Transcriptional profiles for glutamate transporters reveal differences between organophosphates but similarities with unrelated neurotoxicants

Brain Research Bulletin

Volumn 83, Issue 1-2, 2010, Pages 76-83

  Slotkin, Theodore A ^a   Lobner, Doug ^b   Seidler, Frederic J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b MARQUETTE UNIVERSITY   (United States)

Author keywords

Chlorpyrifos; Diazinon; Dieldrin; Gene transcription patterns; Glutamate transporters; Microarrays; Nickel; Organochlorine insecticides; Organophosphate insecticides; PC12 cells

Indexed keywords

CHLORPYRIFOS; CHOLINESTERASE INHIBITOR; CYSTINE; DIELDRIN; DIMPYLATE; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; NERVE GROWTH FACTOR; NICKEL; ORGANOCHLORINE PESTICIDE; ORGANOPHOSPHATE;

ANIMAL CELL; ARTICLE; CELL STRAIN; CONTROLLED STUDY; EXCITOTOXICITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; NERVE CELL DIFFERENTIATION; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; UPREGULATION;

AMINO ACID TRANSPORT SYSTEM X-AG; ANALYSIS OF VARIANCE; ANIMALS; CELL DIFFERENTIATION; CHLORPYRIFOS; CHOLINESTERASE INHIBITORS; CYSTINE; DIAZINON; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLUTAMIC ACID; MAXIMUM TOLERATED DOSE; NERVE GROWTH FACTOR; NEUROTOXINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PC12 CELLS; PHOSPHORIC ACID ESTERS; RATS; STATISTICS AS TOPIC; TIME FACTORS;

EID: 77955662870     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2010.06.010     Document Type: Article

References (68)

1. Adachi M., Koyama H., Long Z., Sekine M., Furuchi T., Imai K., Nimura N., Shimamoto K., Nakajima T., Homma H. l-Glutamate in the extracellular space regulates endogenous d-aspartate homeostasis in rat pheochromocytoma MPT1 cells. Arch. Biochem. Biophys. 2004, 424:89-96.
2. Adigun A.A., Seidler F.J., Slotkin T.A. Disparate developmental neurotoxicants converge on the cyclic AMP signaling cascade, revealed by transcriptional profiles in vitro and in vivo. Brain Res. 2010, 1316:1-16.
3. Bagchi D., Bagchi M., Hassoun E.A., Stohs S.J. In vitro and in vivo generation of reactive oxygen species, DNA damage and lactate dehydrogenase leakage by selected pesticides. Toxicology 1995, 104:129-140.
4. Bagchi D., Bhattacharya G., Stohs S.J. In vitro and in vivo induction of heat shock (stress) protein (Hsp) gene expression by selected pesticides. Toxicology 1996, 112:57-68.
5. Benters J., Schafer T., Beyersmann D., Hechtenberg S. Agonist-stimulated calcium transients in PC12 cells are affected differentially by cadmium and nickel. Cell Calcium 1996, 20:441-446.
6. Beseler C.L., Stallones L., Hoppin J.A., Alavanja M.C.R., Blair A., Keefe T., Kamel F. Depression and pesticide exposures among private pesticide applicators enrolled in the Agricultural Health Study. Environ. Health Perspect. 2008, 116:1713-1719.
7. 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.
8. Brannen K.C., Devaud L.L., Liu J.P., Lauder J.M. Prenatal exposure to neurotoxicants dieldrin or lindane alters tert-butylbicyclophosphorothionate binding to GABA(A) receptors in fetal rat brainstem. Dev. Neurosci. 1998, 20:34-41.
9. Casey C.E., Robinson M.F. Copper, manganese, zinc, nickel, cadmium and lead in human foetal tissues. Br. J. Nutr. 1978, 39:639-646.
10. Casida J.E., Quistad G.B. Organophosphate toxicology: safety aspects of nonacetylcholinesterase secondary targets. Chem. Res. Toxicol. 2004, 17:983-998.
11. Colborn T. A case for revisiting the safety of pesticides: a closer look at neurodevelopment. Environ. Health Perspect. 2006, 114:10-17.
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. Developmental neurotoxicity of chlorpyrifos in vivo and in vitro: effects on nuclear transcription factor involved in cell replication and differentiation. Brain Res. 2000, 857:87-98.
14. 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.
15. Das K.P., Barone S. Neuronal differentiation in PC12 cells is inhibited by chlorpyrifos and its metabolites: is acetylcholinesterase inhibition the site of action? Toxicol. Appl. Pharmacol. 1999, 160:217-230.
16. 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(Suppl. 2):1-125.
17. Faber J.J., Anderson D.F., Morton M.J., Parks C.M., Pinson C.W., Thornburg K.L., Willis D.M. Birth, its physiology, and the problems it creates. The Physiological Development of the Fetus and Newborn 1985, 371-380. Academic Press, London. C.T. Jones, P.W. Nathanielsz (Eds.).
18. Flaskos J., McLean W.G., Hargreaves A.J. The toxicity of organophosphate compounds towards cultured PC12 cells. Toxicol. Lett. 1994, 70:71-76.
19. Fremeau R.T., Burman J., Qureshi T., Tran C.H., Proctor J., Johnson J., Zhang H., Sulzer D., Copenhagen D.R., Storm-Mathisen J., Reimer R.J., Chaudhry F.A., Edwards R.H. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc. Natl. Acad. Sci. 2002, 99:14488-144893.
20. Fujita K., Lazarovici P., Guroff G. Regulation of the differentiation of PC12 pheochromocytoma cells. Environ. Health Perspect. 1989, 80:127-142.
21. 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.
22. Gupta R.C. Brain regional heterogeneity and toxicological mechanisms of organophosphates and carbamates. Toxicol. Mech. Methods 2004, 14:103-143.
23. Jacobsen N., Alfheim I., Jonsen J. Nickel and strontium distribution in some mouse tissues. Passage through placenta and mammary glands. Res. Commun. Chem. Pathol. Pharmacol. 1978, 20:571-584.
24. Jaga K., Dharmani C. The interrelation between organophosphate toxicity and the epidemiology of depression and suicide. Rev. Environ. Health 2007, 22:57-73.
25. Jameson R.R., Seidler F.J., Qiao D., Slotkin T.A. Chlorpyrifos affects phenotypic outcomes in a model of mammalian neurodevelopment: critical stages targeting differentiation in PC12 cells. Environ. Health Perspect. 2006, 114:667-672.
26. Jameson R.R., Seidler F.J., Slotkin T.A. Nonenzymatic functions of acetylcholinesterase splice variants in the developmental neurotoxicity of organophosphates: chlorpyrifos, chlorpyrifos oxon and diazinon. Environ. Health Perspect. 2007, 115:65-70.
27. Kiryu-Seo S., Gamo K., Tachibana T., Tanaka K., Kiyama H. Unique anti-apoptotic activity of EAAC1 in injured motor neurons. EMBO J. 2006, 25:3411-3421.
28. Kitazawa M., Anantharam V., Kanthasamy A.G. Dieldrin-induced oxidative stress and neurochemical changes contribute to apoptopic cell death in dopaminergic cells. Free Radical Biol. Med. 2001, 31:1473-1485.
29. Kitazawa M., Anantharam V., Kanthasamy A.G. Dieldrin induces apoptosis by promoting caspase-3-dependent proteolytic cleavage of protein kinase Cδ in dopaminergic cells: relevance to oxidative stress and dopaminergic degeneration. Neuroscience 2003, 119:945-964.
30. Kobayashi S., Millhorn D.E. Hypoxia regulates glutamate metabolism and membrane transport in rat PC12 cells. J. Neurochem. 2001, 76:1935-1948.
31. Koyama H., Sekine M., Furuchi T., Katane M., Nimura N., Shimamoto K., Nakajima T., Homma H. A novel l-glutamate transporter inhibitor reveals endogenous d-aspartate homeostasis in rat pheochromocytoma MPT1 cells. Life Sci. 2005, 76:2933-2944.
32. Lagercrantz H., Slotkin T.A. The " stress" of being born. Sci. Am. 1986, 254(April):100-107.
33. Li W.W., Casida J.E. Organophosphorus neuropathy target esterase inhibitors selectively block outgrowth of neurite-like and cell processes in cultured cells. Toxicol. Lett. 1998, 98:139-146.
34. Liu J.P., Brannen K.C., Grayson D.R., Morrow A.L., Devaud L.L., Lauder J.M. Prenatal exposure to the pesticide dieldrin or the GABA(A) receptor antagonist bicuculline differentially alters expression of GABA(A) receptor subunit mRNAs in fetal rat brainstem. Dev. Neurosci. 1998, 20:83-92.
35. Mauro R.E., Zhang L. Unique insights into the actions of CNS agents: lessons from studies of chlorpyrifos and other common pesticides. CNS Agents Med. Chem. 2007, 7:183-199.
36. Mileson B.E., Chambers J.E., Chen W.L., Dettbarn W., Ehrich M., Eldefrawi A.T., Gaylor D.W., Hamernik K., Hodgson E., Karczmar A.G., Padilla S., Pope C.N., Richardson R.J., Saunders D.R., Sheets L.P., Sultatos L.G., Wallace K.B. Common mechanism of toxicity: a case study of organophosphorus pesticides. Toxicol. Sci. 1998, 41:8-20.
37. Nagata K., Huang C.S., Song J.H., Narahashi T. Direct actions of anticholinesterases on the neuronal nicotinic acetylcholine receptor channels. Brain Res. 1997, 769:211-218.
38. Ogawa Y., Saito Y., Nishio K., Yoshida Y., Ashida H., Niki E. Gamma-tocopheryl quinone, not alpha-tocopheryl quinone, induces adaptive response through up-regulation of cellular glutathione and cysteine availability via activation of ATF4. Free Radical Res. 2008, 42:674-687.
39. Qiao D., Seidler F.J., Slotkin T.A. Developmental neurotoxicity of chlorpyrifos modeled in vitro: comparative effects of metabolites and other cholinesterase inhibitors on DNA synthesis in PC12 and C6 cells. Environ. Health Perspect. 2001, 109:909-913.
40. Qiao D., Seidler F.J., Slotkin T.A. Oxidative mechanisms contributing to the developmental neurotoxicity of nicotine and chlorpyrifos. Toxicol. Appl. Pharmacol. 2005, 206:17-26.
41. Qiao D., Seidler F.J., Violin J.D., Slotkin T.A. Nicotine is a developmental neurotoxicant and neuroprotectant: stage-selective inhibition of DNA synthesis coincident with shielding from effects of chlorpyrifos. Dev. Brain Res. 2003, 147:183-190.
42. Rauh V.A., Garfinkel R., Perera R., Andrews H., Hoepner L., Barr D., Whitehead D., Tang D., Whyatt R.M. Impact of prenatal chlorpyrifos exposure on neurodevelopment in the first 3 years of life among inner-city children. Pediatrics 2006, 118:1845-1859.
43. Roegge C.S., Timofeeva O.A., Seidler F.J., Slotkin T.A., Levin E.D. Developmental diazinon neurotoxicity in rats: later effects on emotional response. Brain Res. Bull. 2008, 75:166-172.
44. Rush T., Liu X.Q., Hjelmhaug J., Lobner D. Mechanisms of chlorpyrifos and diazinon induced neurotoxicity in cortical culture. Neuroscience 2010, 166:899-906.
45. Slotkin T.A. Developmental cholinotoxicants: nicotine and chlorpyrifos. Environ. Health Perspect. 1999, 107(Suppl. 1):71-80.
46. Slotkin T.A. Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. Toxicol. Appl. Pharmacol. 2004, 198:132-151.
47. Slotkin T.A. Developmental neurotoxicity of organophosphates: a case study of chlorpyrifos. Toxicity of Organophosphate and Carbamate Pesticides 2005, 293-314. Elsevier Academic Press, San Diego. R.C. Gupta (Ed.).
48. 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.
49. Slotkin T.A., MacKillop E.A., Ryde I.T., Seidler F.J. Ameliorating the developmental neurotoxicity of chlorpyrifos: a mechanisms-based approach in PC12 cells. Environ. Health Perspect. 2007, 115:1306-1313.
50. Slotkin T.A., MacKillop E.A., Ryde I.T., Tate C.A., Seidler F.J. Screening for developmental neurotoxicity using PC12 cells: comparisons of organophosphates with a carbamate, an organochlorine and divalent nickel. Environ. Health Perspect. 2007, 115:93-101.
51. Slotkin T.A., Ryde I.T., Levin E.D., Seidler F.J. Developmental neurotoxicity of low-dose diazinon exposure of neonatal rats: effects on serotonin systems in adolescence and adulthood. Brain Res. Bull. 2008, 75:640-647.
52. Slotkin T.A., Seidler F.J. Comparative developmental neurotoxicity of organophosphates in vivo: transcriptional responses of pathways for brain cell development, cell signaling, cytotoxicity and neurotransmitter systems. Brain Res. Bull. 2007, 72:232-274.
53. Slotkin T.A., Seidler F.J. Developmental neurotoxicants target neurodifferentiation into the serotonin phenotype: chlorpyrifos, diazinon, dieldrin and divalent nickel. Toxicol. Appl. Pharmacol. 2008, 233:211-219.
54. 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.
55. Slotkin T.A., Seidler F.J. Protein kinase C is a target for diverse developmental neurotoxicants: transcriptional responses to chlorpyrifos, diazinon, dieldrin and divalent nickel in PC12 cells. Brain Res. 2009, 1263:23-32.
56. Slotkin T.A., Seidler F.J. Transcriptional profiles reveal similarities and differences in the effects of developmental neurotoxicants on differentiation into neurotransmitter phenotypes in PC12 cells. Brain Res. Bull. 2009, 78:211-225.
57. Slotkin T.A., Seidler F.J. Oxidative stress from diverse developmental neurotoxicants: antioxidants protect against lipid peroxidation without preventing cell loss. Neurotoxicol. Teratol. 2010, 32:124-131.
58. Slotkin T.A., Seidler F.J., Fumagalli F. 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. 2007, 115:909-916.
59. Slotkin T.A., Seidler F.J., Fumagalli F. Targeting of neurotrophic factors, their receptors, and signaling pathways in the developmental neurotoxicity of organophosphates in vivo and in vitro. Brain Res. Bull. 2008, 76:424-438.
60. Slotkin T.A., Seidler F.J., Fumagalli F. Unrelated developmental neurotoxicants elicit similar transcriptional profiles for effects on neurotrophic factors and their receptors in an in vitro model. Neurotoxicol. Teratol. 2010, 32:42-51.
61. Slotkin T.A., Tate C.A., Ryde I.T., Levin E.D., Seidler F.J. 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. 2006, 114:1542-1546.
62. Song X., Violin J.D., Seidler F.J., Slotkin T.A. Modeling the developmental neurotoxicity of chlorpyrifos in vitro: macromolecule synthesis in PC12 cells. Toxicol. Appl. Pharmacol. 1998, 151:182-191.
63. Tanaka J., Toku K., Zhang B., Isihara K., Sakanaka M., Maeda N. Astrocytes prevent neuronal death induced by reactive oxygen and nitrogen species. Glia 1999, 28:85-96.
64. Teng K.K., Greene L.A. Cultured PC12 cells: a model for neuronal function and differentiation. Cell Biology: A Laboratory Handbook 1994, 218-224. Academic Press, San Diego. J.E. Celis (Ed.).
65. 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.
66. Tuler S.M., Hazen A.A., Bowen J.M. Release and metabolism of dopamine in a clonal line of pheochromocytoma (PC12) cells exposed to fenthion. Fund. Appl. Toxicol. 1989, 13:484-492.
67. Uzoukwu M., Sleight S.D. Dieldrin toxicosis: fetotoxicosis, tissue concentrations, and microscopic and ultrastructural changes in guinea pigs. Am. J. Vet. Res. 1972, 33:579-583.
68. Yang Y.-L., Meng C.-H., Ding J.-H., He H.-R., Ellsworth K., Wu J., Hu G. Iptakalim hydrochloride protects cells against neurotoxin-induced glutamate transporter dysfunction in in vitro and in vivo models. Brain Res. 2005, 1049:80-88.