Alpha-linolenic acid is a potent neuroprotective agent against soman-induced neuropathology

NeuroToxicology

Volumn 33, Issue 5, 2012, Pages 1219-1229

  Pan, Hongna ^a   Hu, Xian zhang ^a   Jacobowitz, David M ^a   Chen, Cynthia ^a   McDonough, John ^b   Van Shura, Kerry ^b   Lyman, Megan ^b   Marini, Ann M ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b US ARMY MEDICAL RESEARCH INSTITUTE OF CHEMICAL DEFENSE   (United States)

Author keywords

Alpha linolenic acid; Cresyl violet; Fluorojade C; Nerve agent; Neurodegeneration; Neuropathology ; Neuroprotection; Nuclear factor kappa B; Rat; Soman

Indexed keywords

ALCOHOL; DIAZEPAM; LINOLEIC ACID; NEUROPROTECTIVE AGENT; SODIUM CHLORIDE; SOMAN;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN TISSUE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG DOSAGE FORM COMPARISON; DRUG EFFICACY; EXPERIMENTAL DESIGN; GEL MOBILITY SHIFT ASSAY; HIPPOCAMPUS; MALE; NERVE DEGENERATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT; SEIZURE; SINGLE DRUG DOSE; TISSUE SECTION;

ALPHA-LINOLENIC ACID; ANALYSIS OF VARIANCE; ANIMALS; BRAIN INJURIES; CHOLINESTERASE INHIBITORS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; MALE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; NEUROTOXICITY SYNDROMES; NF-KAPPA B; ORGANIC CHEMICALS; RATS; RATS, SPRAGUE-DAWLEY; SOMAN;

RATTUS;

EID: 84867231805     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2012.07.001     Document Type: Article

References (60)

1. Aroniadou-Anderjaska V., Figueiredo T.H., Apland J.P., Qashu F., Braga M.F.M. Primary brain targets of nerve agents: the role of the amygdala in comparison to the hippocampus. Neurotoxicology 2009, 30:772-776.
2. Apland J.P., Aroniadou-Anderjaska V., Braga M.F. Soman induces ictogenesis in the amygdala and interictal activity in the hippocampus that are blocked by a GluR5 kainate receptor antagonist in vitro. Neuroscience 2009, 159:380-389.
3. Baille V., Clarke P.G., Brochier G., Dorandeu F., Verna J.M., Four E., et al. Soman-induced convulsions: the neuropathology revisited. Toxicology 2005, 215:1-24.
4. Bajgar J. Organophosphates/nerve agent poisoning: mechanism of action, diagnosis, prophylaxis, and treatment. Adv Clin Chem 2004, 38:151-216.
5. Bajgar J. Complex view on poisoning with nerve agents and organophosphates. Acta Med 2005, 48:3-21.
6. Barthold C.L., Schier J.G. Organic phosphorus compounds - nerve agents. Crit Care Clin 2005, 21:673-689. v-vi.
7. Blondeau N., Widmann C., Lazdunski M., Heurteaux C. Activation of the nuclear factor-κB is a key event in brain tolerance. J Neurosci 2001, 21:4668-4677.
8. Blondeau N., Widmann C., Lazdunski M., Heurteaux C. Polyunsaturated fatty acids induce ischemic and epileptic tolerance. Neuroscience 2002, 109:231-241.
9. Blondeau N., Nguemeni C., Debruyne D.N., Piens M., Wu X., Pan H., et al. Subchronic alpha-linolenic acid treatment enhances brain plasticity and exerts an antidepressant effect: a versatile potential therapy for stroke. Neuropsychopharmacology 2009, 34:2548-2559.
10. Carpentier P., Lambrinidis M., Blanchet G. Early dendritic changes in hippocampal pyramidal neurones (field CA1) of rats subjected to acute soman intoxication: a light microscopic study. Brain Res 1991, 541:293-299.
11. Choi D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1988, 1:623-634.
12. Duan W., Lee J., Guo Z., Mattson M.P. Dietary restriction stimulates BDNF production in the brain and thereby protects neurons against excitotoxic injury. J Mol Neurosci 2001, 16:1-12.
13. Fernandez de Sevilla D., Buno W. Presynaptic inhibition of Schaffer collateral synapses by stimulation of hippocampal cholinergic afferent fibres. Eur J Neurosci 2003, 17:555-558.
14. Fraser D.D., Hoehn K., Weiss S., MacVicar B.A. Arachidonic acid inhibits sodium currents and synaptic transmission in cultured striatal neurons. Neuron 1993, 11:633-644.
15. Grasshoff C., Gillessen T., Thiermann H., Wagner E., Szinicz L. The effect of acetylcholinesterase-inhibition on depolarization-induced GABA release from rat striatal slices. Toxicology 2003, 1184:149-156.
16. Harrison P.K., Sheridan R.D., Green A.C., Scott I.R., Tattersall J.E. A guinea pig hippocampal slice model of organophosphate-induced seizure activity. J Pharmacol Exp Ther 2004, 310-678.
17. Jiang X., Tian F., Du Y., Copeland N.G., Jenkins N.A., Tessarollo L., et al. BHLHB2 controls Bdnf promoter 4 activity and neuronal excitability. J Neurosci 2008, 28:1118-1130.
18. Lallement G., Carpentier P., Pernot-Marino I., Baubichon D., Collet A., Blanchet G. Involvement of the different rat hippocampal glutamatergic receptors in development of seizures induced by soman: an autoradiographic study. Neurotoxicology 1991, 12:655-664.
19. Lallement C., Carpentier P., Collet A., Pernot-Marino I., Baubichon D., Blanchet G. Effects of soman-induced seizures on different extracellular amino acid levels and on glutamate uptake in rat hippocampus. Brain Res 1992, 563:234-240.
20. Lallement G., Denoyer M., Collet A., Pernot-Marino I., Baubichon D., Monmaur P., et al. Changes in hippocampal acetylcholine and glutamate extracellular levels during soman-induced seizures; influence of septal cholinoceptive cells. Neurosci Lett 1992, 139:104-107.
21. Lang-Lazdunski L., Blondeau N., Jarretou G., Lazdunski M., Heurteaux C. Linolenic acid prevents neuronal cell death and paraplegia after transient spinal cord ischemia in rats. J Vasc Surg 2003, 38:564-575.
22. Lauritzen I., Blondeau N., Heurteaux C., Widmann C., Romey G., Lazdunski M. Polyunsaturated fatty acids are potent neuroprotectors. EMBO J 2000, 19:1784-1793.
23. Layish I., Krivoy A., Rotman E., Finkelstein A., Tashma Z., Yehezkelli Y. Pharmacologic prophylaxis against nerve agent poisoning. Isr Med Assoc J 2005, 7:182-187.
24. Li Q., Hirata Y., Piao S., Minami M. The by-products generated during sarin synthesis in the Tokyo sarin disaster induced inhibition of natural killer and cytotoxic T lymphocyte activity. Toxicology 2000, 146:209-220.
25. Li Q., Hirata Y., Kawada T., Minami M. Elevated frequency of sister chromatid exchanges of lymphocytes in sarin-exposed victims of the Tokyo sarin disaster 3 years after the event. Toxicology 2004, 201:209-217.
26. Li Q., Nakadai A., Ishizaki M., Morimoto K., Ueda A., Krensky A.M., et al. Dimethyl 2,2-dichlorovinyl phosphate (DDVP) markedly decreases the expression of perforin, granzyme A and granulysin in human NK-92CI cell line. Toxicology 2005, 213:107-116.
27. Li Q., Kawada T. The new mechanism of organophosphorus pesticides-induced inhibition of cytolytic activity of killer cells. Cell Mol Immunol 2006, 3:171-178.
28. Li Q., Kobayashi M., Kawada T. DDVP markedly decreases the expression of granzyme B and granzyme 3/K in human NK cells. Toxicology 2008, 243:294-302.
29. Lipsky R.H., Xu K., Zhu D., Kelly C., Terhakopian A., Novelli A., et al. NF-κB is a critical determinant for NMDA receptor-mediated neuroprotection. J Neurochem 2001, 78:254-264.
30. López-Muñoz F., García-García P., Alamo C. The pharmaceutical industry and the German National Socialist Regime: I.G. Farben and pharmacological research. J Clin Pharm Ther 2009, 34:67-77.
31. Mattson M.P., Meffert M.K. Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ 2006, 13:852-860.
32. McDonough J.H., Shih T.M. Pharmacological modulation of soman-induced seizures. Neurosci Biobehav Rev 1993, 17:203-215.
33. McDonough J.H., Dochterman L.W., Smith C.D., Shih T.M. Protection against nerve agent-induced neuropathology, but not cardiac pathology, is associated with the anticonvulsant action of drug treatment. Neurotoxicology 1995, 16:123-132.
34. McDonough H.J., Shih T.-M. Neuropharmacological mechanisms of nerve agent-induced seizure and neuropathology. Neurosci Biobehav Rev 1997, 21:559-579.
35. Newmark J. Therapy for nerve agent poisoning. Arch Neurol 2004, 61:649-652.
36. Nguemeni C., Delplanque B., Rovère C., Simon-Rousseau N., Gandin C., Agnani G., et al. Dietary supplementation of alpha-linolenic acid in an enriched rapeseed oil diet protects from stroke. Pharmacol Res 2010, 61:226-233.
37. Ohtani T., Iwanami A., Kasai K., Yamasue H., Kato T., Sasaki T., et al. Post-traumatic stress disorder symptoms in victims of Tokyo subway attack: a 5-year follow-up study. Psychiatry Clin Neurosci 2004, 58:624-629.
38. Okumura T., Takasu N., Ishimatsu S., Miyanoki S., Matsuhashi A., Kumada K., et al. Report on 640 victims of the Tokyo subway sarin attack. Ann Emerg Med 1996, 28:129-135.
39. Olney J.W., Ho O.L., Rhee V. Cytotoxic effects of acidic and sulphur containing amino acids on the infant mouse central nervous system. Exp Brain Res 1971, 14:61-76.
40. Olney J.W., de Gubareff T., Labruyere J. Seizure-related brain damage induced by cholinergic agents. Nature 1983, 301:520-522.
41. Pazdernik T.L., Cross R.S., Giesler M., Samson F.E., McDonough J. Delayed effect of soman: brain glucose use and pathology. Neurotoxicology 1985, 6:61-70.
42. Raveh L., Chapman S., Cohen G., Alkalay D., Gilat E., Rabinovitz I., et al. The involvement of the NMDA receptor complex in the protective effect of anticholinergic drugs against soman poisoning. Neurotoxicology 1999, 20:551-559.
43. 2+-dependent PKC. J Neurophysiol 2007, 98:952-965.
44. Santos M.D., Pereira E.F., Aracava Y., Castro N.G., Fawcett W.P., Randall W.R., et al. Low concentrations of pyridostigmine prevent soman-induced inhibition of GABAergic transmission in the central nervous system: involvement of muscarinic receptors. J Pharmacol Exp Ther 2003, 304:254-265.
45. Schecter W.P. Cholinergic symptoms due to nerve agent attack: a strategy for management. Anesthesiol Clin North America 2004, 22:579-590. viii.
46. Schmitz M.L., Baeuerle P.A. The p65 subunit is responsible for the strong transcription activating potential of NF-κB. EMBO J 1991, 10:3805-3817.
47. Shih T.-M., McDonough J.H. Organophosphorus nerve agents-induced seizures and efficacy of atropine sulfate as anticonvulsant treatment. Pharmacol Biochem Behav 2000, 64:147-153.
48. Shih T.-M., Duniho S.M., McDonough J.H. Control of nerve agent-induced seizures is critical for neuroprotection and survival. Toxicol Appl Pharmacol 2003, 188:69-80.
49. Shih T.M., Skovira J.W., O'Donnell J.C., McDonough J.H. In vivo reactivation by oximes of inhibited blood, brain and peripheral tissue cholinesterase activity following exposure to nerve agents in guinea pigs. Chem Biol Interact 2010, 187:207-214.
50. Sidell F.R., Borak J. Chemical warfare agents: II. Nerve agents. Ann Emerg Med 1991, 21:865-871.
51. Solberg Y., Belkin M. The role of excitotoxicity in organophosphorous nerve agents central poisoning. Trends Pharmacol Sci 1997, 18:183-185.
52. Sparenborg S., Brennecke L.H., Jaax N.K., Braitman D.J. Dizocilpine (MK-801) arrests status epilepticus and prevents brain damage induced by soman. Neuropharmacology 1992, 31:357-368.
53. Thiermann H., Szinicz L., Eyer P., Felgenhauer N., Zilker T., Worek F. Lessons to be learnt from organophosphorus pesticide poisoning for the treatment of nerve agent poisoning. Toxicology 2007, 233:145-154.
54. Vreugdenhil M., Bruehl C., Voskuyl R.A., Kang J.X., Leaf A., Wadman W.J. Polyunsaturated fatty acids modulate sodium and calcium currents in CA1 neurons. Proc Natl Acad Sci U S A 1996, 93:12559-12563.
55. Wade J.V., Samson F.E., Nelson S.R., Pazdernik T.L. Changes in extracellular amino acids during soman- and kainic acid-induced seizures. J Neurochem 1987, 49:645-650.
56. Wielock T. Hypoglycemia-induced neuronal damage prevented by an N-methyl-d-aspartate antagonist. Science 1985, 230:681-683.
57. Wood S.J., Tattersall J.E. An improved brain slice model of nerve agent-induced seizure activity. J Appl Toxicol 2001, (Suppl. 1):S83-S86.
58. Xiao Y.-F., Li X. Polyunsaturated fatty acids modify mouse hippocampal neuronal excitability during excitotoxic or convulsant stimulation. Brain Res 1999, 846:112-121.
59. Yajeya J., De La Fuente A., Criado J.M., Bajo V., Sanchez-Riolobos A., Heredia M. Muscarinic agonist carbachol depresses excitatory synaptic transmission in the rat basolateral amygdale in vitro. Synapse 2000, 38:151-160.
60. Yu Z., Zhou D., Bruce-Keller A.J., Kindy M.S., Mattson M.P. Lack of the p50 subunit of nuclear factor-kappaB increases the vulnerability of hippocampal neurons to excitotoxic injury. J Neurosci 1999, 19:8856-8865.