Acetylcholine neuroprotection against glutamate-induced excitotoxicity in adult pig retinal ganglion cells is partially mediated through α4 nAChRs

Experimental Eye Research

Volumn 83, Issue 5, 2006, Pages 1135-1145

  Thompson, S A ^a   Smith, O ^a   Linn, D M ^b   Linn, C L ^a  

^a WESTERN MICHIGAN UNIVERSITY   (United States)

^b GRAND VALLEY STATE UNIVERSITY   (United States)

Author keywords

excitotoxicity; neuroprotection; nicotinic acetylcholine receptor; retinal ganglion cell

Indexed keywords

ACETYLCHOLINE; ALPHA4 NICOTINIC ACETYLCHOLINE RECEPTOR; ANATOXIN; BETA2 NICOTINIC ACETYLCHOLINE RECEPTOR; BUNGAROTOXIN RECEPTOR; DIHYDRO BETA ERYTHROIDINE; EPIBATIDINE; FUMARIC ACID; GLUTAMIC ACID; LOBELINE; N METHYL 4 (3 PYRIDINYL) 3 BUTENAMINE; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; RECEPTOR SUBUNIT; UB 165; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL ISOLATION; CELL LABELING; CELL PROTECTION; CELL SELECTION; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; EXCITOTOXICITY; IMMUNOCYTOCHEMISTRY; NEUROPHARMACOLOGY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PHARMACODYNAMICS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RECEPTOR DENSITY; RECEPTOR INTRINSIC ACTIVITY; RETINA GANGLION CELL; RETINA NERVE CELL; SIGNAL TRANSDUCTION; SWINE;

ACETYLCHOLINE; ANIMALS; CELL COUNT; CELLS, CULTURED; CHOLINERGIC AGONISTS; DIHYDRO-BETA-ERYTHROIDINE; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; NEUROPROTECTIVE AGENTS; NICOTINIC ANTAGONISTS; RECEPTORS, NICOTINIC; RETINAL GANGLION CELLS; SWINE;

EID: 33748787967     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2006.05.022     Document Type: Article

References (62)

1. Aarts M.M., and Tymainski M. Molecular mechanisms underlying specificity of excitotoxic signaling in neurons. Curr. Mol. Med. 4 (2004) 137-147
2. Aubert I., Cecyre D., Gauthier S., and Quirion R. Comparative ontogenetic profile of cholinergic markers including nicotinic and muscarinic receptors in the rat brain. J. Comp. Neurol. 369 (1996) 31-55
3. Barabino B., Vailati S., Moretti M., McIntosh J.M., Longhi R., Clementi F., and Gotti C. An α4β4 nicotinic receptor subtype is present in chick retina: Identification, characterization and pharmacological comparison with the transfected α4β4 and α6β4 subtypes. Mol. Pharmacol. 59 (2001) 1410-1417
4. Barres B.A., Silverstein B.E., Corey D.P., and Chun L.L. Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron 1 (1988) 791-803
5. Barnstable C.J., and Drager U.C. Thy-1 antigen: a ganglion cell specific marker in rodent retina. Neuroscience 11 (1984) 847-855
6. Barrantes G.E., Rogers A.T., Lindstrom J.M., and Wonnacott S. Alpha-bungarotoxin binding sites in rat hippocampal and cortical cultures: Initial characterization, colocalization and alpha 7 subunits and up-regulation by chronic nicotine treatment. Brain Res. 672 (1995) 228-236
7. Boyd R.T. The molecular biology of neuronal nicotinic acetylcholine receptors. Crit. Rev. Toxicol. 27 (1997) 299-318
8. Bozyczko-Coyne D., McKenna B.W., Connors T.J., and Neff N.T. A rapid fluorometric assay to measure neuronal survival in vitro. J. Neurosci. Methods 50 (1993) 205-216
9. Brooks D.E., Garcia G.A., Dreyer E.B., Zurakowski D., and Franco-Bourland R.E. Vitreous body glutamate concentration in dogs with glaucoma. Am. J. Vis. Res. 58 (1997) 864-867
10. Brown L., and Benchimol S. The involvement of MAPK signaling pathways in determining the cellular response to p53 activation: cell cycle arrest or apoptosis. J. Biol. Chem. 281 (2006) 3832-3840
11. Burnashev N. Calcium permeability of ligand-gated channels. Cell Calcium 24 (1998) 325-332
12. Cadalbert L., Sloss C.M., Cameron P., and Plevin R. Conditional expression of MAP kinase phosphatase-2 protects against genotoxic stress-induced apoptosis by binding and selective dephosphorylation of nuclear activated c-jun N-terminal kinase. Cell Signal. 17 (2005) 1254-1264
13. Casson R.J. Possible role of excitotoxicity in the pathogenesis of glaucoma. Clin. Exp. Ophthalmol. 34 (2006) 54-63
14. Chavez-Noriega L.E., Gillespie A., Stauderman K.A., Crona J.H., Claeps B.O., Elliot K.J., Reid R.T., Rao T.S., Velicelebi G., Harpold M.M., Johnson E.C., and Carey-Naeve J. Characterization of the recombinant human neuronal nicotinic acetylcholine receptors α3β2 and α4β2 stably expressed in HEK293 cells. Neuropharmacology 39 (2000) 2543-2560
15. Chen Z., Gibson T.B., Robinson F., Silvestro L., Pearson G., Xu B., Wright A., Vanderbilt C., and Cobb M.H. Map kinases. Chem. Rev. 101 (2001) 2449-2476
16. Choi D.W. Glutamate neurotoxicity and disease of the nervous system. Neuron 1 (1988) 623-634
17. Court J.A., Lloyd S., Johnson M., Griffiths M., Birdsall N.J., Piggorr M.A., Oakley A.E., Ince P.G., Perry E.K., and Perry R.H. Nicotinic and muscarinic cholinergic receptor binding in the human hippocampal formation during development and aging. Dev. Brain Res. 101 (1997) 93-105
18. Dajas-Bailador F.A., Lima P.A., and Wonnacott S. The α7 nicotinic acetylcholine receptor subtype mediates nicotine protection against NMDA excitotoxicity in primary hippocampal cultures through a calcium ion dependent mechanism. Neuropharmacology 39 (2000) 2799-2807
19. D'Amico D.J. Diseases of the retina. N. Engl. J. Med. 331 (1994) 95-106
20. Dineley K.T., Westerman M., Bui D., Bell K., Ashe K.H., and Sweatt J.D. β-Amyloid activates the mitogen-activated protein kinase cascade via hippocampal α7 nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer's disease. J. Neurosci. 21 (2001) 4125-4133
21. Dreyer E.B., and Lipton S.A. New perspectives on glaucoma. JAMA 281 (1999) 306-308
22. Gahring L.C., Meyer E.L., and Rogers S.W. Nicotine-induced neuroprotection against NMDA or beta-amyloid peptide occur through independent mechanisms distinguished by proinflammatory cytokines. J. Neurochem. 87 (2003) 1125-1136
23. Garcia M., Forster V., Hicks D., and Vecino E. Effect of Muller glia on cell survival and neuritogenesis in adult porcine retina in vitro. Invest. Ophthalmol. Vis. Sci. 43 (2002) 3735-3743
24. Hashiguchi A., Yano S., Morioka M., Hamada J., Ushio Y., Takeuchi Y., and Fukunaga K. Up-regulation of endothelial nitric oxide synthase via phosphatidylinositol 3-kinase pathway contributes to ischemic tolerance in the CA1 subfield of gerbil hippocampus. J. Cereb. Blood Flow Metab. 24 (2004) 271-279
25. Huang Y.Z., Wang Q., Won S., Luo Z.G., Xiong W.C., and Mei L. Compartmentalized NRG signaling and PDZ domain-containing proteins in synapse structure and function. Int. J. Dev. Neurosci. 20 (2002) 173-185
26. Kaneko S., Maeda T., Kume T., Kochiyama H., Akaike A., Shimohama S., and Kimura J. Nicotine protects cultured cortical neurons against glutamate-induced cytotoxicity via α7-neuronal receptors and neuronal CNS receptors. Brain Res. 765 (1997) 135-140
27. Keiger C.J., Prevette D., Conroy W.G., and Oppenheim R.W. Developmental expression of nicotinic receptors in the chick and human spinal cord. J. Comp. Neurol. 455 (2003) 86-99
28. Keyser K.T., Britto L.R., Schoepfer R., Whiting P., Cooper J., Conroy W., Brozozowska-Prechtl A., Karten H.J., and Lindstrom J. Three subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors are expressed in chick retina. J. Neurosci. 13 (1993) 442-454
29. Kihara T., Shimohama S., Urushitani M., Sawada H., Kimura J., Kume T., Maeda T., and Akaike A. Stimulation of α4β2 nicotinic acetylcholine receptors inhibits β-amyloid toxicity. Brain Res. 792 (1998) 331-334
30. Kihara T., Shimohama S., Sawada H., Honda K., Nakamizo T., Shibasaki H., Kume T., and Akaike A. α7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block Aβ-amyloid-induced neurotoxicity. J. Biol. Chem. 276 (2001) 13541-13546
31. Kim H.C., Jhoo W.K., Ko K.H., Kim W.K., Bing G., Kwon M.S., Shin E.J., Suh J.H., Lee Y.G., and Lee D.W. Prolonged exposure to cigarette smoke blocks the neurotoxicity induced by kainic acid in rats. Life Sci. 66 (1999) 317-326
32. Kitano S., Morgan J., and Caprioli J. Hypoxic and excitotoxic damage to cultured rat retinal ganglion cells. Exp. Eye Res. 63 (1996) 105-112
33. Kuehn M.H., Fingert J.H., and Kwon Y.H. Retinal ganglion cell death in glaucoma: mechanisms and neuroprotective strategies. Ophthalmol. Clin. North Am. 18 (2005) 383-395
34. Lafuente M.P., Villegas-Perez P.M., Sobrado-Calvo P., Garcia-Aviles A., Miralles de Imperial J., and Vidal-Sanz M. Neuroprotective effects of α2-selective adrenergic agonists against ischemia-induced retinal ganglion cell death. Invest. Ophthalmol. Vis. Sci. 42 (2001) 2074-2084
35. Laudenbach V., Medja F., Zoli M., Rossi F.M., Evrard P., Changeux J.P., and Gressens P. Selective activation of central subtypes of the nicotinic acetylcholine receptor has opposite effects on neonatal excitotoxic brain injuries. FASEB J. 16 (2002) 423-425
36. Levin L.A. Models of neural injury. J. Glaucoma 10 (2001) S19-S21
37. Li Y., Schlamp C.L., Poulsen G.L., Jackson M.W., Griep A.E., and Nickells R.W. P53 regulates apoptotic retinal ganglion cell death induced by N-methyl-D-aspartate. Mol. Vis. 8 (2002) 341-350
38. Lipton S.A. Retinal ganglion cells, glaucoma and neuroprotection. Prog. Brain Res. 131 (2001) 713-718
39. Lipton S.A., Leifer D., and Barnstable C.J. Selectivity of Thy-1 monoclonal antibodies in enhancing neurite outgrowth. Neurosci. Lett. 137 (1992) 75-77
40. Livingstone M., and Hubel D. Segregation of form, color, movement and depth: anatomy, physiology and perception. Science 240 (1988) 740-749
41. Luo X., Heidinger V., Picaud S., Lambrou G., Dreyfus H., Sahel J., and Hicks D. Selective excitotoxic degeneration of adult pig retinal ganglion cells in vitro. Invest. Ophthalmol. Vis. Sci. 42 (2001) 1096-1106
42. Marin P., Maus M., Desagher S., Glowinski J., and Premont J. Nicotine protects cultured striatal neurones against N-methyl-D-aspartate receptor-mediated neurotoxicity. Neuroreport 5 (1994) 1977-1980
43. McGehee D.S. Molecular diversity of neuronal nicotinic acetylcholine receptors. Ann. N.Y. Acad. Sci. 868 (1999) 565-577
44. Meyer-Franke A., Kaplan M.R., Pfrieger F.W., and Barres B.A. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15 (1995) 805-819
45. Millar N.S. Assembly and subunit diversity of nicotinic acetylcholine receptors. Biochem. Soc. Trans. 31 (2003) 869-874
46. Nakamizo T., Kawamata J., Yamashita H., Kanki R., Kihara T., Sawada H., Akaike A., and Shimohama S. Stimulation of nicotinic acetylcholine receptor protects motor neurons. Biochem. Biophys. Res. Commun. 330 (2005) 1285-1289
47. Olney J.W., and de Gubareff T. Glutamate neurotoxicity and Huntingtons chorea. Nature 271 (1978) 557-559
48. Olson P.A., Tkatch T., Hernandez-Lopez S., Ulrich S., Ilijic E., Mugnaini E., Zhang H., Bezprozvanny I., and Surmeier D.J. G-protein-coupled receptor modulation of striatal CaV1.3 L-type calcium channels is dependent on a Shank-binding domain. J. Neurosci. 25 (2005) 1050-1062
49. O'Neill M.J., Muaary T.K., Lakies V., Visanji N.P., and Duty S. The role of neuronal nicotinic acetylcholine receptors in acute and chronic neurodegeneration. Curr. Drug Targets CNS Neurol. Disord. 1 (2002) 399-411
50. Quigley H.A., Nickells R.W., Kerrigan L.A., Pease M.E., Thibault D.J., and Zack D.J. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest. Ophthalmol. Vis. Sci. 36 (1995) 774-786
51. Ragozzino D., Barabino B., Fucile S., and Eusebi F. Calcium permeability of mouse and chick nicotinic acetylcholine receptors expressed in transiently transfected human cells. J. Physiol. 507 (1998) 749-757
52. Rogers M., and Dani J.A. Comparison of quantitative calcium flux through NMDA, ATP and ACh receptor channels. Biophys. J. 68 (1995) 501-506
53. Romano C., Price M.T., and Olney J.W. Delayed excitotoxic neurodegeneration induced by excitatory amino acid agonists in isolated retina. J. Neurochem. 65 (1995) 59-67
54. Ruiz-Ederra J., Garcia M., Hicks D., and Vecino E. Comparative study of the three neurofilament subunits within pig and human retinal ganglion cells. Mol. Vis. 10 (2004) 83-92
55. Shaw S., Bencherif M., and Marrero M.B. Janus kinase 2, an early target of α7 nicotinic acetylcholine receptor-mediated neuroprotection against Aβ-(1-42) amyloid. J. Biol. Chem. 277 (2002) 44920-44924
56. Sinclair C.M., Bartlett P.F., Greig D.I., and Jeffrey P.L. Distribution of Thy-1 in the avian nervous system: immunohistochemical and absorption analyses with a monoclonal antibody. Brain Res. 398 (1986) 91-105
57. Slemmer J.E., De Zeeuw C.I., and Weber J.T. Don't get too excited: mechanisms of glutamate-mediated Purkinje cell death. Prog. Brain Res. 148 (2005) 367-390
58. Sucher N.J., Lipton S.A., and Dreyer E.B. Molecular basis of glutamate toxicity in retinal ganglion cells. Vis. Res. 37 (1997) 3483-3493
59. Wang J.M., and De Potter W.P. Pig superior cervical ganglion. In: Haynes L.W. (Ed). The Neuron in Tissue Culture (1999), John Wiley, West Sussex, UK 413-419
60. Waxman E.A., and Lynch D.R. NMDA receptor subtypes: multiple roles in excitotoxicity and neurological disease. Neuroscientist 11 (2005) 37-49
61. Wehrwein E., Thompson S.A., Coulibaly S.F., Linn D.M., and Linn C.L. Acetylcholine neuroprotection of adult pig retinal ganglion cells from glutamate-induced excitotoxicity. Invest. Ophthalmol. Vis. Sci. 45 (2004) 1531-1543
62. Weishaupt J.H., Kussmaul L., Grotsch P., Heckel A., Rohde G., Romig H., Bahr M., and Gillardon F. Inhibition of CDK5 is protective in necrotic and apoptotic paradigms of neuronal cell death and prevents mitochondrial dysfunction. Mol. Cell. Neurosci. 24 (2003) 489-502