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Calcium, AMPA/Kainate Receptors, and Selective Neurodegeneration

  • John H. Weiss
  • Hong Z. Yin
  • Sean G. Carriedo
  • You M. Lu
Part of the GWUMC Department of Biochemistry and Molecular Biology Annual Spring Symposia book series (GWUN)

Abstract

Neurotoxic effects of the excitatory amino acid (EAA) glutamate play an important role in the pathogenesis of acute diseases of the nervous system such as stroke;1 additionally, several lines of evidence lend support to a possibility that slower EAA toxicity may contribute to neurodegeneration associated with certain neurodegenerative disease.2–5 The purpose of this chapter is twofold. First, I will review several lines of evidence supporting the idea that activation of AMPA/kainate-type glutamate receptors might play a particular role in the selective pattern of neurodegeneration seen in Alzheimer’s disease (AD) and amyotrophic lateral sclerosis (ALS). Secondly, I will discuss certain recent results bearing on the role of Ca2+ ions in selective AMPA/kainate receptor-mediated degeneration.

Keywords

Amyotrophic Lateral Sclerosis Excitatory Amino Acid Basal Forebrain Influx Rate Domoic Acid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    S.M. Rothman and J.W. Olney, Glutamate and the pathophysiology of hypoxic-ischemic brain damage, Ann. Neural 19:105 (1986).CrossRefGoogle Scholar
  2. 2.
    M.F. Beal, Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses?, Ann. Neurol. 31:119 (1992).PubMedCrossRefGoogle Scholar
  3. 3.
    J.T. Greenamyre and A.B. Young, Excitatory amino acids and Alzheimer’s disease, Neurobiol Aging 10:593 (1989).PubMedCrossRefGoogle Scholar
  4. 4.
    A. Plaitakis and J.T. Caroscio, Abnormal glutamate metabolism in amyotrophic lateral sclerosis, Ann. Neurol. 22:575 (1987).PubMedCrossRefGoogle Scholar
  5. 5.
    J.D. Rothstein, L.J. Martin, and R.W. Kuncl, Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis, New Engl. J. Med. 326:1464 (1992).PubMedCrossRefGoogle Scholar
  6. 6.
    J. Hugon, F. Tabaraud, M. Rigaud, J.M. Vallat, and M. Dumas, Glutamate dehydrogenase and aspartate aminotransferase in leukocytes of patients with motor neuron disease, Neurology 39:956 (1989).PubMedCrossRefGoogle Scholar
  7. 7.
    J.D. Rothstein, G. Tsai, R.W. Kuncl, L. Clawson, D.R. Cornblath, D.B. Drachman, A. Pestronk, B.L. Stauch, and J.T. Coyle, Abnormal excitatory amino acid metabolism in amyotrophic lateral sclerosis, Ann. Neurol. 28:18 (1990).PubMedCrossRefGoogle Scholar
  8. 8.
    T.M. Perl, L. Bedard, T. Kosatsky, J.C. Hockin, E.C. Todd, and R.S. Remis, An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid, New Engl. J. Med. 322:1775 (1990).PubMedCrossRefGoogle Scholar
  9. 9.
    J.S. Teitelbaum, R.J. Zatorre, S. Carpenter, D. Gendron, A.C. Evans, A. Gjedde, and N.R. Cashman, Neurologic sequelae of domoic acid intoxication due to the ingestion of contaminated mussels, New Engl J. Med. 322:1781 (1990).PubMedCrossRefGoogle Scholar
  10. 10.
    P.S. Spencer, A. Ludolph, M.P. Dwivedi, D.N. Roy, J. Hugon, and H.H. Schaumberg, Lathyrism: evidence for the role of the neuroexcitatory amino acid BOAA, Lancet 2:1066 (1986).PubMedCrossRefGoogle Scholar
  11. 11.
    P.S. Spencer, P.B. Nunn, J. Hugon, J. Ludolph, A.C. Ross, S.M. Ross, D.N. Roy, and R.C. Robertson, Guam amyotrophic lateral sclerosis-Parkinsonism-dementia linked to a plant excitant neurotoxin, Science 237:517 (1987).PubMedCrossRefGoogle Scholar
  12. 12.
    R.J. Bridges, D.R. Stevens, J.S. Kahle, P.B. Nunn, M. Kadri, and C.W. Cotman, Structure-function studies on N-oxalyl-diamino-dicarboxylic acids and excitatory amino acid receptors: evidence that beta-L-ODAP is a selective non-NMDA agonist, J. Neurosci. 9:2073 (1989).PubMedGoogle Scholar
  13. 13.
    G. Debonnel, L. Beauchesne, and C. de Montigny, Domoic acid, the alleged “mussel toxin,” might produce its neurotoxic effect through kainate receptor activation: an electrophysiological study in the dorsal hippocampus, Can. J. Physiol. Pharmacol. 67:29 (1989).PubMedCrossRefGoogle Scholar
  14. 14.
    S.M. Ross, M. Seelig, and P.S. Spencer, Specific antagonism of excitotoxic action of “uncommon” amino acids assayed in organotypic mouse cortical cultures, Brain Res. 425:120 (1987).PubMedCrossRefGoogle Scholar
  15. 15.
    J.H. Weiss, J. Koh, and D.W. Choi, Neurotoxicity of beta-N-methylamino-L-alanine (BMAA) and beta-N-oxalylamino-L-alanine (BOAA) on cultured cortical neurons, Brain Res. 497:64 (1989).PubMedCrossRefGoogle Scholar
  16. 16.
    V. Chan-Palay, Somatostatin immunoreactive neurons in the human hippocampus and cortex shown by immunogold/silver intensification on vibratome sections: coexistence with neuropeptide Y neurons, and effects in Alzheimer-type dementia, J. Comp. Neurol. 260:201 (1987).PubMedCrossRefGoogle Scholar
  17. 17.
    P. Davies, R. Katzman, and R.D. Terry, Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementia, Nature. 288:279 (1980).PubMedCrossRefGoogle Scholar
  18. 18.
    M.N. Rossor, P.C. Emson, C.Q. Mountjoy, M. Roth, and L.L. Iversen, Reduced amounts of immunoreactive somatostatin in the temporal cortex in senile dementia of Alzheimer type, Neurosci. Lett. 20:373 (1980).PubMedCrossRefGoogle Scholar
  19. 19.
    H. Arai, P.C. Emson, C.Q. Mountjoy, L.H. Carassco, and C.W. Heizmann, Loss of parvalbuminimmunoreactive neurones from cortex in Alzheimer-type dementia, Brain Res. 418:164 (1987).PubMedCrossRefGoogle Scholar
  20. 20.
    J. Satoh, T. Tabira, M. Sano, H. Nakayama, and J. Tateishi, Parvalbumin-immunoreactive neurons in the human central nervous system are decreased in Alzheimer’s disease, Acta Neuropathol. 81:388 (1991).PubMedCrossRefGoogle Scholar
  21. 21.
    P.J. Whitehouse, D.L. Price, A.W. Clark, J.T. Coyle, and M.R. DeLong, Alzheimer disease: evidence for selective loss of cholinergic neurons in the nucleus basalis, Ann. Neurol. 10:122 (1981).PubMedCrossRefGoogle Scholar
  22. 22.
    J.H. Weiss, J. Koh, K.G. Baimbridge, and D.W. Choi, Cortical neurons containing somatostatin or parvalbumin-like immunoreactivity are atypically vulnerable to excitotoxic injury in vitro, Neurology 40:1288 (1990).PubMedCrossRefGoogle Scholar
  23. 23.
    K.J. Page, B.J. Everitt, T.W. Robbins, H.M. Marston, and L.S. Wilkinson, Dissociable effects on spatial maze and passive avoidance acquisition and retention following AMPA-and ibotenic acid-induced excitotoxic lesions of the basal forebrain in rats: differential dependence on cholinergic neuronal loss, Neuroscience 43:457 (1991).PubMedCrossRefGoogle Scholar
  24. 24.
    J.H. Weiss, H. Yin, and D.W. Choi, Basal forebrain cholinergtic neurons are selectively vulnerable to AMPA/kainate receptor-mediated neurotoxicity, Neuroscience 60:659 (1994).PubMedCrossRefGoogle Scholar
  25. 25.
    M.J. Campbell and J.H. Morrison, Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex, J. Comp. Neurol. 282:191 (1989).PubMedCrossRefGoogle Scholar
  26. 26.
    J.H. Morrison, D.A. Lewis, M.J. Campbell, G.W. Huntley, D.L. Benson, and C. Bouras, A monoclonal antibody to non-phosphorylated neurofilament protein marks the vulnerable cortical neurons in Alzheimer’s disease, Brain Res. 416:331 (1987).PubMedCrossRefGoogle Scholar
  27. 27.
    P.R. Hof, K. Cox, and J.H. Morrison, Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease: I. Superior frontal and inferior temporal cortex, J. Comp. Neurol. 301:44 (1990).PubMedCrossRefGoogle Scholar
  28. 28.
    P.R. Hof and J.H. Morrison, Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease: II. Primary and secondary visual cortex, J. Comp. Neurol. 301:55 (1990).PubMedCrossRefGoogle Scholar
  29. 29.
    S.J. Burke, H.Z. Yin, and J.H. Weiss, Ca2+ and in vitro kainate damage to cortical and hippocampal SMI-32(+) neurons, NeuroReport 6:629 (1995).PubMedCrossRefGoogle Scholar
  30. 30.
    M.P. Mattson and S.B. Kater, Development and selective neurodegeneration in cell cultures from different hippocampal regions, Brain Res. 490:110 (1989).PubMedCrossRefGoogle Scholar
  31. 31.
    T. Gotow and J. Tanaka, Phosphorylation of neurofilament H subunit as related to arrangement of neurofilaments, J. NeuroscL Res. 37:691 (1994).CrossRefGoogle Scholar
  32. 32.
    S.G. Carriedo, H.Z. Yin, R. Lamberta, and J.H. Weiss, In vitro kainate injury to large, SMI-32 spinal neurons is Ca2+ dependent, NeuroReport 6:945 (1995).PubMedCrossRefGoogle Scholar
  33. 33.
    J. Hugon, J.M. Vallat, P.S. Spencer, M.J. Leboutet, and D. Barthe, Kainic acid induces early and delayed degenerative neuronal changes in rat spinal cord, NeuroscL Lett. 104:258 (1989).CrossRefGoogle Scholar
  34. 34.
    J.D. Rothstein, L. Jin, M. Dykes-Hoberg, and R.W. Kuncl, Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity, Proc. Natl. Acad. Sci. USA 90:6591 (1993).PubMedCrossRefGoogle Scholar
  35. 35.
    A.B. MacDermott, M.L. Mayer, G.L. Westbrook, S.J. Smith, and J.L. Barker, NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones, Nature 321:519 (1986).PubMedCrossRefGoogle Scholar
  36. 36.
    D.W. Choi, Excitotoxic cell death, J. Neurobiol. 23:1261 (1992).PubMedCrossRefGoogle Scholar
  37. 37.
    M. lino, S. Ozawa, and K. Tsuzuki, Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones, J. Physiol. 424:151 (1990).Google Scholar
  38. 38.
    R.M. Pruss, R.L. Akeson, M.M. Racke, and J.L. Wilburn, Agonist-activated cobalt uptake identifies divalent cation-permeable kainate receptors on neurons and glia, Neuron 7:509 (1991).PubMedCrossRefGoogle Scholar
  39. 39.
    J.R. Brorson, P.A. Manzolillo, and R.J. Miller, Ca2+ entry via AMPA/KA receptors and excitotoxicity in cultured cerebellar purkinje cells, J. Neuroscl. 14:187 (1994).Google Scholar
  40. 40.
    D.M. Turetsky, L.M.T. Canzoniero, S.L. Sensi, J.H. Weiss, M.P. Goldberg, and D.W. Choi, Cortical neurons exhibiting kainate-activated Co2+ uptake are selectively vulnerable to AMPA/kainate receptor-mediated toxicity, Neurobiol. Dis. 1:101 (1994).PubMedCrossRefGoogle Scholar
  41. 41.
    H. Yin, A.D. Lindsay, and J.H. Weiss, Kainate injury to cultured basal forebrain cholinergic neurons in Ca2+ dependent, NeuroReport 5:1477 (1994).PubMedCrossRefGoogle Scholar
  42. 42.
    M. Tymianski, M.P. Charlton, P.L. Carlen, and C.H. Tator, Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons, J. Neurosci. 13:2085 (1993).PubMedGoogle Scholar
  43. 43.
    Y.M. Lu, H.Z. Yin, and J.H. Weiss, Ca2+ permeable AMPA/kainate channels permit rapid injurious Ca2+ entry, NeuroReport 13 6 (1995), in press.Google Scholar
  44. 44.
    D.M. Hartley, M.C. Kurth, L. Bjerkness, J.H. Weiss, and D.W. Choi, Glutamate receptor-induced 45Ca2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration, J. Neurosci. 13:1993 (1993).PubMedGoogle Scholar
  45. 45.
    L.L. Dugan, S.L. Sensi, L.M.T. Cazoniero, M.P. Goldberg, S.D. Handran, S.M. Rothman, and D.W. Choi, Imaging of mitochondrial oxygen radical production in cortical neurons exposed to NMDA, Soc. Neurosci. Abstr. 20:1532 (1994).Google Scholar
  46. 46.
    M. Lafon-Cazal, S. Pietri, M. Culcasi, and J. Bockaert, NMDA-dependent Superoxide production and neurotoxicity, Nature 364:535 (1993).PubMedCrossRefGoogle Scholar
  47. 47.
    I.J. Reynolds, T.G. Hastings, and K.R. Hoyt, Studies on the role of mitochondria in NMDA receptor-mediated excitotoxicity, Soc. Neurosci. Abstr. 20:1530 (1994).Google Scholar
  48. 48.
    J.L. Werth and S.A. Thayer, Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons, J. Neurosci. 14:348 (1994).PubMedGoogle Scholar
  49. 49.
    M.F. Beal, K.J. Swartz, S.F. Finn, M.F. Mazurek, and N.W. Kowall, Neurochemical characterization of excitotoxin lesions in the cerebral cortex, J. Neurosci. 11:147 (1991).PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • John H. Weiss
    • 1
  • Hong Z. Yin
    • 1
  • Sean G. Carriedo
    • 1
  • You M. Lu
    • 1
  1. 1.Department of NeurologyUniversity of California, IrvineIrvineUSA

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