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Articles

Simvastatin modulates gene expression of key receptors in zebrafish embryos

ORCID Icon, ORCID Icon, , &
Pages 465-476 | Received 15 Mar 2017, Accepted 23 May 2017, Published online: 06 Jul 2017

References

  • Abrams, E. W., and Mullins, M. C. 2009. Early zebrafish development: It’s in the maternal genes. Curr. Opin. Genet. Dev. 19: 396–403.
  • Aleksunes, L. M., and Klaassen, C. D. 2012. Coordinated regulation of hepatic phase I and II drug-metabolizing genes and transporters using AhR-, CAR-, PXR-, PPARα-, and Nrf2-null mice. Drug Metab. Dispos. 40: 1366–1379.
  • Alvarez de Sotomayor, M., Veja, S., Mingorance, C., Marhuenda, E., and Herrera, M. D. 2008. Effects of HMG-CoA reductase inhibition by simvastatin on vascular dysfunction induced by lipopolysaccharide in rats. Pharmacology 82: 89–96.
  • Andersen, C. L., Ledet-Jensen, J., and Ørntoft, T. 2004. Normalization of real-time quantitative RT-PCR data: A model based variance estimation approach to identify genes suited for normalization – applied to bladder- and colon-cancer data-sets. Cancer Res. 64: 5245–5250.
  • Anderson, J. L., Carten, J. D., and Farber, S. A. 2011. Zebrafish lipid metabolism: From mediating early patterning to the metabolism of dietary fat and cholesterol. Meth. Cell. Biol. 101: 111–141.
  • Baker, M. E. and Hardiman, G. 2014. Transcriptional analysis of endocrine disruption using zebrafish and massively parallel sequencing. J. Mol. Endocrinol. 52: R241–R256.
  • Bertrand, S., Thisse, B., Tavares, R., Sachs, L., Chaumot, A., Bardet, P.L., Escrivà, H., Duffraisse, M., Marchand, O., Safi, R., Thisse, C., and Laudet, V. 2007. Unexpected novel relational links uncovered by extensive developmental profiling of nuclear receptor expression. PLoS Genet. 3: e188.
  • Bou, M., Todorčević, M., Rodríguez, J., Capilla, E., Gutiérrez, J., and Navarro, I. 2014. Interplay of adiponectin, TNFα and insulin on gene expression, glucose uptake and PPARγ, AKT and TOR pathways in rainbow trout cultured adipocytes. Gen. Comp. Endocrinol. 205: 218–225.
  • Cajaraville, M. P., Cancio, I., Ibabe, A., and Orbea, A. 2003. Peroxisome proliferation as a biomarker in environmental pollution assessment. Microsc. Res. Tech. 61: 191–202.
  • Carmona-Antoñanzas, G., Tocher, D. R., Martinez-Rubio, L., and Leaver, M.J. 2014. Conservation of lipid metabolic gene transcriptional regulatory networks in fish and mammals. Gene. 534: 1–9.
  • Castro, L. F. and Santos, M. M. 2014. To bind or not to bind: The taxonomic scope of nuclear receptor mediated endocrine disruption in invertebrate phyla. Environ. Sci. Technol. 48: 5361–5363.
  • Chng, H. T., Ho, H. K., Yap, C. W., Lam, S. H., and Chan, E. C. 2012. An investigation of the bioactivation potential and metabolism profile of zebrafish versus human. J. Biomol. Screen. 17: 974–986.
  • Cocci, P., Mosconi, G., Arukwe, A., Mozzicafreddo, M., Angeletti, M., Aretusi, G., and Palermo, F. A. 2015. Effects of diisodecyl phthalate on PPAR: RXR-dependent gene expression pathways in sea bream hepatocytes. Chem. Res. Toxicol. 28: 935–947.
  • Colliar, L., Sturm, A., and Leaver, M. J. 2011. Tributyltin is a potent inhibitor of piscine peroxisome proliferator-activated receptor α and β. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 153: 168–173.
  • Corcoran, J., Lange, A., Winter, M. J., and Tyler, C. R. 2012. Effects of pharmaceuticals on the expression of genes involved in detoxification in a carp primary hepatocyte model. Environ. Sci. Technol. 46: 6306–6314.
  • Costa, J., Reis-Henriques, M. A., Castro, L. F. C., and Ferreira, M. 2012. Gene expression analysis of ABC efflux transporters, CYP1A and GSTα in Nile tilapia after exposure to benzo(a)pyrene. Comput. Biochem. Physiol., Part C: Toxicol. Pharmacol. 155: 469–482.
  • Cunha, V., Santos, M. M., Moradas-Ferreira, P., and Ferreira, M. 2016a. Simvastatin effects on detoxification mechanisms in Danio rerio embryos. Environ. Sci. Pollut. Res. Int. 23: 10615–10629
  • Cunha, V., Rodrigues, P., Santos, M. M., Moradas-Ferreira, P., and Ferreira, M. 2016b. Danio rerio embryos on Prozac - Effects on the detoxification mechanism and embryo development. Aquat. Toxicol. 178: 182–189.
  • Delfosse, V., Maire, A. L., Balaguer, P., and Bourguet, W. 2015. A structural perspective on nuclear receptors as targets of environmental compounds. Acta Pharmacol. Sin. [Epub ahead of print]
  • Elferink, C. J. 2003. Aryl hydrocarbon receptor-mediated cell cycle control. Prog. Cell Cycle Res. 5: 261–267.
  • Ellesat, K. S., Yazdani, M., Holth, T. F., and Hylland, K. 2011. Species-dependent sensitivity to contaminants: an approach using primary hepatocyte cultures with three marine fish species. Mar. Environ. Res. 72: 216–224.
  • Fent, K., Weston, A., and Caminada, D. 2006. Ecotoxicology of human pharmaceuticals. Aquat. Toxicol. 76: 122–159.
  • Fernández, C. G., Roufidou, C., Antonopoulou, E., and Sarropoulou, E. 2013. Expression of developmental-stage-specific genes in the gilthead sea bream Sparus aurata L. Mar. Biotechnol. 15: 313–320.
  • Flynn III, E. J., Trent, C. M., Rawls, J. F. 2009. Ontogeny and nutritional control of adipogenesis in zebrafish (Danio rerio). J. Lipid Res. 50: 1641–1652.
  • Folch, J., Lees, M., and Sloane Stanley, G. H. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226: 497–509.
  • Fraunberger, P., Gröne, E., Gröne, H. J., and Walli, A. K. 2009. Simvastatin reduces endotoxin-induced nuclear factor kappaB activation and mortality in guinea pigs despite lowering circulating low-density lipoprotein cholesterol. Shock 32: 159–163.
  • Frye, C. A., Bo, E., Calamandrei, G., Calzà, L., Dessì-Fulgheri, F., Fernández, M., Fusani, L., Kah, O., Kajta, M., Le Page, Y., Patisaul, H. B., Venerosi, A., Wojtowicz, A. K., and Panzica, G. C. 2012. Endocrine disrupters: A review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J. Neuroendocrinol. 24: 144–159.
  • Gronemeyer, H., Gustafsson, J. A., and Laudet V. 2004. Principles for modulation of the nuclear receptor superfamily. Nat. Rev. Drug. Discov. 3: 950–964.
  • Grün, F. and Blumberg, B. 2006. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology. 147 (6 Suppl): S50–S55.
  • Hahn, M. E. 2002. Aryl hydrocarbon receptors: diversity and evolution. Chem. Biol. Interact. 141: 131–160.
  • Hamadeh, H. K., Bushel, P. R., Jayadev, S., Martin, K., DiSorbo, O., Sieber, S., Bennett, L., Tennant, R., Stoll, R., Barrett, J. C., Blanchard, K., Paules, R. S., and Afshari, C. A. 2002. Gene expression analysis reveals chemical-specific profiles. Toxicol. Sci. 67: 219–231.
  • Hernando, M. D., Mezcua, M., Fernández-Alba, A. R., and Barceló, D. 2006. Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments. Talanta. 69: 334–342.
  • Hessel, S. and Lampen, A. 2010. All-trans retinoic acid enhances the transport of phase II metabolites of benzo[a]pyrene by inducing the breast cancer resistance protein expression in Caco-2 cells. Toxicol. Lett. 197: 151–155.
  • Ibabe, A., Grabenbauer, M., Baumgart, E., Fahimi, H. D., and Cajaraville, M. P. 2002. Expression of peroxisome proliferator-activated receptors in zebrafish (Danio rerio). Histochem. Cell Biol. 118: 231–239.
  • Ipseiz, N., Scholtysek, C., Culemann, S., and Krönke, G. 2014. Adopted orphans as regulators of inflammation, immunity and skeletal homeostasis. Swiss. Med. Wkly. 144: w14055.
  • Jacobson, T. A. 2004. Comparative pharmacokinetic interaction profiles of pravastatin, simvastatin, and atorvastatin when coadministered with cytochrome P450 inhibitors. Am. J. Cardiol. 94: 1140–1146.
  • Janani, C. and Ranjitha Kumari, B. D. 2015. PPAR gamma gene-a review. Diabetes Metab. Syndrome 9: 46–50.
  • Janosek, J., Hilscherová, K., Bláha, L., and Holoubek, I. 2006. Environmental xenobiotics and nuclear receptors–interactions, effects and in vitro assessment. Toxicol. In Vitro. 20: 18–37.
  • Key, P. B., Hoguet, J., Reed, L. A., Chung, K. W., and Fulton, M. H. 2008. Effects of the statin antihyperlipidemic agent simvastatin on grass shrimp. Palaemonetes pugio. Environ. Toxicol. 23: 153–160.
  • Kim, B., Rhee, J., Hwang, U., Seo, J., Shin, K., and Lee, J. 2015. Dose- and time-dependent expression of aryl hydrocarbon receptor (AhR) and aryl hydrocarbon receptor nuclear translocator (ARNT) in PCB-, B[a]P-, and TBT-exposed intertidal copepod Tigriopus japonicas. Chemosphere 120: 398–406.
  • Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203: 253–310.
  • Kobayashi, K., Yamanaka, Y., Iwazaki, N., Nakajo, I., Hosokawa, M., Negishi, M., and Chiba, K. 2005. Identification of HMG-CoA reductase inhibitors as activators for human, mouse and rat constitutive androstane receptor. Drug Metab. Dispos. 2033: 924–929.
  • Kocarek, T. A., Dahn, M. S., Cai, H., Strom, S. C., and Mercer-Haines, N. A. 2002. Regulation of CYP2B6 and CYP3A expression by hydroxymethylglutaryl coenzyme A inhibitors in primary cultured human hepatocytes. Drug Metab. Dispos. 30: 1400–1405.
  • Lee, J., Hong, E. M., Koh, D. H., Choi, M. H., Jang, H. J., Kae, S. H., and Choi, H. S. 2010. HMG-CoA reductase inhibitors (statins) activate expression of PPARalpha/PPARgamma and ABCA1 in cultured gallbladder epithelial cells. Dig. Dis. Sci. 55: 292–299.
  • Lee, S. Y., Lee, J. Y., Kim, Y. M., Kim, S. K., and Oh, S. J. 2015. Expression of hepatic cytochrome P450s and UDP-glucuronosyltransferases in PXR and CAR double humanized mice treated with rifampicin. Toxicol. Lett. 235: 107–115.
  • Lima, D., Castro, L. F., Coelho, I., Lacerda, R., Gesto, M., Soares, J., André, A., Capela, R., Torres, T., Carvalho, A. P., and Santos, M. M. 2015. Effects of tributyltin and other retinoid receptor agonists in reproductive-related endpoints in the zebrafish (Danio rerio). J. Toxicol. Environ. Health A. 78: 747–760.
  • Lyche, J. L., Grześ, I. M., Karlsson, C., Nourizadeh-Lillabadi, R., Aleström, P., and Ropstad, E. 2016. Parental exposure to natural mixtures of persistent organic pollutants (POP) induced changes in transcription of apoptosis-related genes in offspring zebrafish embryos. J. Toxicol. Environ. Health 79: 602–611.
  • Lyssimachou, A., Santos, J. G., André, A., Soares, J., Lima, D., Guimarães, L., Almeida, C. M., Teixeira, C., Castro, L. F., and Santos, M. M. 2015. The mammalian “Obesogen” tributyltin targets hepatic triglyceride accumulation and the transcriptional regulation of lipid metabolism in the liver and brain of zebrafish. PLoS One. 10: e0143911.
  • Mangelsdorf, D. J., and Evans, R. M. 1995. The RXR heterodimers and orphan receptors. Cell. 83: 841–850.
  • Martin, G., Duez, H., Blanquart, C., Berezowski, V., Poulain, P., Fruchart, J. C., Najib-Fruchart, J., Glineur, C., and Staels, B. 2001. Statin-induced inhibition of the Rho-signaling pathway activates PPARalpha and induces HDL apoA-I. J. Clin. Invest. 107: 1423–1432.
  • Mortensen, A. S. and Arukwe, A. 2007. Effects of 17alpha-ethynylestradiol on hormonal responses and xenobiotic biotransformation system of Atlantic salmon (Salmo salar). Aquat. Toxicol. 85: 113–123.
  • Neuparth, T., Martins, C., de los Santos, C. B., Costa, M. H., Martins, I.Costa, P. M., and Santos, M. M. 2014. Hypocholesterolaemic pharmaceutical simvastatin disrupts reproduction and population growth of amphipod Gammarus locusta at the ng/L range. Aquat. Toxicol. 155: 337–347.
  • Ortiz de García, S. A., Pinto Pinto, G., García-Encina, P. A., and Irusta-Mata, R. 2014. Ecotoxicity and environmental risk assessment of pharmaceuticals and personal care products in aquatic environments and wastewater treatment plants. Ecotoxicology 23: 1517–1533.
  • Ottmar, K. J., Colosi, L. M., and Smith, J. A. 2012. Fate and transport of atorvastatin and simvastatin drugs during conventional wastewater treatment. Chemosphere 88: 1184–1189.
  • Pardee, K., Necakov, A. S., and Krause, H. 2011. Nuclear receptors: Small molecule sensors that coordinate growth, metabolism and reproduction. Subcell Biochem. 52: 123–153.
  • Pereira, A. M. P. T., Silva, L. J., Meisel, L. M., and Pena, A. 2015. Fluoroquinolones and tetracycline antibiotics in a Portuguese aquaculture system and aquatic surroundings: Occurrence and environmental impact. J. Toxicol. Environ. Health 78: 959–975.
  • Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucl. Acids Res. 1: e45.
  • Powell, W. H., Bright, R., Bello, S. M., and Hahn, M. E. 2000. Developmental and tissue-specific expression of AHR1, AHR2, and ARNT2 in dioxin-sensitive and -resistant populations of the marine fish Fundulus heteroclitus. Toxicol. Sci. 57: 229–239.
  • Prasch, A., Teraoka, H., Carney, S. A., Dong, W., Hiraga, T., Stegeman, J., Heideman, W., and Peterson, R. E. 2003. Aryl hydrocarbon receptor 2 mediates 2,3,7,8-tetrachlorodibenzo-p-dioxin developmental toxicity in zebrafish. Toxicol. Sci. 76: 138–150.
  • Ravingerová, T., Adameová, A., Kelly, T., Antonopoulou, E., Pancza, D., Ondrejcáková, M., Khandelwal, V. K., Carnická, S., and Lazou, A. 2009. Changes in PPAR gene expression and myocardial tolerance to ischaemia: Relevance to pleiotropic effects of statins. Can. J. Physiol. Pharmacol. 87: 1028–1036.
  • Ribeiro, S., Torres, T., Martins, R., and Santos, M. M. 2015. Toxicity screening of diclofenac, propanolol, sertraline and simvastatin using Danio rerio and Paracentrotus lividus embryo bioassays. Ecotoxicol. Environ. Saf. 114: 67–74.
  • Rodwell, V. W., Nordstrom, J. L., and Mitschelen, J. H. 1976. Regulation of HMG-CoA reductase. Adv. Lipid Res. 14: 1–74.
  • Ruyter, B., Andersen, O., Dehli, A., Ostlund Farrants, A. K., Gjøen, T., and Thomassen, M. S. 1997. Peroxisome proliferator activated receptors in Atlantic salmon (Salmo salar): Effects on PPAR transcription and acyl-CoA oxidase activity in hepatocytes by peroxisome proliferators and fatty acids. Biochim. Biophys. Acta. 1348: 331–338.
  • Santos da Rosa, J. G., Koakoski, G., Piato, A. L., Bogo, M. R.,Bonan, C. D., and Barcellos, L. J. 2016. Impaired brain StAR and HSP70 gene expression in zebrafish exposed to Methyl-Parathion based insecticide. J. Toxicol. Environ. Health 79: 1–7.
  • Santos, L. H., Araújo, A. N., Fachini, A., Pena, A., Delerue-Matos, C., and Montenegro, M. C. 2010. Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J. Hazard Mater. 175: 45–95.
  • Santos, M. M., Ruivo, R., Lopes-Marques, M., Torres, T., de Los Santos, C. B., Castro, L. F., and Neuparth, T. 2016. Statins: An undesirable class of aquatic contaminants? Aquat. Toxicol. 174: 1–9.
  • Soares, J., Coimbra, A. M., Reis-Henriques, M. A., Monteiro, N. M., Vieira, M. N., Oliveira, J. M., Guedes-Dias, P., Fontaínhas-Fernandes, A., Parra, S. S., Carvalho, A. P., Castro, L. F., and Santos, M. M. 2009. Disruption of zebrafish (Danio rerio) embryonic development after full life-cycle parental exposure to low levels of ethinylestradiol. Aquat. Toxicol. 95: 330–338.
  • Tallafuss, A., Hale, L. A., Yan, Y. L., Dudley, L., Eisen, J. S., and Postlethwait, J. H. 2006. Characterization of retinoid-X receptor genes rxra, rxrba, rxrbb and rxrg during zebrafish development. Gene. Exp. Patterns. 6: 556–565.
  • Tian, S., Pan, L., and Sun, X. 2013. An investigation of endocrine disrupting effects and toxic mechanisms modulated by benzo[a]pyrene in female scallop Chlamys farreri. Aquat Toxicol. 144–145:162–171.
  • Urbaztka, R., Galante-Oliveira, S., Rocha, E., Castro, L., and Cunha, I. 2013. Nornalization strategies for gene expression studies by real-time PCR in marine fish species, Scophthalmus maximus. Mar. Genom. 10: 17–25.
  • Wang, H., and LeCluyse, E. L. 2003. Role of orphan nuclear receptors in the regulation of drug-metabolising enzymes. Clin. Pharmacokinet. 42: 1331–1357.
  • Wang, J. A., Chen, W. A., Wang, Y., Zhang, S., Bi, H., Hong, B., Luo, Y., Daugherty, A., and Xie, X. 2011. Statins exert differential effects on angiotensin II-induced atherosclerosis, but no benefit for abdominal aortic aneurysms. Atherosclerosis. 217: 90–96.
  • Wang, Y. M., Ong, S. S., Chai, S. C., and Chen, T. 2012. Role of car and pxr in xeno-biotic sensing and metabolism. Exp. Opin. Drug Metab. Toxicol. 8: 803–817.
  • Wassmur, B., Gräns, J., Kling, P., and Celander, M. C. 2010. Interactions of pharmaceuticals and other xenobiotics on hepatic pregnane X receptor and cytochrome P450 3A signaling pathway in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol. 100: 91–100.
  • Xu, C., Li, Y. C., and Kong, A. T. 2005. Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch. Pharm. Res. 28: 249–268.
  • Yamasaki, D., Nakamura, T., Okamura, N., Kokudai, M., Inui, N., Takeuchi, K., Watanabe, H., Hirai, M., Okumura, K., and Sakaeda, T. 2009. Effects of acid and lactone forms of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors on the induction of MDR1 expression and function in LS180 cells. Eur. J. Pharm. Sci. 37: 126–132.
  • Yu, V. C., Delsert, C., Andersen, B., Holloway, J. M., Devary, O. V., Naar, A. M., Kim, S. Y., Boutin, J. M., Glass, C. K., and Rosenfeld, M. G. 1991. RXR beta: A coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell. 676: 1251–1266.
  • Zhao, Y., Zhang, K., Giesy, J. P., and Hu, J. 2015. Families of nuclear receptors in vertebrate models: Characteristic and comparative toxicological perspective. Sci. Rep. 25: 8554.
  • Zhou, H., Wu, H., Liao, C., Diao, X., Zhen, J., Chen, L., and Xue, Q. 2010. Toxicology mechanism of the persistent organic pollutants (POPs) in fish through AhR pathway. Toxicol. Mech. Meth. 20: 279–286.
  • Zou, C., Qi, H., Liu, Z. H., Han, L., Zhao, C., and Yang, X. 2013. Simvastatin activates the PPARγ-dependent pathway to prevent left ventricular hypertrophy associated with inhibition of RhoA signaling. Tex. Heart Inst. J. 40: 140–147.

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