Atrazine exposure affects growth, body condition and liver health in Xenopus laevis tadpoles

Aquatic Toxicology

Volumn 104, Issue 3-4, 2011, Pages 243-253

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

^a WESTERN MICHIGAN UNIVERSITY   (United States)

Author keywords

Atrazine; Fat body; Liver; Tadpoles; Xenopus

Indexed keywords

ATRAZINE; CASPASE 3; GLYCOGEN; LIPID;

APOPTOSIS; ATRAZINE; BODY CONDITION; DOSE-RESPONSE RELATIONSHIP; FEEDING BEHAVIOR; FROG; GROWTH RATE; GROWTH RESPONSE; HEALTH STATUS; LARVAL DEVELOPMENT; METAMORPHOSIS; MORTALITY; POLLUTION EFFECT; POLLUTION EXPOSURE; SEX RATIO;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY SIZE; BODY WEIGHT; CONTROLLED STUDY; FAT BODY; FEEDING BEHAVIOR; FEMALE; GLYCOGEN LIVER LEVEL; GROWTH; IMMUNOHISTOCHEMISTRY; LIPID LIVER LEVEL; LIPID STORAGE; LIVER CELL; LIVER FUNCTION; LIVER WEIGHT; MALE; METAMORPHOSIS; NONHUMAN; ORGAN SIZE; PRIORITY JOURNAL; REPRODUCTIVE FITNESS; SEX DIFFERENTIATION DISORDER; SEX RATIO; SURVIVAL RATE; TADPOLE; XENOPUS LAEVIS;

ANIMALS; ATRAZINE; BODY SIZE; CASPASE 3; FAT BODY; FEEDING BEHAVIOR; HERBICIDES; LARVA; LIVER; METAMORPHOSIS, BIOLOGICAL; SEX RATIO; WATER POLLUTANTS, CHEMICAL; XENOPUS LAEVIS;

ANURA; XENOPUS LAEVIS;

EID: 79957636089     PISSN: 0166445X     EISSN: 0166445X     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.04.021     Document Type: Article

References (66)

1. Allran J.W., Karasov W.H. Effects of atrazine on embryos, larvae, and adults of anuran amphibians. Environ. Toxicol. Chem. 2001, 20(4):769-775.
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. Amacher D.E., Schomaker S.J., Burkhardt J.E.J.E. The relationship among microsomal enzyme induction, liver weight and histological change in rat toxicology studies. Food Chem. Toxicol. 1998, 36:831-839.
4. Biagianti-Risbourg S., Bastide J. Hepatic perturbations induced by a herbicide (atrazine) in juvenile grey mullet Liza ramada (Mugilidae, Teleostei): an ultrastructural study. Aquat. Toxicol. 1995, 31:217-229.
5. 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.
6. 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.
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. Carr J.A., Gentles A., Smith E.E., Goleman W.L., Urquidi L.J., Thuett K., Kendall R.J., Geisy J.P., Gross T.S., Solomon K.R., Van Der Kraak G. Response of larval Xenopus laevis to atrazine: assessment of growth, metamorphosis, and gonadal and laryngeal morphology. Environ. Toxicol. Chem. 2003, 22:396-405.
9. Celestine, R.E., 2006. Molecular analysis of the effects of atrazine on Xenopus laevis frogs. Ph.D. Dissertation. Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan.
10. Coady K.K., Murphy M.B., Villeneuve D.L., Hecker M., Jones P.D., Carr J.A., Solomon K.R., Smith E.E., Van Der Kraak G., Kendall R.J., Giesy J.P. Effects of atrazine on metamorphosis, growth, and gonadal development in the green frog (Rana clamitans). J. Toxicol. Environ. Health, Part A: Curr. Iss. 2004, 67:941-957.
11. Coady K.K., Murphy M.B., Villeneuve D.L., Hecker M., Jones P.D., Carr J.A., Solomon K.R., Smith E.E., Van Der Kraak G., Kendall R.J., Giesy J.P. Effects of atrazine on metamorphosis, growth, laryngeal and gonadal development, aromatase activity, and sex steroid concentrations in Xenopus laevis. Ecotoxicol. Environ. Saf. 2005, 62:160-173.
12. Denver R.J., Glennemeier K.A., Boorse G.C. Endocrinology of complex life cycles: amphibians. Hormones, Brain and Behavior 2002, 469-513. Elsevier Science, USA. D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach, R. Rubin (Eds.).
13. Diana S.G., Resetarits W.J., Schaeffer D.J., Beckmen K.B., Beasley V.R. Effects of atrazine on amphibian growth and survival in artificial aquatic communities. Environ. Toxicol. Chem. 2000, 19:2961-2967.
14. Dorval J., Leblond V., Deblois C., Hontela A. Oxidative stress and endocrine endpoints in white sucker (Catostomus commersoni) from a river impacted by agricultural chemicals. Environ. Toxicol. Chem. 2005, 24:1273-1280.
15. 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.
16. Edginton A.N., Rouleau C. Toxicokinetics of 14C-atrazine and its metabolites in stage-66 Xenopus laevis. Environ. Sci. Technol. 2005, 29:8083-8089.
17. 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.
18. Elmore S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007, 35:495-516.
19. EPA, 2009. EPA-HQ-OPP-2003-0367-0186 found at http://www.regulations.gov/search/Regs/home.html%23documentDetail%3FR=0900006480a13725.
20. Etheridge A.L., Richter S.M.A. Xenopus laevis: Rearing and Breeding of the African Clawed Frog Booklet 1978, Nasco, Fort Atkinson, WI.
21. 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.
22. Fitzpatrick L.C. Life history patterns of storage and utilization of lipids for energy in amphibians. Am. Zool. 1976, 16:725-732.
23. 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.
24. 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.
25. 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.
26. Girish S., Saidapur S.K. Interrelationship between food availability, fat body, and ovarian cycle in the frog, Rana tigrina, with a discussion on the role of fat body in anuran reproduction. J. Exp. Zool. 2000, 286:487-493.
27. 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.
28. Gupta S. Molecular signaling in death receptor and mitochondrial pathways of apoptosis. Int. J. Oncol. 2003, 22:15-20. (review).
29. Hayes T.B., Collins A., Lee M., Mendoza M., Noriega N., Stuart A.A., Vonk A. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:5476-5480.
30. Hayes T., Haston K., Tsui M., Hoang A., Haeffele C., Vonk A. Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ. Health Perspect. 2003, 111:568-575.
31. Hecker M., Giesy J.P., Jones P.D., Jooste A.M., Carr J.A., Solomon K.R., Smith E.E., Van Der Kraak G., Kendall R.L., Du Preez L. Plasma sex steroid concentrations and gonadal aromatase activities in African clawed frogs (Xenopus laevis) from South Africa. Environ. Toxicol. Chem. 2004, 23:1996-2007.
32. Hoff K.S., Blaustein A.R., McDiarmid R.W., Altig R. Behavior interactions and their consequences. Tadpoles: The Biology of Anuran Larvae 1999, 215-239. University of Chicago Press, Chicago & London. R.W. McDiarmid, R. Altig (Eds.).
33. 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.
34. Houck A., Sessions S.K. Could atrazine affect the immune system of the frog Rana pipiens?. Bios 2006, 77(4):107-112.
35. Huber W. Ecotoxicological relevance of atrazine in aquatic systems. Environ. Toxicol. Chem. 1993, 12:1865-1881.
36. Jendrach M., Mai S., Pohl S., Voth M., Bereiter-Hahn J. Short- and long-term alterations of mitochondrial morphology, dynamics and mtDNA after transient oxidative stress. Mitochondrion 2008, 8:293-304.
37. Jooste A.M., Du Preez L.H., Carr J.A., Giesy J.P., Gross T.S., Kendall R.J., Smith E.E., Van Der Kraak G.L., Solomon K.R. Gonadal development of larval Xenopus laevis exposed to atrazine in outdoor microcosms. Environ. Sci. Technol. 2005, 39:5255-5261.
38. Kloas W., Lutz I., Springer T., Krueger H., Wolf J., Holden L., Hosmer A. Does atrazine influence larval development and sexual differentiation of Xenopus laevis?. Toxicol. Sci. 2009, 107:376-384.
39. Kowaltowski A.J., Vercesi A.E. Mitochondrial damage induced by conditions of oxidative stress. Free Radic. Biol. Med. 1999, 26:463-471.
40. LaFiandra E.M., Babbitt K.J., Sower S.A. Effects of atrazine on anuran development are altered by the presence of a nonlethal predator. J. Toxicol. Environ. Health A 2008, 71:505-511.
41. 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.
42. Langlois V.S., Carew A.C., Pauli B.D., Wade M.G., Cooke G.M., Trudeau V.L. Low levels of the herbicide atrazine alters sex ratios and reduces metamorphic success in Rana pipiens tadpoles raised in outdoor mesocosms. Environ. Health Perspect. 2010, 118:552-557.
43. 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.
44. Lenkowski J.R., Reed J.M., Deininger L., McLaughlin K.A. Perturbation of organogenesis by the herbicide atrazine in the amphibian Xenopus laevis. Environ. Health Perspect. 2008, 116:223-230.
45. 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.
46. 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.
47. Murphy M.B., Hecker M., Coady K.K., Tompsett A.R., Jones P.D., Du Preez L.H., Everson G.J., Solomon K.R., Carr J.A., Smith E.E., Kendall R.J., Van Der Kraak G., Giesy J.P. Atrazine concentrations, gonadal gross morphology and histology in ranid frogs collected in Michigan agricultural areas. Aquat. Toxicol. 2006, 76:230-245.
48. 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.
49. 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.
50. Oka T., Tooi O., Mitsui N., Miyahara M., Ohnishi Y., Takase M., Kashiwagi A., Shinkai T., Santo N., Iguchi T. Effect of atrazine on metamorphosis and sexual differentiation in Xenopus laevis. Aquat. Toxicol. 2008, 87:215-226.
51. Osmitz T.G., Lake B.G. Mode-of-action analysis for induction of rat liver tumors by pyrethrins: relevance to human cancer risk. Crit. Rev. Toxicol. 2009, 39:501-511.
52. Presnell J.K., Schiebman M.P. Humason's Animal Tissue Techniques 1997, The Johns Hopkins University Press, Baltimore & London.
53. Rohr J.R., Schotthoefer A.M., Raffel T.R., Carrick H.J., Halstead N., Hoverman J.T., Johnson C.M., Johnson L.B., Lieske C., Piwoni M.D., Schoff P.K., Beasley V.R. Agrochemicals increase trematode infections in a declining amphibian species. Nature 2008, 455:1235-1239.
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. Sherwood V., Manbodh R., Sheppard C., Chalmers A.D. RASSF7 is a member of a new family of RAS association domain-containing proteins and is required for completing mitosis. Mol. Biol. Cell. 2008, 19:1772-1782.
56. Solomon K.R., Carr J.A., Du Preez L.H., Giesy J.P., Kendall R.J., Smith E.E., Van Der Kraak G.J. Effects of atrazine on fish, amphibians, and aquatic reptiles: a critical review. Crit. Rev. Toxicol. 2008, 38:721-772.
57. 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.
58. 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.
59. Storrs S.I., Kiesecker J.M. Survivorship patterns of larval amphibians exposed to low concentrations of atrazine. Environ. Health Perspect. 2004, 112:1054-1057.
60. Stuart S.N., Chanson J.S., Cox N.A., Young B.E., Rodrigues A.S.L., Fischman D.L., Waller R.W. Status and tends of amphibian declines and extinctions worldwide. Science 2004, 306:1783-1786.
61. 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.
62. 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.
63. Tseng A., Adams D.S., Qui D., Koustubhan P., Levin M. Apoptosis is required during early stages of tail regeneration in Xenopus laevis. Devel. Biol. 2007, 301:62-69.
64. 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.
65. Zancanaro C., Merigo F., Digito M., Pelosi G. Fat body of the frog Rana esculenta: an ultrastructural study. J. Morphol. 1996, 227:321-334.
66. Zaya, R.M., Amini, Z., Whitaker, A.S., Ide, C.F., 2011. Exposure to atrazine affects the expression of key genes in metabolic pathways integral to energy homeostasis in Xenopus laevis tadpoles. Aquat. Toxicol. this issue., doi:10.1016/j.aquatox.2011.04.022.