M., 1993. Functional ecdysone receptor is the product of EcR and ultraspiracle genes. Nature 366, 476-479. (Pubitemid 24013883)