Transcriptional changes induced by in vivo exposure to pentachlorophenol (PCP) in Chironomus riparius (Diptera) aquatic larvae

Aquatic Toxicology

Volumn 157, Issue , 2014, Pages 1-9

  Morales, Mónica ^a   Martínez Paz, Pedro ^a   Martín, Raquel ^a   Planelló, Rosario ^a   Urien, Josune ^a   Martínez Guitarte, José Luis ^a   Morcillo, Gloria ^a  

^a UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

Author keywords

CYP gene; Ecdysone responsive genes; Endocrine disruptors; GST enzyme; Hsp genes; Organochlorines

Indexed keywords

GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; PENTACHLOROPHENOL; ECDYSONE RECEPTOR; INSECT PROTEIN; STEROID RECEPTOR; WATER POLLUTANT;

BIOMARKER; DETOXIFICATION; ENDOCRINE DISRUPTOR; ENZYME ACTIVITY; FLY; GENE; ORGANOCHLORINE; PCP; STRESS RESISTANCE; TOXICITY;

ANIMAL EXPERIMENT; ARTHROPOD LARVA; ARTICLE; CHIRONOMUS RIPARIUS; CONTROLLED STUDY; CYP4G GENE; EARLY ECDYSONE INDUCIBLE E74 GENE; ECDYSONE RECEPTOR GENE; ENZYME ACTIVITY; ESTROGEN RELATED RECEPTOR GENE; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HSP27 GENE; HSP70 GENE; IN VIVO STUDY; NONHUMAN; TRANSCRIPTION REGULATION; ULTRASPIRACLE GENE; ANIMAL; CHIRONOMIDAE; DRUG EFFECTS; ENDOCRINE SYSTEM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; INSECT GENOME; LARVA; TOXICITY; WATER POLLUTANT;

CHIRONOMUS RIPARIUS; DIPTERA;

ANIMALS; CHIRONOMIDAE; ENDOCRINE SYSTEM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME, INSECT; HSP70 HEAT-SHOCK PROTEINS; INSECT PROTEINS; LARVA; PENTACHLOROPHENOL; RECEPTORS, STEROID; WATER POLLUTANTS, CHEMICAL;

EID: 84908013031     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2014.09.009     Document Type: Article

References (87)

1. Aragon S., Claudinot S., Blais C., Maïbèche M., Dauphin-Villemant C. Molting cycle-dependent expression of CYP4C15, a cytochrome P450 enzyme putatively involved in ecdysteroidogenesis in the crayfish, Orconectes limosus. Insect Biochem. Mol. Biol. 2002, 32:153-159.
2. Arrigo A.P. Small stress proteins: chaperones that act as regulators of intracellular redox state and programmed cell death. Biol. Chem. 1998, 379:19-26.
3. Barque J.P., Abahamid A., Chacun H., Bonaly J. Different heat-shock proteins are constitutively overexpressed in cadmium and pentachlorophenol adapted Euglena gracilis cells. Biochem. Biophys. Res. Commun. 1996, 223:7-11.
4. Chen J., Jiang J., Zhang F., Yu H., Zhang J. Cytotoxic effects of environmentally relevant chlorophenols on L929 cells and their mechanisms. Cell Biol. Toxicol. 2004, 20:183-196.
5. Chen X., Yin D., Hu S., Hou Y. Immunotoxicity of pentachlorophenol on macrophage immunity and IgM secretion of the Crucian carp (Carassius auratus). Bull. Environ. Contam. Toxicol. 2004, 73:153-160.
6. Dallaire R., Muckle G., Dewailly E., Jacobson S.W., Jacobson J.L., Sandanger T.M., Sandau C.D., Ayotte P. Thyroid hormone levels of pregnant inuit women and their infants exposed to environmental contaminants. Environ. Health Perspect. 2009, 117:1014-1020.
7. Dong Y.L., Zhou P.J., Jiang S.Y., Pan X.W., Zhao X.H. Induction of oxidative stress and apoptosis by pentachlorophenol in primary cultures of Carassius carassius hepatocytes. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 2009, 150:179-185.
8. Fernández Freire P., Labrador V., Pérez Martín J.M., Hazen M.J. Cytotoxic effects in mammalian Vero cells exposed to pentachlorophenol. Toxicology 2005, 210:37-44.
9. Feyereisen R. Evolution of insect P450. Biochem. Soc. Trans. 2006, 34:1252-1255.
10. Galeano E., Vasconcelos T.S., Ramiro D.A., De Martin V., de F., Carrer H. Identification and validation of quantitative real-time reverse transcription PCR reference genes for gene expression analysis in teak (Tectona grandis L.f.). BMC Res. Notes 2014, 22:464.
11. Ge J., Pan J., Fei Z., Wu G., Giesy J.P. Concentrations of pentachlorophenol (PCP) in fish and shrimp in Jiangsu Province, China. Chemosphere 2007, 69:164-169.
12. Geyer H.J., Scheunert I., Korte F. Distribution and bioconcentration potential of the environmental chemical pentachlorophenol (PCP) in different tissues of humans. Chemosphere 1987, 16(4):887-899.
13. Gilbert L.I., Warren J.T. A molecular genetic approach to the biosynthesis of the insect steroid molting hormone. Vitam. Horm. 2005, 73:31-57.
14. Gkouvitsas T., Kontogiannatos D., Kourti A. Differential expression of two small Hsps during diapause in the corn stalk borer Sesamia nonagrioides (Lef.). J. Insect Physiol. 2008, 54:1503-1510.
15. Guo Y., Zhou B. Thyroid endocrine system disruption by pentachlorophenol: an in vitro and in vivo assay. Aquat. Toxicol. 2013, 142-143:138-145.
16. Gupta S.C., Shrama A., Mishra M., Mishra R.K., Chowdhuri D.K. Heat shock proteins in toxicology: how close and how far?. Life Sci. 2010, 86:377-384.
17. Gupta S., Stadler M., Noser C.A., Ghosh A., Steinhoff B., Lenoir D., Horwitz C.P., Schramm K.W., Collins T.J. Rapid total destruction of chlorophenols by activated hydrogen peroxide. Science 2002, 296:326-328.
18. Hanna K., de Brauer C., Germain P., Chovelon J.M., Ferronato C. Degradation of pentachlorophenol in cyclodextrin extraction effluent using a photocatalytic process. Sci. Total Environ. 2004, 332:51-60.
19. Hao X., Zhang S., Timakov B., Zhang P. The Hsp27 gene is not required for Drosophila development but its activity is associated with starvation resistance. Cell Stress Chaperones 2007, 12:364-372.
20. He H., Xi G., Lu X. Molecular cloning, characterization, and expression analysis of an estrogen receptor-related receptor homologue in the cricket, Teleogryllus emma. J. Insect Sci. 2010, 10:188.
21. Hellemans J., Mortier G., De Paepe A., Speleman F., Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007, 8:R19.
22. Heudorf U., Letzel S., Peters M., Angerer J. PCP in the blood plasma: current exposure of the population in Germany, based on data obtained in 1998. Int. J. Hyg. Environ. Health 2000, 203:135-139.
23. Hurd T., Walker J., Whalen M.M. Pentachlorophenol decreases tumor-cell-binding capacity and cell-surface protein expression of human natural killer cells. J. Appl. Toxicol. 2012, 32:627-634.
24. Karim F.D., Thummel C.S. Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J. 1992, 11:4083-4093.
25. Karouna-Renier N.K., Zehr J.P. Short-term exposures to chronically toxic copper concentrations induce HSP70 proteins in midge larvae (Chironomus tentans). Sci. Total Environ. 2003, 312:267-272.
26. Karouna-Renier N.K., Rao K.R. An inducible HSP70 gene from the midge Chironomus dilutus: characterization and transcription profile under environmental stress. Insect Mol. Biol. 2009, 18:87-96.
27. Koelle M.R., Talbot W.S., Segraves W.A., Bender M.T., Cherbas P., Hogness D.S. The drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 1991, 67:59-77.
28. Köhler H.R., Kloas W., Schirling M., Lutz I., Reye A.L., Langen J.S., Triebskorn R., Nagel R.Schönfelder Sex steroid receptor evolution and signaling in aquatic invertebrates. Ecotoxicology 2007, 16:131-143.
29. Lee S.B., Choi J. Effects of bisphenol A and ethynyl estradiol exposure on enzyme activities, growth and development in the fourth instar larvae of Chironomus riparius (Diptera, Chironomidae). Ecotoxicol. Environ. Saf. 2007, 68:84-90.
30. Li C., Zheng M., Gao L., Zhang B., Liu L., Xiao K. Levels and distribution of PCDD/Fs, dl-PCBs, and organochlorine pesticides in sediments from the lower reaches of the Haihe River basin, China. Environ. Monit. Assess. 2013, 185:1175-1187.
31. Londoño D.K., Siqueira H.A.A., Wang H., Sarath G., Lydy M.J., Siegfried B.D. Cloning and expression of an atrazine inducible cytochrome P450, CYP4G33, from Chironomus tentans (Diptera: Chironomidae). Pest. Biochem. Physiol. 2007, 89:104-110.
32. Lüchmann K.H., Dafre A.L., Trevisan R., Craft J.A., Meng X., Mattos J.J., Zacchi F.L., Dorrington T.S., Schroeder D.C., Bainy A.C. A light in the darkness: new biotransformation genes, antioxidant parameters and tissue-specific responses in oysters exposed to phenanthrene. Aquat. Toxicol. 2014, 152:324-334.
33. Ma Y., Liu C., Lam P.K., Wu R.S., Giesy J.P., Hecker M., Zhang X., Zhou B. Modulation of steroidogenic gene expression and hormone synthesis in H295R cells exposed to PCP and TCP. Toxicology 2011, 282:146-153.
34. Martinez E.A., Moore B.C., Schaumloffel J., Dasgupta N. Morphological abnormalities in Chironomus tentans exposed to cadmium and copper-spiked sediments. Ecotox. Environ. Safe. 2003, 55:204-212.
35. Martínez-Guitarte J.L., Planelló R., Morcillo G. 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-Biochem. Mol. Biol. 2007, 147:590-596.
36. Martinez-Guitarte J.L., Planelló R., Morcillo G. Overexpression of long non-coding RNAs following exposure to xenobiotics in the aquatic midge Chironomus riparius. Aquat. Toxicol. 2012, 110-111:84-90.
37. Martínez-Paz P., Morales M., Martínez-Guitarte J.L., Morcillo G. 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-Toxicol. Pharmacol. 2012, 155:333-343.
38. Martínez-Paz P., Morales M., Martínez-Guitarte J.L., Morcillo G. Genotoxic effects of environmental endocrine disruptors on the aquatic insect Chironomus riparius evaluated using the comet assay. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2013, 758:41-47.
39. Martínez-Paz P., Morales M., Martín R., Martínez-Guitarte J.L., Morcillo G. Characterization of the small heat shock protein Hsp27 gene in Chironomus riparius (Diptera) and its expression profile in response to temperature changes and xenobiotic exposures. Cell Stress Chaperones 2014, 19:529-540.
40. Mehmood Z., Williamson M.P., Kelly D.E., Kelly S.L. Metabolism of organochlorine pesticides: the role of human cytochrome P450 3A4. Chemosphere 1996, 33:759-769.
41. Montaño M., Gutleb A.C., Murk A.J. Persistent toxic burdens of halogenated phenolic compounds in humans and wildlife. Environ. Sci. Technol. 2013, 47:6071-6081.
42. Morales M., Planelló R., Martínez-Paz P., Herrero O., Cortés E., Martínez-Guitarte J.L., Morcillo G. Characterization of Hsp70 gene in Chironomus riparius: expression in response to endocrine disrupting pollutants as a marker of ecotoxicological stress. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 2011, 153:150-158.
43. Morales M., Martínez-Paz P., Ozáez I., Martínez-Guitarte J.L., Morcillo G. DNA damage and transcriptional changes induced by tributyltin (TBT) after short in vivo exposures of Chironomus riparius (Diptera) larvae. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 2013, 158:57-63.
44. Morrow G., Battistini S., Zhang P., Tanguay R.M. Decreased lifespan in the absence of expression of the mitochondrial small heat shock protein Hsp22 in Drosophila. J. Biol. Chem. 2004, 279:43382-43385.
45. Muir J., Eduljee G. PCP in the freshwater and marine environment of the European Union. Sci. Total Environ. 1999, 236:41-56.
46. Nair P.M., Park S.Y., Lee S.W., Choi J. Differential expression of ribosomal protein gene, gonadotrophin releasing hormone gene and Balbiani ring protein gene in silver nanoparticles exposed Chironomus riparius. Aquat. Toxicol. 2011, 101:31-37.
47. Nair P.M., Choi J. Modulation in the mRNA expression of ecdysone receptor gene in aquatic midge, Chironomus riparius upon exposure to nonylphenol and silver nanoparticles. Environ. Toxicol. Pharmacol. 2012, 33:98-106.
48. Nair P.M., Park S.Y., Choi J. Characterization and expression of cytochrome p450 cDNA (CYP9AT2) in Chironomus riparius fourth instar larvae exposed to multiple xenobiotics. Environ. Toxicol. Pharmacol. 2013, 36:1133-1140.
49. Nolen E.A., Morimoto R.I. Chaperoning signaling pathways: molecular chaperones as stress-sensing heat shock proteins. J. Cell Sci. 2002, 115:2809-2816.
50. OECD OECD guideline for the testing of chemicals. Series on Testing and Assessment 2013, 184.
51. Ozáez I., Martínez-Guitarte J.L., Morcillo G. 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. 2013, 456-457:120-126.
52. Ozáez I., Martínez-Guitarte J.L., Morcillo G. The UV filter benzophenone 3 (BP-3) activates hormonal genes mimicking the action of ecdysone and alters embryo development in the insect Chironomus riparius (Diptera). Environ. Pollut. 2014, 192:19-26.
53. Park K., Kwak I.S. Characterization of heat shock protein 40 and 90 in Chironomus riparius larvae: effects of di(2-ethylhexyl) phthalate exposure on gene expressions and mouthpart deformities. Chemosphere 2008, 74:89-95.
54. Park K., Bank H.W., Park J., Kwak I.S. Ecotoxicological multilevel-evaluation of the effects of fenbendazole exposure to Chironomus riparius larvae. Chemosphere 2009, 77:359-367.
55. Park K., Kwak I.S. Alcohol dehydrogenase gene expression in Chironomus riparius exposed to di(2-ethylhexyl) phthalate. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 2009, 150:361-367.
56. Park K., Kwak I.S. Molecular effects of endocrine-disrupting chemicals on the Chironomus riparius estrogen-related receptor gene. Chemosphere 2010, 79:934-941.
57. Pfaffl M.W. Quantification Strategies in Real-Time PCR. The Real-Time PCR Encyclopedia, A-Z of Quantitative PCR. 2004, 87-112. International University Line, La Jolla. S.A. Bustin (Ed.).
58. Planelló R., Martínez-Guitarte J.L., Morcillo G. Ribosomal genes as early targets of cadmium-induced toxicity in Chironomus riparius larvae. Sci. Total Environ. 2007, 373:113-121.
59. Planelló R., Martínez-Guitarte J.L., Morcillo G. The endocrine disruptor bisphenol A increases the expression of HSP70 and ecdysone-receptor genes in the aquatic larvae of Chironomus riparius. Chemosphere 2008, 71:1870-1876.
60. Planelló R., Martínez-Guitarte J.L., Morcillo G. 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. 2010, 408:1598-1603.
61. Planelló R., Herrero O., Martínez-Guitarte J.L., Morcillo G. 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. 2011, 105:62-70.
62. Proudfoot A.T. Pentachlorophenol poisoning. Toxicol. Rev. 2003, 22:3-11.
63. Raessler M., Rothe J., Hilke I. Accurate determination of Cd, Cr, Cu and Ni in woodlice and their skins--is moulting a means of detoxification?. Sci. Total Environ. 2005, 337:83-90.
64. Rauch P., Grebe M., Elke C., Spindler K.D., Spindler-Barth M. Ecdysteroid receptor and ultraspiracle from Chironomus tentans (Insecta) are phosphoproteins and are regulated differently by molting hormone. Insect Biochem. Mol. Biol. 1998, 28:265-275.
65. Rettie A.E., Kelly E.J. The CYP4 family. Cytochromes P450. Role in the Metabolism and Toxicity of Drugs and Other Xenobiotics. Issues in Toxicology 2008, 384-414. RSC Publishing, Cambridge. C. Ioannides (Ed.).
66. Ryan J.A., Hightower L.E. Heat shock proteins: molecular biomarkers of effects. Molecular Biology of the Toxic Response 1998, 449-466. Hamilton Printing Co, Castlton, New York. A. Puga, K.B. Wallale (Eds.).
67. Song Z.H. Effects of pentachlorophenol on Galba pervia, Tubifex sinicus and Chironomus plumousus larvae. Bull. Environ. Contam. Toxicol. 2007, 79:278-282.
68. Segner H., Caroll K., Fenske M., Janssen C.R., Maack G., Pascoe D., Schäfers C., Vandenbergh G.F., Watts M., Wenzel A. Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotoxicol. Environ. Saf. 2003, 54:302-314.
69. Sugiyama S., Shimada N., Miyoshi H., Yamauchi K. Detection of thyroid system-disrupting chemicals using in vitro and in vivo screening assays in Xenopus laevis. Toxicol. Sci. 2005, 88:367-374.
70. Telang A., Frame L., Brown M.R. Larval feeding duration affects ecdysteroid levels and nutritional reserves regulating pupal commitment in the yellow fever mosquito Aedes aegypti (Diptera: Culicidae). J. Exp. Biol. 2007, 210:854-864.
71. Tohmé M., Prud'homme S.M., Boulahtouf A., Samarut E., Brunet F., Bernard L., Bourguet W., Gibert Y., Balaguer P., Laudet V. Estrogen-related receptor γ is an in vivo receptor of bisphenol A. FASEB J. 2014, 10.1096/fj.13-240465.
72. Tokumoto T., Tokumoto M., Nagahama Y. Induction and inhibition of oocyte maturation by EDCs in zebrafish. Reprod. Biol. Endocrinol. 2005, 3:69.
73. Tsvetkova N.M., Horváth I., Török Z., Wolkers W.F., Balogi Z., Shigapova N., Crowe L.M., Tablin F., Vierling E., Crowe J.H., Vigh L. Small heat-shock proteins regulate membrane lipid polymorphism. Proc. Natl. Acad. Sci. USA 2002, 99:13504-13509.
74. US-EPA Methods for measuring the toxicity and bioaccumulation of sediment-associated contaminants with freshwater invertebrates 2000, EPA 600/R-99/064, Washington DC. 2nd ed.
75. Wang Y.J., Lee C.C., Chang W.C., Liou H.B., Ho Y.S. Oxidative stress and liver toxicity in rats and human hepatoma cell line induced by pentachlorophenol and its major metabolite tetrachlorohydroquinone. Toxicol. Lett. 2001, 122:157-169.
76. WHO Pentachlorophenol, International Programme on Chemical Safety. Environ Health Criteria 1987, World Health Organization. Health and safety guide 19. Geneva, Geneva.
77. Wispriyono B., Matsuoka M., Igisu H. Effects of pentachlorophenol and tetrachlorohydroquinone on mitogen-activated protein kinase pathways in Jurkat T cells. Environ. Health Perspect. 2002, 110:139-143.
78. Xu T., Zhao J., Hu P., Dong Z., Li J., Zhang H., Yin D., Zhao Q. Pentachlorophenol exposure causes Warburg-like effects in zebrafish embryos at gastrulation stage. Toxicol. Appl. Pharmacol. 2014, 277:183-191.
79. Xu Z.B., Zou X.P., Zhang N., Feng Q.L., Zheng S.C. Detoxification of insecticides, allechemicals and heavy metals by glutathione S-transferase SlGSTE1 in the gut of Spodoptera litura. Insect Sci. 2014, 10.1111/1744-7917.12142.
80. Yang S., Han X., Wei C., Chen J., Yin D. The toxic effects of pentachlorophenol on rat Sertoli cells in vitro. Environ. Toxicol. Pharmacol. 2005, 20:182-187.
81. Yao T.O., Forman B.M., Jiang Z., Cherbas L., Chen J.D., McKeown M., Cherbas P., Evans R.M. Functional ecdysone receptor is the product of EcR and ultraspiracle genes. Nature 1993, 366:476-479.
82. Yoshimi T., Minowa K., Karouna-Renier N.K., Watanabe C., Sugaya Y., Miura T. Activation of stress-induced gene by insecticides in the midge Chironomus yoshimatsui. J. Biochem. Mol. Toxicol. 2002, 16:10-17.
83. Yu L.Q., Zhao G.F., Feng M., Wen W., Li K., Zhang P.W., Peng X., Huo W.J., Zhou H.D. Chronic exposure to pentachlorophenol alters thyroid hormones and thyroid hormone pathway mRNAs in zebrafish. Environ. Toxicol. Chem. 2014, 33:170-176.
84. Zha J., Wang Z., Schlenk D. Effects of pentachlorophenol on the reproduction of Japanese medaka (Oryzias latipes). Chem. Biol. Interact. 2006, 161:26-36.
85. Zhang X., Xiong L., Liu Y., Deng C., Mao S. Histopathological and estrogen effect of pentachlorophenol on the rare minnow (Gobiocypris rarus). Fish Physiol. Biochem. 2014, 40:805-816.
86. Zheng W., Wang X., Yu H., Tao X., Zhou Y., Qu W. Global trends and diversity in pentachlorophenol levels in the environment and in humans: a meta-analysis. Environ. Sci. Technol. 2011, 45:4668-4675.
87. Zheng W., Yu H., Wang X., Qu W. Systematic review of pentachlorophenol occurrence in the environment and in humans in China: Not a negligible health risk due to the re-emergence of schistosomiasis. Environ. Int. 2012, 42:105-116.