Daphnia HR96 is a promiscuous xenobiotic and endobiotic nuclear receptor

Aquatic Toxicology

Volumn 116-117, Issue , 2012, Pages 69-78

  Karimullina, Elina ^a,b   Li, Yangchun ^a   Ginjupalli, Gautam K ^a   Baldwin, William S ^a  

^a CLEMSON UNIVERSITY   (United States)

^b INSTITUTE OF PLANT AND ANIMAL ECOLOGY   (Russian Federation)

Author keywords

Daphnia; HR96; Nuclear receptor; Transactivation; Unsaturated fatty acids

Indexed keywords

BILE ACID; DOCOSAHEXAENOIC ACID; ENVIRONMENTAL CHEMICAL; FATTY ACID; HORMONE RECEPTOR; HORMONE RECEPTOR 96; LINOLEIC ACID; OLEIC ACID; STEROID HORMONE; UNCLASSIFIED DRUG;

CRUSTACEAN; ENVIRONMENTAL STRESS; FATTY ACID; GENOME; PESTICIDE; XENOBIOTICS;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DAPHNIA; MOLECULAR PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BINDING; RECEPTOR UPREGULATION; TRANSACTIVATION; XENOBIOTIC STRESS;

ANIMALS; DAPHNIA; ENZYME ACTIVATION; LIGANDS; LUCIFERASES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SEQUENCE HOMOLOGY, NUCLEIC ACID; WATER POLLUTANTS, CHEMICAL; XENOBIOTICS;

EID: 84859976200     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.03.005     Document Type: Article

References (63)

1. Antebi A., Yeh W.H., Tait D., Hedgecock E.M., Riddle D.L. daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev 2000, 14:1512-1527.
2. Adachi R., Honma Y., Masuno H., Kawana K., Shimomura I., Yamada S., Makishima M. Selective activation of vitamin D receptor by lithocholic acid acetate, a bile acid derivative. J. Lipid Res. 2005, 56:46-57.
3. Antolino-Lobo I., Meulenbelt J., Nijmeijer S.M., Maas-Bakker R.F., Meijerman I., van den Berg M., van Duursen M.B. 3,4-methylenedioxymethamphetamine (MDMA) interacts with therapeutic drugs on CYP3A by inhibition of pregnane X receptor (PXR) activation and catalytic enzyme inhibition. Toxicol. Lett. 2011, 203:82-91.
4. Baldwin W.S., LeBlanc G.A. Identification of multiple steroid hydroxylases in Daphnia magna and their modulation by xenobiotics. Environ. Toxicol. Chem. 1994, 13:1013-1021.
5. Baldwin W.S., Marko P.B., Nelson D.R. The cytochrome P450 (CYP) gene superfamily in Daphnia pulex. BMC Genomics 2009, 10:169.
6. Baldwin W.S., Milam D.L., LeBlanc G.A. Physiological and biochemical perturbations in Daphnia magna following exposure to the model environmental estrogen diethylstilbestrol. Environ. Toxicol. Chem. 1995, 14:945-952.
7. Baldwin W.S., Roling J.A. A concentration addition model for the activation of the constitutive androstane receptor by xenobiotic mixtures. Toxicol. Sci. 2009, 107:93-105.
8. Becker C., Boersma M. Differential effects of phosphorus and fatty acids on Daphnia magna growth and reproduction. Limnol. Oceanogr. 2005, 50:388-397.
9. Bertrand S., Brunet F., Escriva H., Parmentier G., Laudet V., Robinson-Rechavi M. Evolutionary genomics of nuclear receptors: from twenty-five ancestral genes to derived endocrine systems. Mol. Biol. Evol. 2004, 21:1923-1937.
10. Blumberg B., Sabbagh W.J., Juguilon H., Bolado J.J., van Meter C.M., Ong E.S., Evans R.M. SXR, a novel steroid and xenobiotic-sensing nuclear receptor. Genes Dev. 1998, 12:3195-3205.
11. Brett M.T., Muller-Navarra D.C., Ballantyne A.P., Ravet M.L., Goldman C.R. Daphnia fatty acid composition reflects that of their diet. Limnol. Oceanogr. 2006, 51:2428-2437.
12. Bujold M., Gopalakrishnan A., Nally E., King-Jones K. Nuclear receptor DHR96 acts as a sentinel for low cholesterol concentrations in Drosophila melanogaster. Mol. Cell Biol. 2010, 30:793-805.
13. Carpenter S.R., Kitchell J.F., Hodgson J.R., Cochran P.A., Elser J.J., Elser M.M., Lodge D.M., Kretchmer D., He X., von Ende C.N. Regulation of lake primary productivity by food web structure. Ecology 1987, 68:1863-1876.
14. Christiaens O., Iga M., Velarde R.A., Rougé P., Smagghe G. Halloween genes and nuclear receptors in ecdysteroid biosynthesis and signalling in the pea aphid. Insect Mol Biol 2010, 19:187-200.
15. Colbourne J.K., Pfrender M.E., Gilbert D., Thomas W.K., Tucker A., Oakley T.H., Tokishita S., Aerts A., Arnold G.J., Basu M.K., Bauer D.J., Caceres C.E., Carmel L., Casola C., Choi J.-H., Detter J.C., Dong Q., Dusheyko S., Eads B.D., Frohlich T., Geiler-Samerotte K.A., Gerlach D., Hatcher P., Jogdeo S., Krijgsveld J., Kriventseva E.V., Kultz D., Laforsch C., Lindquist E., Lopez J., Manak R., Muller J., Pangilinan J., Patwardhan R.P., Pitluck S., Pritham E.J., Rechtsteiner A., Rho M., Rogozin I.B., Sakarya O., Salamov A., Schaack S., Shapiro H., Shiga Y., Skalitzky C., Smith Z., Souvorov A., Sung W., Tang Z., Tsuchiya D., Tu H., Vos H., Wang M., Wolf Y.I., Yamagata H., Yamada T., Ye Y., Shaw J.R., Andrews J., Crease T.J., Tang H., Lucas S.M., Robertson H.M., Bork P., Zdobnov E.M., Grigoriev I.V., Lynch M., Boore J.L. The ecoresponsive genome of Daphnia pulex. Science 2011, 331:555-561.
16. De Coen W.M., Janssen C.R. The use of biomarkers in Daphnia magna toxicity test. IV. Cellular energy allocation: a new methodology to assess the energy budget of toxicant-stressed Daphnia populations. J. Aquat. Eco. Stress Recov. 1997, 6:43-55.
17. Dong B., Saha P.K., Huang W., Chen W., Abu-Elheiga L.A., Wakil S.J., Stevens R.D., Ilkayeva O., Newgard C.B., Chan L., Moore D.D. Activation of nuclear receptor CAR ameliorates diabetes and fatty liver disease. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18831-18836.
18. Filho T.U.B., Soares A.M.V.M., Loureiro S. Energy budget in Daphnia magna exposed to natural stressors. Envion. Sci. Pollut. Res. 2011, 18:655-662.
19. Finn R.D., Henderson C.J., Scott C.L., Wolf C.R. Unsaturated fatty acid regulation of cytochrome P450 expression via a CAR-dependent pathway. Biochem. J. 2009, 417:43-54.
20. Fisk G.J., Thummel C.S. Isolation, regulation, and DNA-binding properties of three Drosophila nuclear hormone receptor superfamily members. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:10604-10608.
21. Forman B.M., Tzameli I., Choi H.S., Chen J., Simha D., Seol W., Evans R.M., Moore D.D. Androstane metabolites bind to and deactivate the nuclear receptor CAR-beta. Nature 1998, 395:612-615.
22. Gao J., He J., Zhal Y., Wada T., Xie W. The constitutive androstane receptor is an anti-obesity nuclear receptor that improves insulin sensitivity. J. Biol. Chem. 2009, 284:25984-25992.
23. Gao J., Xie W. Pregnane X receptor and constitutive androstane receptor at the crossroads of drug metabolism and energy metabolism. Drug Metab. Dispos. 2010, 38:2091-2095.
24. Hannas B.R., Wang Y.H., Baldwin W.S., Li Y., Wallace A.D., LeBlanc G.A. Interactions of the crustacean nuclear receptors HR3 and E75 in the regulation of gene transcription. Gen. Comp. Endocrinol. 2010, 167:268-278.
25. Haussler M.R., Haussler C.A., Bartik L., Whitfield G.K., Hsieh J.-C., Slater S., Jurutka P.W. Vitamin D receptor: molecular signaling and actions of nutritional ligands in disease prevention. Nutr. Rev. 2008, 66(Suppl. 2):S98-S112.
26. Hernandez J.P., Huang W., Chapman L.M., Chua S., Moore D.D., Baldwin W.S. The environmental estrogen, nonylphenol, activates the constitutive androstane receptor (CAR). Toxicol. Sci. 2007, 98:416-426.
27. Hernandez J.P., Mota L.C., Baldwin W.S. Activation of CAR and PXR by dietary, environmental and occupational chemicals alters drug metabolism, intermediary metabolism, and cell proliferation. Curr. Pharmacog. Personal Med. 2009, 7:81-105.
28. Horner M.A., Pardee K., Liu S., King-Jones K., Lajoie G., Edwards A., Krause H.M., Thummel C.S. The Drosophila DHR96 nuclear receptor binds cholesterol and regulates cholesterol homeostasis. Genes Dev. 2009, 23:2711-2716.
29. Ishizawa M., Matsunawa M., Adachi R., Uno S., Ikeda K., Masuno H., Shimizu M., Iwasaki K., Yamada S., Makishima M. Lithocholic acid derivatives act as selective vitamin D receptor modulators without inducing hypercalcemia. J. Lipid Res. 2008, 49:763-772.
30. King-Jones K., Horner M.A., Lam G., Thummel C.S. The DHR96 nuclear receptor regulates xenobiotic responses in Drosophila. Cell Metab. 2006, 4:37-48.
31. Kliewer S.A., Moore J.T., Wade L., Staudinger J.L., Watson M.A., Jones S.A., McKee D.D., Oliver B.B., Willson T.M., Zetterstrom R.H., Perlmann T., Lehmann J.M. An orphan nuclear receptor activated by pregnanes defines a novel steroid signaling pathway. Cell 1998, 92:73-82.
32. Kretschmer X.C., Baldwin W.S. CAR and PXR: xenosensors of endocrine disrupters?. Chem-Biol. Interact. 2005, 155:111-128.
33. Kuan C.-Y., Walker T.H., Luo P.G., Chen C.-F. Long-chain polyunsaturated fatty acids promote paclitaxel cytotoxicity via inhibition of the MDR1 gene in the human colon cancer Caco-2 cell line. J. Am. Coll. Nutr. 2011, 30:265-273.
34. Laufer H., Biggers W.J. Unifying concepts learned from methyl farnesoate for invertebrate reproduction and post-embryonic development. Am. Zool. 2001, 41:442-457.
35. LeBlanc G.A. Interspecies relationships in acute toxicity of chemicals to aquatic organisms. Environ. Toxicol. Chem. 1984, 3:47-60.
36. Lemaire G., de Sousa G., Rahmani R. A PXR reporter gene assay in a stable cell culture system: CYP3A4 and CYP2B6 induction by pesticides. Biochem. Pharmacol. 2004, 68:2347-2358.
37. Lemaire G., Mnif W., Pascussi J.M., Pillon A., Rabenoelina F., Fenet H., Gomez E., Casellas C., Nicolas J.C., Cavailles V., Duchesne M.J., Balaguer P. Identification of new human pregnane X receptor ligands among pesticides using a stable reporter cell system. Toxicol. Sci. 2006, 91:501-509.
38. Lin G.G., Kozaki T., Scott J.G. Hormone receptor-like in 96 and broad-complex modulate phenobarbital induced transcription of cytochrome P450 CYP6D1 in Drosophila S2 cells. Insect Mol. Biol. 2011, 20:87-95.
39. Lindblom T.H., Pierce G.J., Sluder A.E. A C. elegans orphan nuclear receptor contributes to xenobiotic resistance. Curr. Biol. 2001, 11:864-868.
40. Maglich J.M., Sluder A., Guan X., Shi Y., McKee D.D., Carrick K., Kamdar K., Willson T.M., Moore J.T. Comparison of complete nuclear receptor sets from the human Caenorhabditis elegans and Drosophila genomes. Genome Biol 2001, 2. research0029.0021-0029.0027.
41. Maki A.W. Correlation between Daphnia magna and fathead minnow (Pimephales promelas) chronic toxicity values for several classes of test substances. J. Fish Res. Board Can. 1979, 36:411-421.
42. Marchler-Bauer A., Anderson J.B., Derbyshire M.K., DeWeese-Scott C., Gonzales N.R., Gwadz M., Hao L., He S., Hurwitz D.I., Jackson J.D., Ke Z., Krylov D., Lanczycki C.J., Liebert C.A., Liu C., Lu F., Lu S., Marchler G.H., Mullokandov M., Song J.S., Thanki N., Yamashita R.A., Yin J.J., Zhang D., Bryant S.H. CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 2007, 35:237-240.
43. Mota L.C., Hernandez J.P., Baldwin W.S. CAR-null mice are sensitive to the toxic effects of parathion: association with reduced CYP-mediated parathion metabolism. Drug Metab. Dispos. 2010, 38:1582-1588.
44. Nakamura K., Moore R., Negishi M., Sueyoshi T. Nuclear pregnane X receptor cross-talk with FOXA2 to mediate the drug-induced regulation of lipid metabolism in fasting mouse liver. J. Biol. Chem. 2007, 282:9768-9776.
45. Ourlin J.C., Lasserre F., Pineau T., Fabre J.M., Sa-Cunha A., Maurel P., Vilarem M.J., Pascussi J.M. The small heterodimer partner interacts with the pregnane X receptor and represses its transcriptional activity. Mol. Endocrinol. 2003, 17:1693-1703.
46. Qatanani M., Moore D.D. CAR, the continuously advancing receptor, in drug metabolism and disease. Curr. Drug Metab. 2005, 6:329-339.
47. Regier J.C., Shultz J.W., Zwick A., Hussey A., Ball B., Wetzer R., Martin J.W., Cunningham C.W. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 2010, 463:1079-1083.
48. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
49. Schlechtriem C., Arts M.T., Zellmer I.D. Effect of temperature on the fatty acid composition and temporal trajectories of fatty acids in fasting Daphnia pulex (Crustacea, Cladocera). Lipids 2006, 41:397-400.
50. Sieber M.H., Thummel C.S. The DHR96 nuclear receptor controls triacylglycerol homeostasis in Drosophila. Cell Metab. 2009, 10:481-490.
51. Staudinger J.L., Goodwin B., Jones S.A., Hawkins-Brown D., MacKenzie K.I., LaTour A., Liu Y., Klaassen C.D., Brown K.K., Reinhard J., Willson T.M., Koller B.H., Kliewer S.A. The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc. Natl. Acad. Sci. U S A 2001, 98:3369-3374.
52. Swales K., Negishi M. Car, driving into the future. Mol. Endocrinol. 2004, 18:1589-1598.
53. Takeshita A., Taguchi M., Koibuchi N., Ozawa Y. Putative role of the orphan nuclear receptor SXR (Steroid and Xenobiotics Receptor) in the Mechanism of CYP3A4 Inhibition by Xenobiotics. J. Biol. Chem. 2002, 277:32453-32458.
54. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The clustalx windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 24:4876-4882.
55. Thomson S.A., Baldwin W.S., Wang Y.H., Kwon G., LeBlanc G.A. Annotation, phylogenetics, and expression of the nuclear receptors in Daphnia pulex. BMC Genomics 2009, 10:500.
56. Tzameli I., Pissios P., Schuetz E.G., Moore D.D. The xenobiotic compound 1,4-bis[2-(3,5-dichloropyridyloxy)]benzene is an agonist ligand for the nuclear receptor CAR. Mol. Cell Biol. 2000, 20:2951-2958.
57. US Department of Agriculture, Agricultural Research Service, 2007. USDA Nutrient Database for Standard Reference, Release 20. Retrieved November 15, 2011 from the Nutrient Data Laboratory Home Page: http://www.ars.usda.gov/ba/bhnrc/ndl.
58. Valverde R.A., Robinson G.E., Fahrback S.E. Nuclear receptors in the honey bee: annotation and expression in the adult brain. Insect Mol. Biol. 2006, 15:583-595.
59. Wong K.E., Kong J., Zhang W., Szeto F.L., Ye H., Deb D.K., Brady M.J., Li Y.C. Targeted expression of human vitamin D receptor in adipocytes decreases energy expenditure and induces obesity in mice. J. Biol. Chem. 2011, 286:33804-33810.
60. Wong K.E., ZSzeto F.L., Zhang W., Ye H., Kong J., Zhang Z., Sun X.J., Li Y.C. Involvement of the vitamin D receptor in energy metabolism: regulation of uncoupling proteins. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E820-E828.
61. Xu J., Tan A., Palli S.R. The function of nuclear receptors in regulation of female reproduction and embryogenesis in the red flour beetle, Tribolium castaneum. J. Insect Physiol. 2010, 56:1471-1480.
62. Yu C., Chai X., Yu L., Chen S., Zeng S. Identification of novel pregnane X receptor activators from traditional Chinese medicines. J. Ethnopharmacol. 2011, 136:137-143.
63. Zhang J., Huang W., Qatanani M., Evans R.M., Moore D.D. The constitutive androstane receptor and pregnane X receptor function coordinately to prevent bile acid-induced hepatotoxicity. J. Biol. Chem. 2004, 279:49517-49522.