Exposure to atrazine affects the expression of key genes in metabolic pathways integral to energy homeostasis in Xenopus laevis tadpoles

Aquatic Toxicology

Volumn 104, Issue 3-4, 2011, Pages 254-262

  Zaya, Renee M ^a   Amini, Zakariya ^a   Whitaker, Ashley S ^a   Ide, Charles F ^a  

^a WESTERN MICHIGAN UNIVERSITY   (United States)

Author keywords

ADP; ATP; Atrazine; Microarray; QRT PCR; Xenopus

Indexed keywords

ACYL COENZYME A DEHYDROGENASE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ATRAZINE; GLUCOCORTICOID RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA;

ATRAZINE; DNA; GENE EXPRESSION; HOMEOSTASIS; POLLUTION EXPOSURE; POLYMERASE CHAIN REACTION;

ACYL COA DEHYDROGENASE GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; DNA MICROARRAY; ENERGY BALANCE; ENERGY METABOLISM; FAT BODY; FATTY ACID OXIDATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLUCOCORTICOID RECEPTOR GENE; LIPID STORAGE; LIPOGENESIS; NONHUMAN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR BETA GENE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; TADPOLE; XENOPUS LAEVIS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ATRAZINE; GENE EXPRESSION; HERBICIDES; HOMEOSTASIS; LARVA; METABOLIC NETWORKS AND PATHWAYS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; WATER POLLUTANTS, CHEMICAL; XENOPUS LAEVIS;

ANIMALIA; XENOPUS LAEVIS;

EID: 79957555849     PISSN: 0166445X     EISSN: 0166445X     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.04.022     Document Type: Article

References (64)

1. Abel E.L., Opp S.M., Verlinde C.L.M.J., Bammler T.K., Eaton D.L. Characterization of atrazine biotransformation by human and murine glutathione-s-transferases. Toxicol. Sci. 2004, 80:230-238.
2. Alvarez M.C., Fuiman L.A. Environmental levels of atrazine and its degradation products impair survival skills and growth of red drum larvae. Aquat. Toxicol. 2005, 74:229-241.
3. Battaglin W.A., Rice K.C., Focazio M.J., Salmons S., Barry R.X. The occurrence of glyphosate, atrazine and other pesticides in vernal pools and adjacent streams in Washington, DC, Maryland, Iowa and Wyoming, 2005-2006. Environ. Monit. Assess. 2009, 155:281-307.
4. Bisson M., Hontela A. Cytotoxic and endocrine-disrupting potential of atrazine, diazinon, endosulfan, and mancozeb in adrenocortical steroidogenic cells of rainbow trout exposed in vitro. Toxicol. Appl. Pharmacol. 2002, 180:110-117.
5. Boyle R., McLean S., Foley W.J., Davies N.W. Comparative metabolism of dietary terpene, p-cymene, in generalist and specialist folivorous marsupials. J. Chem. Ecol. 2000, 25:2109-2126.
6. Bradbury D.A., Simmons T.D., Slater K.J., Crouch S.P.M. Measurement of the ADP:ATP ratio in human leukaemic cell lines can be used as an indicator of the cell viability, necrosis and apoptosis. J. Immunol. Meth. 2000, 240:79-92.
7. Brodkin M.A., Madhoun H., Rameswaren M., Vatnick I. Atrazine is an immune disruptor in adult northern leopard frogs (Rana pipiens). Environ. Toxicol. Chem. 2007, 26:80-84.
8. Cericato L., Neto J.G., Kreutz L.C., Quevedo R.M., da Rosa J.G., Koakoski G., Centenaro L., Pottker E., Marqueze A., Barcellos L.J. Responsiveness of the interrenal tissue of Jundia (Rhamdi quelen) to an in vivo ACTH test following acute exposure to sublethal concentrations of agrichemicals. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2009, 149:363-367.
9. Cooper R.I., Stoker T.E., Tyrey L., Goldman J.M., McElroy W.K. Atrazine disrupts the hypothalamic control of pituitary-ovarian function. Toxicol. Sci. 2000, 53:297-307.
10. DiMarco J.P., Hoppel C. Hepatic mitochondrial function in ketogenic states. Diabetes, starvation and after growth hormone administration. J. Clin. Invest. 1975, 55:1237-1244.
11. Dong Y., Poellinger L., Gustafsson J.A., Okret S. Regulation of glucocorticoid receptor expression: evidence for transcriptional and posttranslational mechanisms. Mol. Endocrinol. 1988, 2:1256-1264.
12. Dorval J., Leblond V., Deblois C., Hontela H. Oxidative stress and endocrine endpoints in white sucker (Catostomus commersoni) from a river impacted by agricultural chemicals. Environ. Toxicol. Chem. 2005, 24:1273-1280.
13. Eason T.H., Scanlon P.F. Effects of atrazine and glyphosate ingestion on body weight and nutritional well-being of Coturnix quail. Z. Zagdwiss 2002, 48(Suppl. 1):281-285.
14. Egaas E., Skaare J.U., Svendsen N.O., Sandvik M., Falls J.G., Dauterman W.C., Collier T.K., Netland J. A comparative study of effects of atrazine on xenobiotic metabolizing enzymes in fish and insect, and of the in vitro phase II atrazine metabolism in some fish, insects, mammals and one plant species. Comp. Biochem. Physiol. C 1993, 106:141-149.
15. Elia A.C., Waller W.T., Norton S.J. Biochemical responses of bluegill sunfish (Lepomis macrochirus Rafinesque) at atrazine induced oxidative stress. Bull. Environ. Contam. Toxicol. 2002, 68:809-816.
16. Elmore S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007, 35:495-516.
17. Fan W.Q., Yanase T., Morinaga H., Gondo S., Okabe T., Nomura M., Komatsu T., Morohashi K.I., Hayes T.B., Takayanagi R., Nawata H. Atrazine-induced aromatase expression is SF-1 dependent: implications for endocrine disruption in wildlife and reproductive cancers in humans. Environ. Health Perspect. 2008, 115:720-727.
18. Freeman J.L., Rayburn A.L. Developmental impact of atrazine on metamorphing Xenopus laevis as revealed by nuclear analysis and morphology. Environ. Toxicol. Chem. 2005, 24:1648-1653.
19. Fisher M.A., Mehne C., Means J.C., Ide C.F. Induction of CYP1A mRNA in Carp (Cyprinus carpio) from the Kalamazoo River Polychlorinated Biphenyl-Contaminated Superfund Site and in a Laboratory Study. Arch. Environ. Contam. Toxicol. 2006, 50:14-22.
20. Gammon D.W., Aldous C.N., Carr W.C., Sanborn J.R., Pfeifer K.F. A risk assessment of atrazine use in California: human health and ecological aspects. Pest Manag. Sci. 2005, 61:331-355.
21. Gaynor J.D., Tan C.S., Drury C.F., van Wesenbeeck I.J., Welacky T.W. Atrazine in surface and subsurface runoff as affected by cultural practices. Water Qual. Res. J. Can. 1995, 30:513-531.
22. Gluth G., Hanke W. A comparison of physiological changes in carp, Cyrpinus carpio, induced by several pollutants at the sublethal concentrations. 1. The dependency on exposure time. Ecotoxicol. Environ. Saf. 1985, 9:179-188.
23. Gross C.J., Kramer J.A. The role of investigative molecular toxicology in early stage drug development. Expert Opin. Drug Saf. 2003, 2:147-159.
24. Gupta S. Molecular signaling in death receptor and mitochondrial pathways of apoptosis. Int. J. Oncol. 2003, 22:15-20. (review).
25. Hanioka N., Jinno H., Tanaka-Kagawa T., Nishimura T., Ando M. In vitro metabolism of simazine, atrazine, and propazine by hepatic Cytochrome P450 enzymes of rat, mouse and guinea pig, and oestrogenic activity of chlorotriazines and their main metabolites. Xenobiotica 1999, 29:1213-1226.
26. Hansen J.M., Go Y.M., Jones D.P. Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. Annu. Rev. Pharmacol. Toxicol. 2006, 46:215-243.
27. Holloway A.C., Anger D.A., Crankshaw D.J., Wu M., Foster G. Atrazine-induced changes in aromatase activity in estrogen sensitive target tissues. J. Appl. Toxicol. 2008, 28:260-270.
28. Hu C., Wang L., Chodosh L.A., Keith B., Simon M.C. Differential roles of hypoxia factor 1β (HIF-1β) and HIF-2β in hypoxic gene regulation. Mol. Cell. Biol. 2003, 23:9361-9374.
29. Infurna R., Levy B., Meng C., Yau E., Traina V., Rolofson G., Stevens J., Barnett J. Teratological evaluations of atrazine technical, a triazine herbicide, in rats and rabbits. J. Toxicol. Environ. Health 1988, 24:307-319.
30. Klionsky D.J., Emr S.C. Autophagy as a regulated pathway of cellular degradation. Science 2003, 290:1717-1721.
31. Kyrou L., Tsigos C. Stress hormones: physiological stress and regulation of metabolism. Curr. Opin. Pharmacol. 2009, 9:787-793.
32. Lando D., Gorman J.J., Whitelaw M.L., Peet D.J. Oxygen regulation of hypoxia-inducible factors by prolyl and asparaginyl hydroxylation. Eur. J. Biochem. 2003, 270:781-790.
33. Lang D., Criegee D., Grothusen A., Saalfrank R.W., Böcker R.H. In vitro metabolism of atrazine, terbuthylazine, ametryne, and terbutryne in rats, pigs, and humans. Drug Metab. Dispos. 1996, 24:859-865.
34. Langerveld A.J., Celestine R., Zaya R., Mihalko D., Ide C.F. Chronic exposure to high levels of atrazine alters expression of genes that regulate immune and growth-related functions in developing Xenopus laevis tadpoles. Environ. Res. 2009, 109:379-389.
35. Laws S.C., Ferrel J.M., Stoker T.E., Cooper R.L. Pubertal development in female Wistar rats following exposure to propazine and atrazine biotransformation by-products, diamino-s-chlorotriazine and hydroxyatrazine. Toxicol. Sci. 2003, 76:190-200.
36. Lehigh Shirey E.A., Langerveld A.J., Mihalko D., Ide C.F. Polychlorinated biphenyl exposure delays metamorphosis and alters thyroid hormone system gene expression in developing Xenopus laevis. Environ. Res 2006, 102:205-214.
37. Lin J., Tarr P.T., Yang R., Rhee J., Puigserver P., Newgard C.B., Spiegelman B.M. PGC-1β in the regulation of hepatic glucose and energy metabolism. J. Biol. Chem. 2003, 278:30843-30848.
38. Lu S.C. Regulation of glutathione synthesis. Mol. Asp. Med. 2009, 30:42-59.
39. McCarthy I.D., Fuiman L.A. Growth and protein metabolism in red drum (Sciaenops ocellatus) larvae exposed to environmental levels of atrazine and malathion. Aquat. Toxicol. 2008, 88:220-229.
40. McMullin T.S., Brzezicki J.M., Cranmer B.K., Tessari J.D., Andersen M.E. Pharmacokinetic modeling of disposition and time-course studies with [14C]atrazine. J. Toxicol. Environ. Health A 2003, 66:941-964.
41. McMullin T.S., Andersen M.E., Nagahara A., Lund T.D., Pak T., Handa R.J., Hanneman W.H. Evidence that atrazine and diaminochlorotriazine inhibit the estrogen/progesterone induced surge of luteinizing hormone in female Sprague-Dawley rats without changing estrogen receptor actin. Toxicol. Sci. 2004, 79:278-286.
42. Messner B., Berndt J., Still J. Increases in rat liver cyclic AMP and glycogen phosphorylase activity caused by the herbicide atrazine. Biochem. Pharmacol. 1979, 28:207-210.
43. Napolitano M.J., Shain D.H. Quantitating adenylate nucleotides in diverse organisms. J. Biophys. Meth. 2005, 63:69-77.
44. Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin) a Systematic and Chronological Survey of the Development from the Fertilized Egg Till the End of Metamorphosis 1994, Garland Publishing, Inc., New York & London.
45. Nieves-Puigdoller K., Bjornsson B.N., McCormick S.D. Effects of hexazinone and atrazine on the physiology and endocrinology of smolt development in Atlantic salmon. Aquat. Toxicol. 2007, 84:27-37.
46. Ottinger M.A., Lavoie E., Thompson N., Whitehouse K., Barton M., Abdelnabi M., McKernan M., Pollack S., Quinn M. Comparative effects of estrogenic, androgenic endocrine disruptors, and atrazine on behavior and neuroendocrine systems in quail. ICN 2006 Conference Abstracts, Comparative neuroendocrinology. Front. Neuroendocr. 2006, 27:23.
47. Patel M.S., Korotchkina L.G. Regulation of the pyruvate dehydrogenase complex. Biochem. Soc. Trans. 2006, 34:217-222.
48. Pinchuk L.M., Lee S.R., Filipov N.M. In vitro atrazine exposure affects that phenotypic and functional maturation of dendritic cells. Toxicol. Appl. Pharmacol. 2007, 223:206-217.
49. Pruett S.B., Fan R., Zheng Q., Myers L.P., Hébert P. Modeling and predicting immunological effects of chemical stressors: characterization of a quantitative biomarker for immunological changes caused by atrazine and ethanol. Toxicol. Sci. 2003, 75:343-354.
50. Randle P.J. Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years. Diabetes Metab. Rev. 1998, 14:263-283.
51. Rayner J.L., Enoch R.R., Fenton S. Adverse effects of prenatal exposure to atrazine during a critical period of mammary gland growth. Toxicol. Sci. 2005, 87:255-266.
52. Rowe A.M., Brundage K.M., Barnett J.B. In vitro atrazine-exposure inhibits human natural killer cell lytic granule release. Toxicol. Appl. Pharmacol. 2007, 221:179-188.
53. Rowe A.M., Brundage K.M., Barnett J.B. Developmental immunotoxicity of atrazine in rodents. Basic Clin. Pharmacol. Toxicol. 2008, 102:139-145.
54. Santa-Maria C., Moreno J., Lopez-Campos J.L. Hepatotoxicity induced by the herbicide atrazine in the rat. J. Appl. Toxicol. 1987, 7:373-378.
55. Srinivas T., Prasad T.A., Raffi G.M., Reddy D.C. Effect of atrazine on some aspects of lipid metabolism in fresh water fish. Biochem. Int. 1991, 23:603-609.
56. Stoker T.E., Guidici D.L., Laws S.C., Cooper R.L. The effects of atrazine metabolites on puberty and thyroid function in the male Wistar rat. Toxicol. Sci. 2002, 67:198-206.
57. Storrs S.I., Kiesecker J.M. Survivorship patterns of larval amphibians exposed to low concentrations of atrazine. Environ. Health Perspect. 2004, 112:1054-1057.
58. Tavera-Mendoza L., Ruby S., Brousseau P., Fournier M., Cyr D., Marcogliese D. Response of the amphibian tadpole (Xenopus laevis) to atrazine during sexual differentiation of the testis. Environ. Toxicol. Chem. 2001, 21:527-531.
59. Tavera-Mendoza L., Ruby S., Brousseau P., Fournier M., Cyr D., Marcogliese D. Response of the amphibian tadpole (Xenopus laevis) to atrazine during sexual differentiation of the ovary. Environ. Toxicol. Chem. 2002, 21:1264-1267.
60. Wanders R.J., Ferdinandusse S., Brites P., Kemp S. Peroxisomes, lipid metabolism and lipotoxicity. Biochim. Biophys. Acta 2010, 1801:272-280.
61. Waterlow J.C. The mysteries of nitrogen balance. Nutr. Res. Rev. 1999, 12:25-54.
62. Weigand C., Krause E., Steinberg C., Pflugmacher S. Toxicokinetics of atrazine in embryos of the zebrafish (Danio rerio). Ecotoxicol. Environ. Saf. 2001, 49:199-205.
63. Yuanxiang J., Xiangxiang Z., Shu L., Chen L., Sun L., Qian H., Liu W., Fu Z. Oxidative stress response and gene expression with atrazine exposure in adult female zebrafish (Danio rerio). Chemosphere 2010, 78:846-852.
64. Zaya, R.M., Amini, Z., Whitaker, A.S., Kohler, S., Ide, C.F., 2011 Atrazine exposure affects growth, body condition and liver health in Xenopus laevis tadpoles, Aquat. Toxicol. doi:10.1016/j.aquatox.2011.04.021.