Metabolic and immune impairments induced by the endocrine disruptors benzo[a]pyrene and triclosan in Xenopus tropicalis

Chemosphere

Volumn 155, Issue , 2016, Pages 519-527

  Regnault, Christophe ^a,b   Willison, John ^a,b,c   Veyrenc, Sylvie ^a,b   Airieau, Antinéa ^a,b   Méresse, Patrick ^a   Fortier, Marlène ^d   Fournier, Michel ^e   Brousseau, Pauline ^e   Raveton, Muriel ^a,b   Reynaud, Stéphane ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b CNRS   (France)

^c DIF   (France)

^d INRS INSTITUT ARMAND FRAPPIER   (Canada)

^e INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

Author keywords

Amphibian; Benzo a pyrene; Endocrine disruptors; Metabolism; NAFLD; Triclosan; Xenopus tropicalis

Indexed keywords

BARIUM COMPOUNDS; CELL PROLIFERATION; EMERGENCY ROOMS; IMMUNE SYSTEM; MIXTURES; MODULATION; POPULATION STATISTICS; PYRENE; TRANSCRIPTION;

AMPHIBIAN; BENZO [A] PYRENE; ENDOCRINE DISRUPTOR; NAFLD; TRICLOSAN; XENOPUS TROPICALIS;

METABOLISM;

BENZO[A]PYRENE; ENDOCRINE DISRUPTOR; GLUCOSE; INSULIN; LIPID; SEX HORMONE; TRICLOSAN; TOPICAL ANTIINFECTIVE AGENT;

CONCENTRATION (COMPOSITION); ENDOCRINE DISRUPTOR; FROG; IMMUNE SYSTEM; METABOLISM; PAH; PHENOTYPE; POPULATION DECLINE; SEX HORMONE;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE METABOLISM; CELL ADHESION; CELL INTERACTION; DISORDERS OF LIPID AND LIPOPROTEIN METABOLISM; GLUCOSE METABOLISM; IMMUNE SYSTEM; IMMUNOPATHOLOGY; INNATE IMMUNITY; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; LIVER TOXICITY; MALE; METABOLIC DISORDER; METABOLISM; NONALCOHOLIC FATTY LIVER; NONHUMAN; PHENOTYPE; REPRODUCTION; SPLEEN; TESTIS; XENOPUS TROPICALIS; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; XENOPUS;

AMPHIBIA; XENOPUS TROPICALIS;

ANIMALS; ANTI-INFECTIVE AGENTS, LOCAL; BENZO(A)PYRENE; ENDOCRINE DISRUPTORS; IMMUNITY, INNATE; LIPID METABOLISM; LIVER; MALE; METABOLIC DISEASES; REPRODUCTION; SPLEEN; TESTIS; TRICLOSAN; XENOPUS;

EID: 84966431177     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2016.04.047     Document Type: Article

References (80)

1. Arciello M., Gori M., Maggio R., Barbaro B., Tarocchi M., Galli A., Balsano C. Environmental pollution: a tangible risk for NAFLD pathogenesis. Int. J. Mol. Sci. 2013, 14:22052-22066. 10.3390/ijms141122052.
2. Azzout-Marniche D., Bécard D., Guichard C., Foretz M., Ferré P., Foufelle F. Insulin effects on sterol regulatory-element-binding protein-1c (SREBP-1c) transcriptional activity in rat hepatocytes. Biochem. J. 2000, 350:389-393.
3. Bado-Nilles A., Techer R., Porcher J.M., Geffard A., Gagnaire B., Betoulle S., Sanchez W. Detection of immunotoxic effects of estrogenic and androgenic endocrine disrupting compounds using splenic immune cells of the female three-spined stickleback, Gasterosteus aculeatus (L.). Environ. Toxicol. Pharmacol. 2014, 38:672-683. 10.1016/j.etap.2014.08.002.
4. Banerjee S. Solubility of organic mixtures in water. Environ. Sci. Technol. 1984, 18:587-591. 10.1021/es00126a004.
5. Bitter A., Nüssler A.K., Thasler W.E., Klein K., Zanger U.M., Schwab M., Burk O. Human sterol regulatory element-binding protein 1a contributes significantly to hepatic lipogenic gene expression. Cell. Physiol. Biochem. 2015, 35:803-815. 10.1159/000369739.
6. Blaustein A.R., Bancroft B.A. Amphibian population declines: evolutionary considerations. BioScience 2007, 57:437-444.
7. Brousseau P., Payette Y., Tryphonas H., Blakley B., Boermans H., Flipo D., Fournier M. Manual of Immunological Methods 1999, CRC Press.
8. Brunengraber D.Z., McCabe B.J., Kasumov T., Alexander J.C., Chandramouli V., Previs S.F. Influence of diet on the modeling of adipose tissue triglycerides during growth. Am. J. Physiol. Endocrinol. Metab. 2003, 285:E917-E925. 10.1152/ajpendo.00128.2003.
9. Caballero F., Fernández A., De Lacy A.M., Fernández-Checa J.C., Caballería J., García-Ruiz C. Enhanced free cholesterol, SREBP-2 and StAR expression in human NASH. J. Hepatol. 2009, 50:789-796. 10.1016/j.jhep.2008.12.016.
10. Cantó C., Auwerx J. PGC-1α, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr. Opin. Lipidol. 2009, 20:98-105. 10.1097/MOL.0b013e328328d0a4.
11. Carey C., Cohen N., Rollins-Smith L. Amphibian declines: an immunological perspective. Dev. Comp. Immunol. 1999, 23:459-472. 10.1016/S0145-305X(99)00028-2.
12. Carlson E.A., Li Y., Zelikoff J.T. Benzo[a]pyrene-induced immunotoxicity in Japanese medaka (Oryzias latipes): relationship between lymphoid CYP1A activity and humoral immune suppression. Toxicol. Appl. Pharmacol. 2004, 201:40-52. 10.1016/j.taap.2004.04.018.
13. Casals-Casas C., Desvergne B. Endocrine disruptors: from endocrine to metabolic disruption. Annu. Rev. Physiol. 2011, 73:135-162. 10.1146/annurev-physiol-012110-142200.
14. Cevasco A., Urbatzka R., Bottero S., Massari A., Pedemonte F., Kloas W., Mandich A. Endocrine disrupting chemicals (EDC) with (anti)estrogenic and (anti)androgenic modes of action affecting reproductive biology of Xenopus laevis: II. Effects on gonad histomorphology. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2008, 147:241-251. 10.1016/j.cbpc.2007.10.001.
15. Christin M.-S., Gendron A.D., Brousseau P., Ménard L., Marcogliese D.J., Cyr D., Ruby S., Fournier M. Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environ. Toxicol. Chem. 2003, 22:1127-1133. 10.1002/etc.5620220522.
16. Crump D., Werry K., Veldhoen N., Van Aggelen G., Helbing C.C. Exposure to the herbicide acetochlor alters thyroid hormone-dependent gene expression and metamorphosis in Xenopus laevis. Environ. Health Perspect. 2002, 110:1199-1205.
17. Devaux A., Fiat L., Gillet C., Bony S. Reproduction impairment following paternal genotoxin exposure in brown trout (Salmo trutta) and Arctic charr (Salvelinus alpinus). Aquat. Toxicol. 2011, 101:405-411. 10.1016/j.aquatox.2010.11.017.
18. Dortch M.S., Zakikhani M., Kim S.-C., Steevens J.A. Modeling water and sediment contamination of lake Pontchartrain following pump-out of Hurricane Katrina floodwater. J. Environ. Manage. 2008, 87:429-442. 10.1016/j.jenvman.2007.01.035.
19. Duarte-Guterman P., Navarro-Martin L., Trudeau V.L. Mechanisms of crosstalk between endocrine systems: regulation of sex steroid hormone synthesis and action by thyroid hormones. Gen. Comp. Endocrinol. 2014, 203:69-85.
20. Farrell G.C., van Rooyen D., Gan L., Chitturi S. NASH is an inflammatory disorder: pathogenic, prognostic and therapeutic omplications. Gut Liver 2012, 6:149-171. 10.5009/gnl.2012.6.2.149.
21. Fedorenkova A., Vonk J.A., Lenders H.J.R., Creemers R.C.M., Breure A.M., Hendriks A.J. Ranking ecological risks of multiple chemical stressors on amphibians. Environ. Toxicol. Chem. 2012, 31:1416-1421. 10.1002/etc.1831.
22. Fraker S.L., Smith G.R. Direct and interactive effects of ecologically relevant concentrations of organic wastewater contaminants on Rana pipiens tadpoles. Environ. Toxicol. 2004, 19:250-256. 10.1002/tox.20017.
23. Garrigues P., Djomo J.E., Ferrier V., Dauta A., Monkiedje A., Ze A.M., Narbonne J.F. Toxicokinetics of polycyclic aromatic hydrocarbons from contaminated sediment by the amphibian larvae (pleurodeles Waltl). Polycycl. Aromat. Compd. 2004, 24:207-219. 10.1080/10406630490460692.
24. Gilbertson M.K., Haffner G.D., Drouillard K.G., Albert A., Dixon B. Immunosuppression in the northern leopard frog (Rana pipiens) induced by pesticide exposure. Environ. Toxicol. Chem. 2003, 22:101-110. 10.1002/etc.5620220113.
25. Hajra A.K., Larkins L.K., Das A.K., Hemati N., Erickson R.L., MacDougald O.A. Induction of the peroxisomal glycerolipid-synthesizing enzymes during differentiation of 3T3-L1 adipocytes role in triacylglycerol synthesis. J. Biol. Chem. 2000, 275:9441-9446. 10.1074/jbc.275.13.9441.
26. Hammond S.A., Veldhoen N., Helbing C.C. Influence of temperature on thyroid hormone signaling and endocrine disruptor action in Rana (Lithobates) catesbeiana tadpoles. Gen. Comp. Endocrinol. 2015, 219:6-15. Disruption of the Thyroid and Sex Steroid Hormone Systems and Their Crosstalk in Aquatic Wildlife. 10.1016/j.ygcen.2014.12.001.
27. Hansmannel F., Mordier S., Iynedjian P.B. Insulin induction of glucokinase and fatty acid synthase in hepatocytes: analysis of the roles of sterol-regulatory-element-binding protein-1c and liver X receptor. Biochem. J. 2006, 399:275-283. 10.1042/BJ20060811.
28. Hassan A.M., Alam S.S., Abdel-Aziem S.H., Ahmed K.A. Benzo-a-pyrene induced genotoxicity and cytotoxicity in germ cells of mice: intervention of radish and cress. J. Genet. Eng. Biotechnol. 2011, 9:65-72. 10.1016/j.jgeb.2011.05.006.
29. Hayes T., Haston K., Tsui M., Hoang A., Haeffele C., Vonk A. Herbicides: feminization of male frogs in the wild. Nature 2002, 419:895-896. 10.1038/419895a.
30. Hayes T.B., Falso P., Gallipeau S., Stice M. The cause of global amphibian declines: a developmental endocrinologist's perspective. J. Exp. Biol. 2010, 213:921-933. 10.1242/jeb.040865.
31. Hayes T.B., Anderson L.L., Beasley V.R., de Solla S.R., Iguchi T., Ingraham H., Kestemont P., Kniewald J., Kniewald Z., Langlois V.S., Luque E.H., McCoy K.A., Munoz-de-Toro M., Oka T., Oliveira C.A., Orton F., Ruby S., Suzawa M., Tavera-Mendoza L.E., Trudeau V.L., Victor-Costa A.B., Willingham E. Demasculinization and feminization of male gonads by atrazine: consistent effects across vertebrate classes. J. Steroid Biochem. Mol. Biol. 2011, 127. 10.1016/j.jsbmb.2011.03.015.
32. Helbing C.C. The metamorphosis of amphibian toxicogenomics. Front. Genet. 2012, 3:37. 10.3389/fgene.2012.00037.
33. Jagnytsch O., Opitz R., Lutz I., Kloas W. Effects of tetrabromobisphenol A on larval development and thyroid hormone-regulated biomarkers of the amphibian Xenopus laevis. Environ. Res. 2006, 101:340-348. 10.1016/j.envres.2005.09.006.
34. James M.O., Marth C.J., Rowland-Faux L. Slow O-demethylation of methyl triclosan to triclosan, which is rapidly glucuronidated and sulfonated in channel catfish liver and intestine. Aquat. Toxicol. Amst. Neth. 2012, 124-125. 10.1016/j.aquatox.2012.07.009.
35. Kashiwagi A., Utsumi K., Kashiwagi K., Ohta S., Sugihara K., Hanada H., Kitamura S. Effects of endocrine disrupting chemicals on amphibian metamorphosis and mitochondrial membrane permeability transition. J. Health Sci. 2008, 54:273-280. 10.1248/jhs.54.273.
36. Kloas W., Lutz I. Amphibians as model to study endocrine disrupters. 9th Int. Symp. Hyphenated Tech. Chromatogr. Hyphenated Chromatogr. Anal 2006, vol. 1130:16-27. 10.1016/j.chroma.2006.04.001.
37. Langlois V.S., Carew A.C., Pauli B.D., Wade M.G., Cooke G.M., Trudeau V.L. Low levels of the herbicide atrazine alter sex ratios and reduce metamorphic success in rana pipiens tadpoles raised in outdoor mesocosms. Env. Health. Persp. 2010, 118:552-557.
38. Langlois V.S., Duarte-Guterman P., Sally I., Pauli B.D., Cooke G.M., Trudeau V.L. Fadrozole and finasteride exposures modulate sex steroid- and thyroid hormone-related gene expression in Silurana (Xenopus) tropicalis early larval development. Gen. Comp. Endocrinol. 2010, 166:417-427.
39. Langlois V.S., Zhang D., Cooke G.M., Trudeau V.L. Evolution of steroid-5 alpha-reductases and comparison of their function with 5 beta-reductase. Gen. Comp. Endocrinol. 2010, 166:489-497.
40. León-Olea M., Martyniuk C.J., Orlando E.F., Ottinger M.A., Rosenfeld C.S., Wolstenholme J.T., Trudeau V.L. Current concepts in neuroendocrine disruption. Gen. Comp. Endocrinol. 2014, 203:158-173. 2nd Meeting of the North American Society for Comparative Endocrinology. 10.1016/j.ygcen.2014.02.005.
41. Liaskou E., Wilson D.V., Oo Y.H., Liaskou E., Wilson D.V., Oo Y.H. Innate immune cells in liver inflammation. Mediat. Inflamm. Mediat. Inflamm. 2012, 2012(2012):e949157. 10.1155/2012/949157. 10.1155/2012/949157.
42. Lips K.R., Diffendorfer J., Mendelson J.R., Sears M.W. Riding the Wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biol. 2008, 6:e72. 10.1371/journal.pbio.0060072.
43. Massart S., Milla S., Kestemont P. Evaluation of estrogenic endocrine disruptors effects on rainbow trout (Oncorhynchus mykiss) immunity. Fish. Shellfish Immunol. 2013, 34:1723-1724. 10.1016/j.fsi.2013.03.268.
44. Matamoros V., Jover E., Bayona J.M. Advances in the determination of degradation intermediates of personal care products in environmental matrixes: a review. Anal. Bioanal. Chem. 2008, 393:847-860. 10.1007/s00216-008-2371-7.
45. Matsumura N., Ishibashi H., Hirano M., Nagao Y., Watanabe N., Shiratsuchi H., Kai T., Nishimura T., Kashiwagi A., Arizono K. Effects of nonylphenol and triclosan on production of plasma vitellogenin and testosterone in male South African clawed frogs (Xenopus laevis). Biol. Pharm. Bull. 2005, 28:1748-1751.
46. McAvoy D.C., Schatowitz B., Jacob M., Hauk A., Eckhoff W.S. Measurement of triclosan in wastewater treatment systems. Environ. Toxicol. Chem. SETAC 2002, 21:1323-1329.
47. McConnell L.L., Sparling D. Emerging contaminants and their potential effects on amphibians and reptiles. Ecotoxicology of Amphibians and Reptiles 2010, 487-509. CRC Press.
48. Mirhaghparast S.K., Zibaee A., Sendi J.J., Hoda H., Fazeli-Dinan M. Immune and metabolic responses of Chilo suppressalis Walker (Lepidoptera: Crambidae) larvae to an insect growth regulator, hexaflumuron. Pestic. Biochem. Physiol. 2015, 125:69-77. 10.1016/j.pestbp.2015.05.007.
49. Mosconi G., Carnevali O., Franzoni M.F., Cottone E., Lutz I., Kloas W., Yamamoto K., Kikuyama S., Polzonetti-Magni A.M. Environmental estrogens and reproductive biology in amphibians. Gen. Comp. Endocrinol. 2002, 126:125-129. 10.1006/gcen.2002.7781.
50. Naik A., Košir R., Rozman D. Genomic aspects of NAFLD pathogenesis. Genom. SI Clin. Transl. Genom. 2013, 102:84-95. 10.1016/j.ygeno.2013.03.007.
51. Opitz R., Braunbeck T., Bogi C., Pickford D.B., Nentwig G., Oehlmann J., Tooi O., Lutz I., Kloas W. Description and initial evaluation of a Xenopus metamorphosis assay for detection of thyroid system-disrupting activities of environmental compounds. Environ. Toxicol. Chem. 2005, 24:653-664. 10.1897/04-214R.1.
52. Opitz R., Hartmann S., Blank T., Braunbeck T., Lutz I., Kloas W. Evaluation of histological and molecular endpoints for enhanced detection of thyroid system disruption in Xenopus laevis Tadpoles. Toxicol. Sci. 2006, 90:337-348. 10.1093/toxsci/kfj083.
53. Opitz R., Lutz I., Nguyen N.-H., Scanlan T.S., Kloas W. Analysis of thyroid hormone receptor βA mRNA expression in Xenopus laevis tadpoles as a means to detect agonism and antagonism of thyroid hormone action. Toxicol. Appl. Pharmacol. 2006, 212:1-13. 10.1016/j.taap.2005.06.014.
54. Orton F., Tyler C.R. Do hormone-modulating chemicals impact on reproduction and development of wild amphibians?. Biol. Rev. 2015, 90:1100-1117. 10.1111/brv.12147.
55. Palmquist H., Hanæus J. Hazardous substances in separately collected grey- and blackwater from ordinary Swedish households. Sci. Total Environ. 2005, 348:151-163. 10.1016/j.scitotenv.2004.12.052.
56. Park C.J., Kang H.S., Gye M.C. Effects of nonylphenol on early embryonic development, pigmentation and 3,5,3'-triiodothyronine-induced metamorphosis in Bombina orientalis (Amphibia: Anura). Chemosphere 2010, 81:1292-1300. 10.1016/j.chemosphere.2010.08.039.
57. Perez A.L., De Sylor M.A., Slocombe A.J., Lew M.G., Unice K.M., Donovan E.P. Triclosan occurrence in freshwater systems in the United States (1999-2012): a meta-analysis. Environ. Toxicol. Chem. SETAC 2013, 32:1479-1487. 10.1002/etc.2217.
58. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT- PCR. Nucleic Acids Res. 2001, 29:29-45.
59. Pinto P., Vandreal P., Kaplan A. Aldolase.i. Colorimetric determination. Clin. Chem. 1969, 15:339.
60. Puigserver P., Rhee J., Donovan J., Walkey C.J., Yoon J.C., Oriente F., Kitamura Y., Altomonte J., Dong H., Accili D., Spiegelman B.M. Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1α interaction. Nature 2003, 423:550-555. 10.1038/nature01667.
61. Regnault C., Worms I.A., Oger-Desfeux C., MelodeLima C., Veyrenc S., Bayle M.-L., Combourieu B., Bonin A., Renaud J., Raveton M., others Impaired liver function in Xenopus tropicalis exposed to benzo [a] pyrene: transcriptomic and metabolic evidence. BMC Genomics 2014, 15:666.
62. Reynaud S., Duchiron C., Deschaux P. 3-Methylcholanthrene induces lymphocyte and phagocyte apoptosis in common carp (Cyprinus carpio L) in vitro. Aquat. Toxicol. 2004, 66:307-318. 10.1016/j.aquatox.2003.10.003.
63. Reynaud S., Deschaux P. The effects of polycyclic aromatic hydrocarbons on the immune system of fish: a review. Aquat. Toxicol. 2006, 77:229-238. 10.1016/j.aquatox.2005.10.018.
64. Reynaud S., Worms I.A.M., Veyrenc S., Portier J., Maitre A., Miaud C., Raveton M. Toxicokinetic of benzo[a]pyrene and fipronil in female green frogs (Pelophylax kl. esculentus). Environ. Pollut. 2012, 161:206-214. Mercury in the Laurentian Great Lakes Region. 10.1016/j.envpol.2011.10.029.
65. Roelants K., Gower D.J., Wilkinson M., Loader S.P., Biju S.D., Guillaume K., Moriau L., Bossuyt F. Global patterns of diversification in the history of modern amphibians. Proc. Natl. Acad. Sci. 2007, 104:887-892.
66. Rollins-Smith L.A., Doersam J.K., Longcore J.E., Taylor S.K., Shamblin J.C., Carey C., Zasloff M.A. Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Dev. Comp. Immunol. 2002, 26:63-72.
67. Säfholm M., Ribbenstedt A., Fick J., Berg C. Risks of hormonally active pharmaceuticals to amphibians: a growing concern regarding progestagens. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369:20130577. 10.1098/rstb.2013.0577.
68. Saraste A., Pulkki K. Morphologic and biochemical hallmarks of apoptosis. Cardiovasc. Res. 2000, 45:528-537. 10.1016/S0008-6363(99)00384-3.
69. Shi H., Zhu P., Guo S. Effects of tributyltin on metamorphosis and gonadal differentiation of Xenopus laevis at environmentally relevant concentrations. Toxicol. Ind. Health 2014, 30:297-303. 10.1177/0748233712457440.
70. Smith G.R., Burgett A.A. Effects of three organic wastewater contaminants on American toad, Bufo americanus, tadpoles. Ecotoxicology 2005, 14:477-482. 10.1007/s10646-004-1352-7.
71. Sookoian S., Castaño G.O., Burgueño A.L., Rosselli M.S., Gianotti T.F., Mallardi P., Martino J.S., Pirola C.J. Circulating levels and hepatic expression of molecular mediators of atherosclerosis in nonalcoholic fatty liver disease. Atherosclerosis 2010, 209:585-591. 10.1016/j.atherosclerosis.2009.10.011.
72. Srogi K. Monitoring of environmental exposure to polycyclic aromatic hydrocarbons: a review. Environ. Chem. Lett. 2007, 5:169-195.
73. Tietge J.E., Holcombe G.W., Flynn K.M., Kosian P.A., Korte J.J., Anderson L.E., Wolf D.C., Degitz S.J. Metamorphic inhibition of Xenopus laevis by sodium perchlorate: effects on development and thyroid histology. Environ. Toxicol. Chem. 2005, 24:926-933. 10.1897/04-105R.1.
74. Ung C.Y., Lam S.H., Hlaing M.M., Winata C.L., Korzh S., Mathavan S., Gong Z. Mercury-induced hepatotoxicity in zebrafish: in vivo mechanistic insights from transcriptome analysis, phenotype anchoring and targeted gene expression validation. BMC Genomics 2010, 11:212. 10.1186/1471-2164-11-212.
75. Urbatzka R., Bottero S., Mandich A., Lutz I., Kloas W. Endocrine disrupters with (anti)estrogenic and (anti)androgenic modes of action affecting reproductive biology of Xenopus laevis: I. Effects on sex steroid levels and biomarker expression. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2007, 144:310-318. 10.1016/j.cbpc.2006.10.008.
76. Urbatzka R., Lutz I., Opitz R., Kloas W. Luteinizing hormone, follicle stimulating hormone, and gonadotropin releasing hormone mRNA expression of Xenopus laevis in response to endocrine disrupting compounds affecting reproductive biology. Gen. Comp. Endocrinol. 2006, 146:119-125. 10.1016/j.ygcen.2005.10.005.
77. Veldhoen N., Skirrow R.C., Osachoff H., Wigmore H., Clapson D.J., Gunderson M.P., Van Aggelen G., Helbing C.C. The bactericidal agent triclosan modulates thyroid hormone-associated gene expression and disrupts postembryonic anuran development. Aquat. Toxicol. 2006, 80:217-227. 10.1016/j.aquatox.2006.08.010.
78. Wallet M.A., Calderon N.L., Alonso T.R., Choe C.S., Catalfamo D.L., Lalane C.J., Neiva K.G., Panagakos F., Wallet S.M. Triclosan alters anti-microbial and inflammatory responses of epithelial cells. Oral Dis. 2012, 19:296-302. 10.1111/ODI.12001.
79. Yoneda M., Hotta K., Nozaki Y., Endo H., Uchiyama T., Mawatari H., Iida H., Kato S., Hosono K., Fujita K., Yoneda K., Takahashi H., Kirikoshi H., Kobayashi N., Inamori M., Abe Y., Kubota K., Saito S., Maeyama S., Wada K., Nakajima A. Association between PPARGC1A polymorphisms and the occurrence of nonalcoholic fatty liver disease (NAFLD). BMC Gastroenterol. 2008, 8:27. 10.1186/1471-230X-8-27.
80. Zhang X., Pan Y., Yu C., Xu C., Xu L., Li Y., Chen W. PDIA3 knockdown exacerbates free fatty acid-induced hepatocyte steatosis and apoptosis. PLoS One 2015, 10:e0133882. 10.1371/journal.pone.0133882.