Induction of endocannabinoid levels in juvenile rat brain following developmental chlorpyrifos exposure

Toxicological Sciences

Volumn 135, Issue 1, 2013, Pages 193-201

  Carr, Russell L ^a   Adams, Ashley L ^a   Kepler, Darin R ^a   Ward, Antonio B ^a   Ross, Matthew K ^a  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

Chlorpyrifos; Developmental; Neurotoxicity; Organophosphate; Pesticides

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ACYLGLYCEROL LIPASE; ANANDAMIDE; CHLORPYRIFOS; CHOLINESTERASE; CORN OIL; FATTY ACID AMIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; FOREBRAIN; HYDROLYSIS; MALE; NEUROTOXICITY; NONHUMAN; RAT;

CHLORPYRIFOS; DEVELOPMENTAL; NEUROTOXICITY; ORGANOPHOSPHATE.; PESTICIDES;

AGING; AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; BRAIN; CHLORPYRIFOS; CHOLINESTERASE INHIBITORS; ENDOCANNABINOIDS; FEMALE; GLYCERIDES; INSECTICIDES; MALE; MONOACYLGLYCEROL LIPASES; POLYUNSATURATED ALKAMIDES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84883170137     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft126     Document Type: Article

References (67)

1. Ahn, K., Johnson, D. S., Fitzgerald, L. R., Liimatta, M., Arendse, A., Stevenson, T., Lund, E. T., Nugent, R. A., Nomanbhoy, T. K., Alexander, J. P., et al. (2007). Novel mechanistic class of fatty acid amide hydrolase inhibitors with remarkable selectivity. Biochemistry 46, 13019-13030.
2. Aldridge, J. E., Levin, E. D., Seidler, F. J., and Slotkin, T. A. (2005a). Developmental exposure of rats to chlorpyrifos leads to behavioral alterations in adulthood, involving serotonergic mechanisms and resembling animal models of depression. Environ. Health Perspect. 113, 527-531.
3. Aldridge, J. E., Meyer, A., Seidler, F. J., and Slotkin, T. A. (2005b). Developmental exposure to terbutaline and chlorpyrifos: Pharmacotherapy of preterm labor and an environmental neurotoxicant converge on serotonergic systems in neonatal rat brain regions. Toxicol. Appl. Pharmacol. 203, 132-144.
4. Aldridge, J. E., Seidler, F. J., and Slotkin, T. A. (2004). Developmental exposure to chlorpyrifos elicits sex-selective alterations of serotonergic synaptic function in adulthood: Critical periods and regional selectivity for effects on the serotonin transporter, receptor subtypes, and cell signaling. Environ. Health Perspect. 112, 148-155.
5. Anavi-Goffer, S., and Mulder, J. (2009). The polarised life of the endocannabinoid system in CNS development. Chembiochem 10, 1591-1598.
6. Andersen, S. L. (2003). Trajectories of brain development: Point of vulnerability or window of opportunity? Neurosci. Biobehav. Rev. 27, 3-18.
7. Auman, J. T., Seidler, F. J., and Slotkin, T. A. (2000). Neonatal chlorpyrifos exposure targets multiple proteins governing the hepatic adenylyl cyclase signaling cascade: Implications for neurotoxicity. Brain Res. Dev. Brain Res. 121, 19-27.
8. Berrendero, F., Sepe, N., Ramos, J. A., Di Marzo, V., and Fernández-Ruiz, J. J. (1999). Analysis of cannabinoid receptor binding and mRNA expression and endogenous cannabinoid contents in the developing rat brain during late gestation and early postnatal period. Synapse 33, 181-191.
9. Bisogno, T., Berrendero, F., Ambrosino, G., Cebeira, M., Ramos, J. A., Fernandez-Ruiz, J. J., and Di Marzo, V. (1999). Brain regional distribution of endocannabinoids: Implications for their biosynthesis and biological function. Biochem. Biophys. Res. Commun. 256, 377-380.
10. Blankman, J. L., Simon, G. M., and Cravatt, B. F. (2007). A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem. Biol. 14, 1347-1356.
11. Bouchard, M. F., Chevrier, J., Harley, K. G., Kogut, K., Vedar, M., Calderon, N., Trujillo, C., Johnson, C., Bradman, A., Barr, D. B., et al. (2011). Prenatal exposure to organophosphate pesticides and IQ in 7-year-old children. Environ. Health Perspect. 119, 1189-1195.
12. Carr, R. L., Borazjani, A., and Ross, M. K. (2011). Effect of developmental chlorpyrifos exposure, on endocannabinoid metabolizing enzymes, in the brain of juvenile rats. Toxicol. Sci. 122, 112-120.
13. Carr, R. L., and Nail, C. A. (2008). Effect of different administration paradigms on cholinesterase inhibition following repeated chlorpyrifos exposure in late preweanling rats. Toxicol. Sci. 106, 186-192.
14. Chambers, J. E., Wiygul, S. M., Harkness, J. E., and Chambers, H. W. (1988). Effects of acute paraoxon and atropine exposures on retention of shuttle avoidance behavior in rats. Neurosci. Res. Commun. 3, 85-92.
15. Counotte, D. S., Smit, A. B., Pattij, T., and Spijker, S. (2011). Development of the motivational system during adolescence, and its sensitivity to disruption by nicotine. Dev. Cogn. Neurosci. 1, 430-443.
16. Dam, K., Garcia, S. J., Seidler, F. J., and Slotkin, T. A. (1999). Neonatal chlorpyrifos exposure alters synaptic development and neuronal activity in cholinergic and catecholaminergic pathways. Brain Res. Dev. Brain Res. 116, 9-20.
17. Dam, K., Seidler, F. J., and Slotkin, T. A. (2000). Chlorpyrifos exposure during a critical neonatal period elicits gender-selective deficits in the development of coordination skills and locomotor activity. Brain Res. Dev. Brain Res. 121, 179-187.
18. Dam, K., Seidler, F. J., and Slotkin, T. A. (2003). Transcriptional biomarkers distinguish between vulnerable periods for developmental neurotoxicity of chlorpyrifos: Implications for toxicogenomics. Brain Res. Bull. 59, 261-265.
19. Devane, W. A., Hanus, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A., and Mechoulam, R. (1992). Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946-1949.
20. Di Marzo, V., Fontana, A., Cadas, H., Schinelli, S., Cimino, G., Schwartz, J. C., and Piomelli, D. (1994). Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372, 686-691.
21. Ellman, G. L., Courtney, K. D., Andres, V., Jr, and Feather-Stone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88-95.
22. Engel, S. M., Wetmur, J., Chen, J., Zhu, C., Barr, D. B., Canfield, R. L., and Wolff, M. S. (2011). Prenatal exposure to organophosphates, paraoxonase 1, and cognitive development in childhood. Environ. Health Perspect. 119, 1182-1188.
23. Fride, E. (2008). Multiple roles for the endocannabinoid system during the earliest stages of life: Pre- and postnatal development. J. Neuroendocrinol. 20(Suppl. 1), 75-81.
24. Grube, A., Donaldson, D., Kiely, T., Wu, L. (2011). Pesticides Industry Sales and Usage, 2006 and 2007 Market Estimates, EPA 733-R-11-001. United States Environmental Protection Agency, Washington, DC.
25. Harkany, T., Keimpema, E., Barabás, K., and Mulder, J. (2008). Endocannabinoid functions controlling neuronal specification during brain development. Mol. Cell. Endocrinol. 286(1-2 Suppl. 1), S84-S90.
26. Iglewicz, B., and Hoaglin, D. (1993). How to Detect and Handle Outliers, The ASQC Basic References in Quality Control: Statistical Techniques, Vol. 16. ASQC Quality Press. Milwaukee, WI.
27. Jiang, W., Zhang, Y., Xiao, L., Van Cleemput, J., Ji, S. P., Bai, G., and Zhang, X. (2005). Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J. Clin. Invest. 115, 3104-3116.
28. Koch, D., Lu, C., Fisker-Andersen, J., Jolley, L., and Fenske, R. A. (2002). Temporal association of children's pesticide exposure and agricultural spraying: Report of a longitudinal biological monitoring study. Environ. Health Perspect. 110, 829-833.
29. Levin, E. D., Addy, N., Baruah, A., Elias, A., Christopher, N. C., Seidler, F. J., and Slotkin, T. A. (2002). Prenatal chlorpyrifos exposure in rats causes persistent behavioral alterations. Neurotoxicol. Teratol. 24, 733-741.
30. Littell, R. C., Milliken, G. A., Stroup, W. W., and Wolfinger, R. D. (1996). SAS System for Mixed Models. SAS Institute, Cary, NC.
31. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
32. Macrì, S., Ceci, C., Canese, R., and Laviola, G. (2012). Prenatal stress and peripubertal stimulation of the endocannabinoid system differentially regulate emotional responses and brain metabolism in mice. PLoS One 7, e41821.
33. Marco, E. M., Rubino, T., Adriani, W., Viveros, M. P., Parolaro, D., and Laviola, G. (2009). Long-term consequences of URB597 administration during adolescence on cannabinoid CB1 receptor binding in brain areas. Brain Res. 1257, 25-31.
34. Mechoulam, R., Ben-Shabat, S., Hanus, L., Ligumsky, M., Kaminski, N. E., Schatz, A. R., Gopher, A., Almog, S., Martin, B. R., and Compton, D. R. (1995). Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 50, 83-90.
35. Meyer, A., Seidler, F. J., Aldridge, J. E., and Slotkin, T. A. (2005). Developmental exposure to terbutaline alters cell signaling in mature rat brain regions and augments the effects of subsequent neonatal exposure to the organophosphorus insecticide chlorpyrifos. Toxicol. Appl. Pharmacol. 203, 154-166.
36. Meyer, A., Seidler, F. J., Aldridge, J. E., Tate, C. A., Cousins, M. M., and Slotkin, T. A. (2004a). Critical periods for chlorpyrifos-induced developmental neurotoxicity: Alterations in adenylyl cyclase signaling in adult rat brain regions after gestational or neonatal exposure. Environ. Health Perspect. 112, 295-301.
37. Meyer, A., Seidler, F. J., and Slotkin, T. A. (2004b). Developmental effects of chlorpyrifos extend beyond neurotoxicity: Critical periods for immediate and delayed-onset effects on cardiac and hepatic cell signaling. Environ. Health Perspect. 112, 170-178.
38. Moreira, F. A., and Lutz, B. (2008). The endocannabinoid system: Emotion, learning and addiction. Addict. Biol. 13, 196-212.
39. Morozov, Y. M., Ben-Ari, Y., and Freund, T. F. (2004). The spatial and temporal pattern of fatty acid amide hydrolase expression in rat hippocampus during postnatal development. Eur. J. Neurosci. 20, 459-466.
40. Nomura, D. K., Blankman, J. L., Simon, G. M., Fujioka, K., Issa, R. S., Ward, A. M., Cravatt, B. F., and Casida, J. E. (2008). Activation of the endocannabinoid system by organophosphorus nerve agents. Nat. Chem. Biol. 4, 373-378.
41. Nomura, D. K., and Casida, J. E. (2011). Activity-based protein profiling of organophosphorus and thiocarbamate pesticides reveals multiple serine hydrolase targets in mouse brain. J. Agric. Food Chem. 59, 2808-2815.
42. O'Shea, M., McGregor, I. S., and Mallet, P. E. (2006). Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar longlasting deficits in object recognition and reduced social interaction in rats. J. Psychopharmacol. 20, 611-621.
43. Pope, C. N., Chakraborti, T. K., Chapman, M. L., Farrar, J. D., and Arthun, D. (1991). Comparison of in vivo cholinesterase inhibition in neonatal and adult rats by three organophosphorothioate insecticides. Toxicology 68, 51-61.
44. Quistad, G. B., Klintenberg, R., Caboni, P., Liang, S. N., and Casida, J. E. (2006). Monoacylglycerol lipase inhibition by organophosphorus compounds leads to elevation of brain 2-arachidonoylglycerol and the associated hypomotility in mice. Toxicol. Appl. Pharmacol. 211, 78-83.
45. Quistad, G. B., Sparks, S. E., and Casida, J. E. (2001). Fatty acid amide hydrolase inhibition by neurotoxic organophosphorus pesticides. Toxicol. Appl. Pharmacol. 173, 48-55.
46. Quistad, G. B., Sparks, S. E., Segall, Y., Nomura, D. K., and Casida, J. E. (2002). Selective inhibitors of fatty acid amide hydrolase relative to neuropathy target esterase and acetylcholinesterase: Toxicological implications. Toxicol. Appl. Pharmacol. 179, 57-63.
47. Rauh, V., Arunajadai, S., Horton, M., Perera, F., Hoepner, L., Barr, D. B., and Whyatt, R. (2011). Seven-year neurodevelopmental scores and prenatal exposure to chlorpyrifos, a common agricultural pesticide. Environ. Health Perspect. 119, 1196-1201.
48. Rauh, V. A., Garfinkel, R., Perera, F. P., Andrews, H. F., Hoepner, L., Barr, D. B., Whitehead, R., Tang, D., and Whyatt, R. W. (2006). Impact of prenatal chlorpyrifos exposure on neurodevelopment in the first 3 years of life among inner-city children. Pediatrics 118, e1845-e1859.
49. Rauh, V. A., Perera, F. P., Horton, M. K., Whyatt, R. M., Bansal, R., Hao, X., Liu, J., Barr, D. B., Slotkin, T. A., and Peterson, B. S. (2012). Brain anomalies in children exposed prenatally to a common organophosphate pesticide. Proc. Natl. Acad. Sci. U. S. A. 109, 7871-7876.
50. 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 sexspecific behaviors at adulthood in mice. Toxicol. Sci. 93, 105-113.
51. Roegge, C. S., Timofeeva, O. A., Seidler, F. J., Slotkin, T. A., and Levin, E. D. (2008). Developmental diazinon neurotoxicity in rats: Later effects on emotional response. Brain Res. Bull. 75, 166-172.
52. Ruckart, P. Z., Kakolewski, K., Bove, F. J., and Kaye, W. E. (2004). Long-term neurobehavioral health effects of methyl parathion exposure in children in Mississippi and Ohio. Environ. Health Perspect. 112, 46-51.
53. SAS Institute. (2009). SAS/STAT User's Guide, Version 9.2. SAS Publishing, Cary, NC.
54. Slotkin, T. A., and Seidler, F. J. (2007). Developmental exposure to terbutaline and chlorpyrifos, separately or sequentially, elicits presynaptic serotonergic hyperactivity in juvenile and adolescent rats. Brain Res. Bull. 73, 301-309.
55. Slotkin, T. A., Seidler, F. J., and Fumagalli, F. (2007). Exposure to organophosphates reduces the expression of neurotrophic factors in neonatal rat brain regions: Similarities and differences in the effects of chlorpyrifos and diazinon on the fibroblast growth factor superfamily. Environ. Health Perspect. 115, 909-916.
56. Slotkin, T. A., Tate, C. A., Ryde, I. T., Levin, E. D., and Seidler, F. J. (2006). Organophosphate insecticides target the serotonergic system in developing rat brain regions: Disparate effects of diazinon and parathion at doses spanning the threshold for cholinesterase inhibition. Environ. Health Perspect. 114, 1542-1546.
57. Stella, N., Schweitzer, P., and Piomelli, D. (1997). A second endogenous cannabinoid that modulates long-term potentiation. Nature 388, 773-778.
58. Sugiura, T., Kondo, S., Sukagawa, A., Nakane, S., Shinoda, A., Itoh, K., Yamashita, A., and Waku, K. (1995). 2-Arachidonoylglycerol: A possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun. 215, 89-97.
59. Taber, K. H., and Hurley, R. A. (2009). Endocannabinoids: Stress, anxiety, and fear. J. Neuropsychiatry Clin. Neurosci. 21, 109-113.
60. Tau, G. Z., and Peterson, B. S. (2010). Normal development of brain circuits. Neuropsychopharmacology 35, 147-168.
61. Timofeeva, O. A., Roegge, C. S., Seidler, F. J., Slotkin, T. A., and Levin, E. D. (2008a). Persistent cognitive alterations in rats after early postnatal exposure to low doses of the organophosphate pesticide, diazinon. Neurotoxicol. Teratol. 30, 38-45.
62. Timofeeva, O. A., Sanders, D., Seemann, K., Yang, L., Hermanson, D., Regenbogen, S., Agoos, S., Kallepalli, A., Rastogi, A., Braddy, D., et al. (2008b). Persistent behavioral alterations in rats neonatally exposed to low doses of the organophosphate pesticide, parathion. Brain Res. Bull. 77, 404-411.
63. Venerosi, A., Cutuli, D., Colonnello, V., Cardona, D., Ricceri, L., and Calamandrei, G. (2008). Neonatal exposure to chlorpyrifos affects maternal responses and maternal aggression of female mice in adulthood. Neurotoxicol. Teratol. 30, 468-474.
64. Venerosi, A., Ricceri, L., Rungi, A., Sanghez, V., and Calamandrei, G. (2010). Gestational exposure to the organophosphate chlorpyrifos alters socialemotional behaviour and impairs responsiveness to the serotonin transporter inhibitor fluvoxamine in mice. Psychopharmacology (Berl). 208, 99-107.
65. Wyffels, L., Muccioli, G. G., Kapanda, C. N., Labar, G., De Bruyne, S., De Vos, F., and Lambert, D. M. (2010). PET imaging of fatty acid amide hydrolase in the brain: Synthesis and biological evaluation of an 11C-labelled URB597 analogue. Nucl. Med. Biol. 37, 665-675.
66. Xie, S., Borazjani, A., Hatfield, M. J., Edwards, C. C., Potter, P. M., and Ross, M. K. (2010). Inactivation of lipid glyceryl ester metabolism in human THP1 monocytes/macrophages by activated organophosphorus insecticides: Role of carboxylesterases 1 and 2. Chem. Res. Toxicol. 23, 1890-1904.
67. Zheng, Q., Olivier, K., Won, Y. K., and Pope, C. N. (2000). Comparative cholinergic neurotoxicity of oral chlorpyrifos exposures in preweanling and adult rats. Toxicol. Sci. 55, 124-132.