Gestational and lactational exposure to atrazine via the drinking water causes specific behavioral deficits and selectively alters monoaminergic systems in C57BL/6 Mouse Dams, juvenile and adult offspring

Toxicological Sciences

Volumn 141, Issue 1, 2014, Pages 90-102

  Lin, Zhoumeng ^a,b,c   Dodd, Celia A ^a,b,d   Xiao, Shuo ^a,b,e   Krishna, Saritha ^a   Ye, Xiaoqin ^a,b   Filipov, Nikolay M ^a,b  

^a Anatomic Pathology Service Department of Veterinary Pathobiology College of Veterinary   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

^d FORT VALLEY STATE UNIVERSITY   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Atrazine; Behavior; Developmental neurotoxicity; Dopamine; Pesticides

Indexed keywords

ATRAZINE; DOPAMINE; DRINKING WATER; SEROTONIN; WATER POLLUTANT;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR CHANGE; BEHAVIOR DISORDER; BODY WEIGHT; BRAIN WEIGHT; C57BL 6 MOUSE; CONTROLLED STUDY; EXPERIMENTAL BEHAVIORAL TEST; EXPERIMENTAL HYPERACTIVITY; FEMALE; FORCED SWIM TEST; GESTATIONAL AGE; GRIP STRENGTH TEST; HOMEOSTASIS; JUVENILE; LACTATION; MALE; MARBLE BURYING TEST; MARE; MENTAL PERFORMANCE; MONOAMINERGIC SYSTEM; MOTOR PERFORMANCE; MOUSE; NEUROTOXICITY; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; OPEN FIELD TEST; PERIRHINAL CORTEX; PREGNANCY; PROGENY; SWIMMING; WEIGHT GAIN; AGING; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; CORPUS STRIATUM; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PRENATAL EXPOSURE; PSYCHOLOGY; SEXUAL DEVELOPMENT; TOXICITY; WATER POLLUTANT;

AGING; ANIMALS; ATRAZINE; BEHAVIOR, ANIMAL; CORPUS STRIATUM; DOPAMINE; DRINKING WATER; FEMALE; GESTATIONAL AGE; LACTATION; MALE; MICE, INBRED C57BL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEX CHARACTERISTICS; WATER POLLUTANTS, CHEMICAL;

EID: 84912103131     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu107     Document Type: Article

References (49)

1. Antunes, M. and Biala, G. (2012). The novel object recognition memory: Neurobiology, test procedure, and its modifications. Cogn. Process 13, 93-110.
2. ATSDR (2003) Potential for human exposure. InToxicological Profile for Atrazine, pp. 129-160. Agency for Toxic Substances and Disease Registry, Atlanta.
3. Balduini, L., Matoga, M., Cavalli, E., Seilles, E., Riethmuller, D., Thomassin, M. and Guillaume, Y. C. (2003). Triazinic herbicide determination by gas chromatography-mass spectrometry in breastmilk. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 794, 389-395.
4. Bardullas, U., Giordano, M. and Rodriguez, V. M. (2011). Chronic atrazine exposure causes disruption of the spontaneous locomotor activity and alters the striatal dopaminergic system of the male Sprague-Dawley rat. Neurotoxicol. Teratol. 33, 263- 272.
5. Belloni, V., Dessi-Fulgheri, F., Zaccaroni, M., Di Consiglio, E., De Angelis, G., Testai, E., Santochirico, M., Alleva, E. and Santucci, D. (2011). Early exposure to low doses of atrazine affects behavior in juvenile and adult CD1 mice. Toxicology 279, 19-26.
6. Chevrier, C., Limon, G., Monfort, C., Rouget, F., Garlantezec, R., Petit, C., Durand, G. and Cordier, S. (2011). Urinary biomarkers of prenatal atrazine exposure and adverse birth outcomes in the PELAGIE birth cohort. Environ. Health Perspect. 119, 1034-1041.
7. Coban, A. and Filipov, N.M. (2007). Dopaminergic toxicity associated with oral exposure to the herbicide atrazine in juvenile male C57BL/6 mice. J. Neurochem. 100, 1177-1187.
8. Cooper, R. L., Stoker, T. E., Goldman, J. M., Parrish,M. B. and Tyrey, L. (1996). Effect of atrazine on ovarian function in the rat. Reprod. Toxicol. 10, 257-264.
9. Curwin, B. D., Hein, M. J., Sanderson, W. T., Striley, C., Heederik, D., Kromhout, H., Reynolds, S. J. and Alavanja, M. C. (2007). Urinary pesticide concentrations among children, mothers and fathers living in farm and non-farm households in iowa. Ann. Occup. Hyg. 51, 53-65.
10. Dooley, G. P., Ashley, A. K., Legare, M. E., Handa, R. J. and Hanneman, W. H. (2010). Proteomic analysis of diaminochlorotriazine (DACT) adducts in three brain regions ofWistar rats. Toxicol. Lett. 199, 17-21.
11. Dyet, L. E., Kennea, N., Counsell, S. J., Maalouf, E. F., Ajayi-Obe, M., Duggan, P. J., Harrison, M., Allsop, J. M., Hajnal, J., Herlihy, A. H., et al. (2006). Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 118, 536-548.
12. EPA (2003) Interim Reregistration Eligibility Decision for Atrazine, Case No. 0062. pp. 15-52. U.S. Environmental Protection Agency, Washington, DC. Available at: http://www.epa.gov/oppsrrd1/REDs/atrazineired.pdf.
13. Fakhouri, W. D., Nunez, J. L. and Trail, F. (2010). Atrazine binds to the growth hormone-releasing hormone receptor and affects growth hormone gene expression. Environ. Health Perspect. 118, 1400-1405.
14. Fraites, M. J., Narotsky, M. G., Best, D. S., Stoker, T. E., Davis, L. K., Goldman, J. M., Hotchkiss, M. G., Klinefelter, G. R., Kamel, A., Qian, Y., et al. (2011). Gestational atrazine exposure: effects on male reproductive development and metabolite distribution in the dam, fetus, and neonate. Reprod. Toxicol. 32, 52-63.
15. Friedmann, A. S. (2002). Atrazine inhibition of testosterone production in rat males following peripubertal exposure. Reprod. Toxicol. 16, 275-279.
16. Frye, C. A. and Walf, A. A. (2009). Depression-like behavior of aged male and female mice is ameliorated with administration of testosterone or its metabolites. Physiol. Behav. 97, 266- 269.
17. Giusi, G., Facciolo, R. M., Canonaco, M., Alleva, E., Belloni, V., Dessi'-Fulgheri, F. and Santucci, D. (2006). The endocrine disruptor atrazine accounts for a dimorphic somatostatinergic neuronal expression pattern in mice. Toxicol. Sci. 89, 257-264.
18. Glajch, K. E., Fleming, S. M., Surmeier, D. J. and Osten, P. (2012). Sensorimotor assessment of the unilateral 6- hydroxydopamine mouse model of Parkinson's disease. Behav. Brain Res. 230, 309-316.
19. Kobayashi, T., Hayashi, E., Shimamura, M., Kinoshita, M. and Murphy, N. P. (2008). Neurochemical responses to antidepressants in the prefrontal cortex of mice and their efficacy in preclinical models of anxiety-like and depression-like behavior: A comparative and correlational study. Psychopharmacology (Berl.) 197, 567-580.
20. Lang, D., Criegee, D., Grothusen, A., Saalfrank, R. W. and Bocker, R. H. (1996). In vitro metabolism of atrazine, terbuthylazine, ametryne, and terbutryne in rats, pigs, and humans. Drug Metab. Dispos. 24, 859-865.
21. Lin, Z., Dodd, C. A. and Filipov, N. M. (2013a). Differentiation state-dependent effects of in vitro exposure to atrazine or its metabolite diaminochlorotriazine in a dopaminergic cell line. Life Sci. 92, 81-90.
22. Lin, Z., Dodd, C. A. and Filipov, N.M. (2013b). Short-term atrazine exposure causes behavioral deficits and disruptsmonoaminergic systems in male C57BL/6mice. Neurotoxicol. Teratol. 39C, 26-35.
23. Lin, Z., Fisher, J.W., Ross, M. K. and Filipov, N. M. (2011). A physiologically based pharmacokinetic model for atrazine and its main metabolites in the adult male C57BL/6 mouse. Toxicol. Appl. Pharmacol. 251, 16-31.
24. Lin, Z., Fisher, J. W., Wang, R., Ross, M. K. and Filipov, N. M. (2013c). Estimation of placental and lactational transfer and tissue distribution of atrazine and its main metabolites in rodent dams, fetuses, and neonates with physiologically based pharmacokinetic modeling. Toxicol. Appl. Pharmacol. 273, 140- 158.
25. Malkova, N. V., Yu, C. Z., Hsiao, E. Y., Moore, M. J. and Patterson, P. H. (2012).Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav. Immun. 26, 607-616.
26. Matsuura, K., Kabuto, H., Makino, H. and Ogawa, N. (1997). Pole test is a useful method for evaluating the mouse movement disorder caused by striatal dopamine depletion. J. Neurosci. Methods 73, 45-48.
27. Miller, G., Neilan, M., Chia, R., Gheryani, N., Holt, N., Charbit, A., Wells, S., Tucci, V., Lalanne, Z., Denny, P., et al. (2010). ENUmutagenesis reveals a novel phenotype of reduced limb strength in mice lacking fibrillin 2. PLoS One 5, e9137.
28. Mosquin, P., Whitmore, R. W. and Chen, W. (2012). Estimation of upper centile concentrations using historical atrazine monitoring data from community water systems. J. Environ. Qual. 41, 834-844.
29. Negishi, T., Matsunaga, Y., Kobayashi, Y., Hirano, S. and Tashiro, T. (2013) Developmental subchronic exposure to diphenylarsinic acid induced increased exploratory behavior, impaired learning behavior, and decreased cerebellar glutathione concentration in rats. Toxicol. Sci., 136, 478-486.
30. Nelson, A. J., Thur, K. E.,Marsden, C. A. and Cassaday, H. J. (2010). Dissociable roles of dopamine within the core and medial shell of the nucleus accumbens in memory for objects and place. Behav. Neurosci. 124, 789-799.
31. Ochoa-Acuña, H., Frankenberger, J., Hahn, L. and Carbajo, C. (2009). Drinking-water herbicide exposure in Indiana and prevalence of small-for-gestational-age and preterm delivery. Environ. Health Perspect. 117, 1619-1624.
32. OECD (2007) Organization for Economic Cooperation and Development (OECD), Guidelines for the Testing of Chemicals. Test No. 426: Developmental Neurotoxicity Study. OECD Environment Directorate, Paris, France.
33. Onishchenko, N., Tamm, C., Vahter, M., Hokfelt, T., Johnson, J. A., Johnson, D. A. and Ceccatelli, S. (2007). Developmental exposure to methylmercury alters learning and induces depression-like behavior in male mice. Toxicol. Sci. 97, 428- 437.
34. Palanza, P. (2001). Animal models of anxiety and depression: How are females different? Neurosci. Biobehav. Rev. 25, 219- 233.
35. Peterson, B. S., Vohr, B., Staib, L. H., Cannistraci, C. J., Dolberg, A., Schneider, K. C., Katz, K. H., Westerveld, M., Sparrow, S., Anderson, A. W., et al. (2000). Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 284, 1939-1947.
36. Petit-Demouliere, B., Chenu, F. and Bourin, M. (2005). Forced swimming test in mice: A review of antidepressant activity. Psychopharmacology (Berl.) 177, 245-255.
37. Prakash, N. andWurst,W. (2006). Development of dopaminergic neurons in the mammalian brain. Cell. Mol. Life Sci. 63, 187- 206.
38. Preston, A. R. and Eichenbaum, H. (2013). Interplay of hippocampus and prefrontal cortex in memory. Curr. Biol. 23, R764- R773.
39. Rayner, J. L.,Wood, C. and Fenton, S. E. (2004). Exposure parameters necessary for delayed puberty and mammary gland development in Long-Evans rats exposed in utero to atrazine. Toxicol. Appl. Pharmacol. 195, 23-34.
40. Ressler, K. J. and Nemeroff, C. B. (2000). Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress. Anxiety 12(Suppl. 1), 2-19.
41. Ricceri, L., Venerosi, A., Capone, F., Cometa, M. F., Lorenzini, P., Fortuna, S. and Calamandrei, G. (2006). Developmental neurotoxicity of organophosphorous pesticides: fetal and neonatal exposure to chlorpyrifos alters sex-specific behaviors at adulthood in mice. Toxicol. Sci. 93, 105-113.
42. Rice, D. and Barone, S., Jr. (2000). Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environ. Health Perspect. 108(Suppl. 3), 511-533.
43. Rodriguez, V. M., Limon-Pacheco, J. H., Mendoza-Trejo, M. S., Gonzalez-Gallardo, A., Hernandez-Plata, I. and Giordano, M. (2013). Repeated exposure to the herbicide atrazine alters locomotor activity and the nigrostriatal dopaminergic system of the albino rat. Neurotoxicology 34, 82-94.
44. Schultz,W. (2007).Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259-288.
45. Sik, A., van Nieuwehuyzen, P., Prickaerts, J. and Blokland, A. (2003). Performance of different mouse strains in an object recognition task. Behav. Brain Res. 147, 49-54.
46. Sisk, C. L. and Zehr, J. L. (2005). Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 26, 163- 174.
47. Tattoli, M., Cagiano, R., Gaetani, S., Ghiglieri, V., Giustino, A., Mereu, G., Trabace, L. and Cuomo, V. (2001). Neurofunctional effects of developmental alcohol exposure in alcoholpreferring and alcohol-nonpreferring rats. Neuropsychopharmacology 24, 691-705.
48. Volpe, J. J. (2009). Brain injury in premature infants: A complex amalgam of destructive and developmental disturbances. Lancet Neurol. 8, 110-124.
49. Whyatt, R. M., Barr, D. B., Camann, D. E., Kinney, P. L., Barr, J. R., Andrews, H. F., Hoepner, L. A., Garfinkel, R., Hazi, Y., Reyes, A., et al. (2003). Contemporary-use pesticides in personal air samples during pregnancy and blood samples at delivery among urban minority mothers and newborns. Environ. Health Perspect. 111, 749-756.