Diazinon and diazoxon impair the ability of astrocytes to foster neurite outgrowth in primary hippocampal neurons

Toxicology and Applied Pharmacology

Volumn 274, Issue 3, 2014, Pages 372-382

  Pizzurro, Daniella M ^a   Dao, Khoi ^a   Costa, Lucio G ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF PARMA   (Italy)

Author keywords

Diazinon; Diazoxon; Glial neuronal interactions; Neurite outgrowth; Organophosphorus insecticides; Oxidative stress

Indexed keywords

ACETYLCHOLINESTERASE; ANTIOXIDANT; DIAZOXON; DIMPYLATE; FIBRONECTIN; ORGANOPHOSPHATE INSECTICIDE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL VIABILITY; ENZYME ACTIVITY; ENZYME INHIBITION; HIPPOCAMPAL NEURONAL CULTURE; NERVE FIBER GROWTH; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING;

DIAZINON; DIAZOXON; GLIAL-NEURONAL INTERACTIONS; NEURITE OUTGROWTH; ORGANOPHOSPHORUS INSECTICIDES; OXIDATIVE STRESS;

ACETYLCHOLINESTERASE; ANIMALS; ANTIOXIDANTS; ASTROCYTES; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; DIAZINON; FIBRONECTINS; HIPPOCAMPUS; INSECTICIDES; NEUROGENESIS; NEURONS; ORGANOPHOSPHORUS COMPOUNDS; OXIDATIVE STRESS; RATS;

EID: 84892448321     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.11.023     Document Type: Article

References (90)

1. ATSDR (Agency of Toxic Substances and Disease Registry) Toxicological Profile for Diazinon 2008, (Atlanta, GA).
2. Axelrad J.C., Howard C.V., McLean W.G. The effects of acute pesticide exposure on neuroblastoma cells chronically exposed to diazinon. Toxicology 2003, 185:67-78.
3. Banks C.N., Lein P.J. A review of experimental evidence linking neurotoxic organophosphorus compounds and inflammation. Neurotoxicology 2012, 33:575-584.
4. Barnham K.J., Masters C.L., Bush A.I. Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov. 2004, 3:205-214.
5. Barr D.B., Bravo R., Weerasekera G., Caltabiano L.M., Whitehead R.D., Olsson A.O., Caudill S.A., Schober S.E., Pirkle J.L., Sampson E.J., Jackson R.J., Needham L.L. Concentrations of dialkyl phosphate metabolites of organophosphorus pesticides in the US population. Environ. Health Perspect. 2004, 112:186-200.
6. Beamer P., Canales R.A., Ferguson A.C., Eskenazi B., Leckie J.O., Bradman A. Organophosphate pesticide and exposure route contribution to aggregate and cumulative dose for young farmworker children. Epidemiology 2008, 19:S264-S264.
7. Benarroch E.E. Neuron-astrocyte interactions: partnership for normal function and disease in the central nervous system. Mayo Clin. Proc. 2005, 80:1326-1338.
8. Bouchard M.F., Bellinger D.C., Wright R.O., Weisskopf M.G. Attention-deficit/hyperactivity disorder and urinary metabolites of organophosphate pesticides. Pediatrics 2010, 125:E1270-E1277.
9. Brewer G.J., Torricelli J.R., Evege E.K., Price P.J. Optimized survival of hippocampal-neurons in B27-supplemented Neurobasal™, a new serum-free medium combination. J. Neurosci. Res. 1993, 35:567-576.
10. Cardinali D.P., Pagano E.S., Bernasconi P.A.S., Reynoso R., Scacchi P. Melatonin and mitochondrial dysfunction in the central nervous system. Horm. Behav. 2013, 63:322-330.
11. Christopherson K.S., Ullian E.M., Stokes C.C.A., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005, 120:421-433.
12. Costa L.G. Current issues in organophosphate toxicology. Clin. Chim. Acta 2006, 366:1-13.
13. Crumpton T.L., Seidler F.J., Slotkin T.A. Is oxidative stress involved in the developmental neurotoxicity of chlorpyrifos?. Dev. Brain Res. 2000, 121:189-195.
14. Dickinson B.C., Chang C.J. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat. Chem. Biol. 2011, 7:504-511.
15. DiProspero N.A., Meiners S., Geller H.M. Inflammatory cytokines interact to modulate extracellular matrix and astrocytic support of neurite outgrowth. Exp. Neurol. 1997, 148:628-639.
16. Do K.Q., Cabungcal J.H., Frank A., Steullet P., Cuenod M. Redox dysregulation, neurodevelopment, and schizophrenia. Curr. Opin. Neurobiol. 2009, 19:220-230.
17. Eaton D.L., Daroff R.B., Autrup H., Bridges J., Buffler P., Costa L.G., Coyle J., McKhann G., Mobley W.C., Nadel L., Neubert D., Schulte-Hermann R., Spencer P.S. Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit. Rev. Toxicol. 2008, 38:1-125.
18. Ellman G.L., Courtney K.D., Andres V., Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 1961, 7:88-95.
19. EPA (U.S. Environmental Protection Agency) Pesticides Industry Sales and Usage: 2006-2007 Market Estimates 2011, (Washington, D.C.).
20. Eskenazi B., Marks A.R., Bradman A., Harley K., Barr D.B., Johnson C., Morga N., Jewell N.A. Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ. Health Perspect. 2007, 115:792-798.
21. Eskenazi B., Rosas L.G., Marks A.R., Bradman A., Harley K., Holland N., Johnson C., Fenster L., Barr D.B. Pesticide toxicity and the developing brain. Basic Clin. Pharmacol. 2008, 102:228-236.
22. Fenske R.A., Kedan G., Lu C., Fisker-Andersen J.A., Curl C.L. Assessment of organophosphorous pesticide exposures in the diets of preschool children in Washington State. J. Expo. Sci. Environ. Epidemiol. 2002, 12:21.
23. Flaskos J., Harris W., Sachana M., Munoz D., Tack J., Hargreaves A.J. The effects of diazinon and cypermethrin on the differentiation of neuronal and glial cell lines. Toxicol. Appl. Pharmacol. 2007, 219:172-180.
24. Frustaci A., Neri M., Cesario A., Adams J.B., Domenici E., Dalla Bernardina B., Bonassi S. Oxidative stress-related biomarkers in autism: systematic review and meta-analyses. Free Radic. Biol. Med. 2012, 52:2128-2141.
25. Genova M.L., Pich M.M., Bernacchia A., Bianchi C., Biondi A., Bovina C., Falasca A.I., Formiggini G., Castelli G.P., Lenaz G. The mitochondrial production of reactive oxygen species in relation to aging and pathology. Ann. N.Y. Acad. Sci. 2004, 1011:86-100.
26. Giordano G., White C.C., McConnachie L.A., Fernandez C., Kavanagh T.J., Costa L.G. Neurotoxicity of domoic acid in cerebellar granule neurons in a genetic model of glutathione deficiency. Mol. Pharmacol. 2006, 70:2116-2126.
27. Giordano G., Afsharinejad Z., Guizzetti M., Vitalone A., Kavanagh T.J., Costa L.G. Organophosphorus insecticides chlorpyrifos and diazinon and oxidative stress in neuronal cells in a genetic model of glutathione deficiency. Toxicol. Appl. Pharmacol. 2007, 219:181-189.
28. Giordano G., Pizzurro D., VanDeMark K., Guizzetti M., Costa L.G. Manganese inhibits the ability of astrocytes to promote neuronal differentiation. Toxicol. Appl. Pharmacol. 2009, 240:226-235.
29. Giordano G., Guizzetti M., Dao K., Mattison H.A., Costa L.G. Ethanol impairs muscarinic receptor-induced neuritogenesis in rat hippocampal slices: role of astrocytes and extracellular matrix proteins. Biochem. Pharmacol. 2011, 82:1792-1799.
30. Gris P., Tighe A., Levin D., Sharma R., Brown A. Transcriptional regulation of scar gene expression in primary astrocytes. Glia 2007, 55:1145-1155.
31. Guizzetti M., Costa L.G. Inhibition of muscarinic receptor-stimulated glial cell proliferation by ethanol. J. Neurochem. 1996, 67:2236-2245.
32. Guizzetti M., Pathak S., Giordano G., Costa L.G. Effect of organophosphates and their metabolites on astroglial cell proliferation. Toxicology 2005, 215:182-190.
33. Guizzetti M., Moore N.H., Giordano G., Costa L.G. Modulation of neuritogenesis by astrocyte muscarinic receptors. J. Biol. Chem. 2008, 283:31884-31897.
34. Guizzetti M., Moore N.H., Giordano G., VanDeMark K.L., Costa L.G. Ethanol inhibits neuritogenesis induced by astrocyte muscarinic receptors. Glia 2010, 58:1395-1406.
35. He F., Sun Y.E. Glial cells more than support cells?. Int. J. Biochem. Cell Biol. 2007, 39:661-665.
36. Howard A.S., Bucelli R., Jett D.A., Bruun D., Yang D.R., Lein P.J. Chlorpyrifos exerts opposing effects on axonal and dendritic growth in primary neuronal cultures. Toxicol. Appl. Pharmacol. 2005, 207:112-124.
37. Jafari M., Salehi M., Ahmadi S., Asgari A., Abasnezhad M., Hajigholamali M. The role of oxidative stress in diazinon-induced tissues toxicity in Wistar and Norway rats. Toxicol. Mech. Methods 2012, 22:638-647.
38. Karami-Mohajeri S., Abdollahi M. Mitochondrial dysfunction and organophosphorus compounds. Toxicol. Appl. Pharmacol. 2013, 270:39-44.
39. Kiryushko D., Berezin V., Bock E. Regulators of neurite outgrowth: role of cell adhesion molecules. Ann. N.Y. Acad. Sci. 2004, 1014:140-154.
40. Lee J.E., Park J.H., Shin I.C., Koh H.C. Reactive oxygen species regulated mitochondria-mediated apoptosis in PC12 cells exposed to chlorpyrifos. Toxicol. Appl. Pharmacol. 2012, 263:148-162.
41. Levin E., Timofeeva O., Seidler F., Slotkin T. Long-term cognitive effects of low-level developmental organophosphate pesticide exposure: divergent effects of chlorpyrifos, diazinon and parathion. Neurotoxicol. Teratol. 2008, 30:251-251.
42. Li W.F., Costa L.G., Richter R.J., Hagen T., Shih D.M., Tward A., Lusis A.J., Furlong C.E. Catalytic efficiency determines the in-vivo efficacy of PON1 for detoxifying organophosphorus compounds. Pharmacogenetics 2000, 10:767-779.
43. Lin C.C., Hsieh H.L., Shih R.H., Chi P.L., Cheng S.E., Chen J.C., Yang C.M. NADPH oxidase 2-derived reactive oxygen species signal contributes to bradykinin-induced matrix metalloproteinase-9 expression and cell migration in brain astrocytes. Cell Commun. Signal. 2012, 10.
44. Lu C., Fenske R.A., Simcox N.J., Kalman D. Pesticide exposure of children in an agricultural community: evidence of household proximity to farmland and take home exposure pathways. Environ. Res. 2000, 84:290-302.
45. Lukaszewicz-Hussain A. Role of oxidative stress in organophosphate insecticide toxicity - short review. Pesticide Biochem. Physiol. 2010, 98:145-150.
46. Mahler M., Ben-Ari Y., Represa A. Differential expression of fibronectin, tenascin-C and NCAMs in cultured hippocampal astrocytes activated by kainate, bacterial lipopolysaccharide or basic fibroblast growth factor. Brain Res. 1997, 775:63-73.
47. Martinez R., Gomes F.C.A. Neuritogenesis induced by thyroid hormone-treated astrocytes is mediated by epidermal growth factor/mitogen-activated protein kinase-phosphatidylinositol 3-kinase pathways and involves modulation of extracellular matrix proteins. J. Biol. Chem. 2002, 277:49311-49318.
48. Massicotte C., Knight K., Van Der Schyf C.J., Jortner B.S., Ehrich M. Effects of organophosphorus compounds on ATP production and mitochondrial integrity in cultured cells. Neurotox. Res. 2005, 7:203-217.
49. Matés J.M. Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 2000, 153:83-104.
50. Matthiessen H.P., Schmalenbach C., Muller H.W. Astroglia-released neurite growth-inducing activity for embryonic hippocampal neurons is associated with laminin bound in a sulfated complex and free fibronectin. Glia 1989, 2:177-188.
51. Mense S.M., Sengupta A., Lan C.G., Zhou M., Bentsman G., Volsky D.J., Whyatt R.M., Perera F.P., Zhang L. The common insecticides cyfluthrin and chlorpyrifos alter the expression of a subset of genes with diverse functions in primary human astrocytes. Toxicol. Sci. 2006, 93:125-135.
52. Montoliu C., Sanchotello M., Azorin I., Burgal M., Valles S., Renaupiqueras J., Guerri C. Ethanol increases cytochrome P4502E1 and induces oxidative stress in astrocytes. J. Neurochem. 1995, 65:2561-2570.
53. Moore N.H., Costa L.G., Shaffer S.A., Goodlett D.R., Guizzetti M. Shotgun proteomics implicates extracellular matrix proteins and protease systems in neuronal development induced by astrocyte cholinergic stimulation. J. Neurochem. 2009, 108:891-908.
54. Moser V.C., Padilla S. Age- and gender-related differences in the time course of behavioral and biochemical effects produced by oral chlorpyrifos in rats. Toxicol. Appl. Pharmacol. 1998, 149:107-119.
55. Moser V.C., Chanda S.M., Mortensen S.R., Padilla S. Age- and gender-related differences in sensitivity to chlorpyrifos in the rat reflect developmental profiles of esterase activities. Toxicol. Sci. 1998, 46:211-222.
56. Nedergaard M., Ransom B., Goldman S.A. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 2003, 26:523-530.
57. Pasinetti G.M., Nichols N.R., Tocco G., Morgan T., Laping N., Finch C.E. Transforming growth-factor-beta-1 and fibronectin messenger-RNA in rat-brain - responses to injury and cell-type localization. Neuroscience 1993, 54:893-907.
58. Peterszegi G., Dagonet F.B., Labat-Robert J., Robert L. Inhibition of cell proliferation and fibronectin biosynthesis by Na ascorbate. Eur. J. Clin. Invest. 2002, 32:372-380.
59. Pope C.N., Liu J. Age-related differences in sensitivity to organophosphorus pesticides. Environ. Toxicol. Pharmacol. 1997, 4:309-314.
60. Potashkin J.A., Meredith G.E. The role of oxidative stress in the dysregulation of gene expression and protein metabolism in neurodegenerative disease. Antioxid. Redox Signal. 2006, 8:144-151.
61. Raha S., Robinson B.H. Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem. Sci. 2000, 25:502-508.
62. Ranjbar A., Solhi H., Mashayekhi F.J., Susanabdi A., Rezaie A., Abdollahi M. Oxidative stress in acute human poisoning with organophosphorus insecticides; a case control study. Environ. Toxicol. Pharmacol. 2005, 20:88-91.
63. Rauh V., Arunajadai S., Horton M., Perera F., Hoepner L., Barr D.B., Whyatt R. 7-year neurodevelopmental scores and prenatal exposure to chlorpyrifos, a common agricultural pesticide. Environ. Health Perspect. 2011, 119:1196-1201.
64. Ren L.Q., Garrett D.K., Syapin M., Syapin P.J. Differential fibronectin expression in activated C6 glial cells treated with ethanol. Mol. Pharmacol. 2000, 58:1303-1309.
65. Rodgers K., Xiong S.Q. Effect of administration of malathion for 90days on macrophage function and mast cell, degranulation. Toxicol. Lett. 1997, 93:73-82.
66. Roegge C., Timofeva O., Seidler F., Slotkin T.A., Levin E.D. Persisting effects of early postnatal diazinon exposure on emotional reactivity in rats. Neurotoxicol. Teratol. 2006, 28:709-709.
67. Rohlman D.S., Anger W.K., Lein P.J. Correlating neurobehavioral performance with biomarkers of organophosphorous pesticide exposure. Neurotoxicology 2011, 32:268-276.
68. Samarawickrema N., Pathmeswaran A., Wickremasinghe R., Peiris-John R., Karunaratna M., Buckley N., Dawson A., de Silva J. Fetal effects of environmental exposure of pregnant women to organophosphorus compounds in a rural farming community in Sri Lanka. Clin. Toxicol. (Phila.) 2008, 46:489-495.
69. Selmi S., El-Fazaa S., Gharbi N. Oxidative stress and cholinesterase inhibition in plasma, erythrocyte and brain of rats' pups following lactational exposure to malathion. Environ. Toxicol. Pharmacol. 2012, 34:753-760.
70. Sidiropoulou E., Sachana M., Flaskos J., Harris W., Hargreaves A.J., Woldehiwet Z. Diazinon oxon affects the differentiation of mouse N2a neuroblastoma cells. Arch. Toxicol. 2009, 83:373-380.
71. Skowronska M., Zielinska M., Wojcik-Stanaszek L., Ruszkiewicz J., Milatovic D., Aschner M., Albrecht J. Ammonia increases paracellular permeability of rat brain endothelial cells by a mechanism encompassing oxidative/nitrosative stress and activation of matrix metalloproteinases. J. Neurochem. 2012, 121:125-134.
72. Slotkin T.A., Seidler F.J. Oxidative and excitatory mechanisms of developmental neurotoxicity: transcriptional profiles for chlorpyrifos, diazinon, dieldrin, and divalent nickel in PC12 cells. Environ. Health Perspect. 2009, 117:587-596.
73. Slotkin T.A., Oliver C.A., Seidler F.J. Critical periods for the role of oxidative stress in the developmental neurotoxicity of chlorpyrifos and terbutaline, alone or in combination. Dev. Brain Res. 2005, 157:172-180.
74. Slotkin T.A., Bodwell B.E., Levin E.D., Seidler F.J. Neonatal exposure to low doses of diazinon: long-term effects on neural cell development and acetylcholine systems. Environ. Health Perspect. 2008, 116:340-348.
75. Tang G.M., Rios P.G., Kuo S.H., Akman H.O., Rosoklija G., Tanji K., Dwork A., Schon E.A., DiMauro S., Goldman J., Sulzer D. Mitochondrial abnormalities in temporal lobe of autistic brain. Neurobiol. Dis. 2013, 54:349-361.
76. Thorburne S.K., Juurlink B.H. Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J. Neurochem. 1996, 67:1014-1022.
77. Timofeeva O.A., Roegge C.S., Seidler F.J., Slotkin T.A., Levin E.D. Persistent cognitive alterations in rats after early postnatal exposure to low doses of the organophosphate pesticide, diazinon. Neurotoxicol. Teratol. 2008, 30:38-45.
78. Tom V.J., Doller C.M., Malouf A.T., Silver J. Astrocyte-associated fibronectin is critical for axonal regeneration in adult white matter. J. Neurosci. 2004, 24:9282-9290.
79. Uner N., Oruc E.O., Sevgiler Y., Sahin N., Durmaz H., Usta D. Effects of diazinon on acetylcholinesterase activity and lipid peroxidation in the brain of Oreochromis niloticus. Environ. Toxicol. Pharmacol. 2006, 21:241-245.
80. Valcke M., Samuel O., Bouchard M., Dumas P., Belleville D., Tremblay C. Biological monitoring of exposure to organophosphate pesticides in children living in peri-urban areas of the Province of Quebec, Canada. Int. Arch. Occup. Environ. Health 2006, 79:568-577.
81. VanDeMark K.L., Guizzetti M., Giordano G., Costa L.G. Ethanol inhibits muscarinic receptor-induced axonal growth in rat hippocampal neurons. Alcohol. Clin. Exp. Res. 2009, 33:1945-1955.
82. Vidyasagar J., Karunakar N., Reddy M.S., Rajnarayana K., Surender T., Krishna D.R. Oxidative stress and antioxidant status in acute organophosphorous insecticide poisoning. Indian J. Pharmacol. 2004, 36:76-79.
83. Viviani B., Corsini E., Galli C.L., Marinovich M. Glia increases degeneration of hippocampal neurons through release of tumor necrosis factor-alpha. Toxicol. Appl. Pharmacol. 1998, 150:271-276.
84. Volterra A., Meldolesi J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 2005, 6:626-640.
85. Wang M.F., Lai S.C. Fibronectin degradation by MMP-2/MMP-9 in the serum of pregnant women and umbilical cord with Toxoplasma gondii infection. J. Obstet. Gynaecol. 2013, 33:370-374.
86. Watanabe K., Takahashi H., Habu Y., Kamiya-Kubushiro N., Kamiya S., Nakamura H., Yajima H., Ishii T., Katayama T., Miyazaki K., Fukai F. Interaction with heparin and matrix metalloproteinase 2 cleavage expose a cryptic anti-adhesive site of fibronectin. Biochemistry 2000, 39:7138-7144.
87. Woessner J.F. Matrix metalloproteinases and their inhibitors in connective-tissue remodeling. FASEB J. 1991, 5:2145-2154.
88. Won Y.K., Liu J., Olivier K., Zheng Q., Pope C.N. Age-related effects of chlorpyrifos on acetylcholine release in rat brain. Neurotoxicology 2001, 22:39-48.
89. Yilmaz N., Yilmaz M., Altuntas I. Diazinon-induced brain toxicity and protection by vitamins E plus C. Toxicol. Ind. Health 2012, 28:51-57.
90. Yong V.W., Power C., Forsyth P., Edwards D.R. Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci. 2001, 2:502-511.