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6 - Calcium binding proteins in selective vulnerability of motor neurons

from Part I - Basic aspects of neurodegeneration

Published online by Cambridge University Press:  04 August 2010

M. Flint Beal ,
Anthony E. Lang  and
Albert C. Ludolph
By
László Siklós  and
Stanley H. Appel
M. Flint Beal
Affiliation:
Cornell University, New York
Anthony E. Lang
Affiliation:
University of Toronto
Albert C. Ludolph
Affiliation:
Universität Ulm, Germany
László Siklós
Affiliation:
Institute of Biophysics, Biological Research Center, Szeged, Hungary
Stanley H. Appel
Affiliation:
Department of Neurology, Baylor College of Medicine, Houston, TX, USA
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Summary

Introduction

Since the mid-1990s, the specific etiologies and mechanisms leading to dysfunction and loss of motor neurons in ALS have been under intensive investigation. No single mechanism appears to explain the devastating and inexorable injury to motor neurons. What appears far more likely is a convergence of a number of different mechanisms that collectively or sequentially impair motor neuron structure and function. Among the various proposals implicated, increased free radicals and oxidative stress, increased glutamate excitotoxicity, increased cellular aggregates and increased intracellular calcium have received the most attention (Rothstein, 1995; Cleveland, 1999; Shaw & Eggett, 2000; Rowland, 2000; Julien, 2001; Rowland & Shneider, 2001; Cleveland & Rothstein, 2001). None of these mechanisms is mutually exclusive and altered calcium homeostasis, free radicals, and glutamate excitotoxicity may all participate in the cell injury cascade leading to motor neuron death. Alterations in one parameter can lead to alterations in other parameters, and each can enhance and propagate the injury cascade. Such perturbations could critically impair motor neuron mitochondria and neurofilaments, compromise energy production and axoplasmic flow, and impair synaptic function. However, these alterations would be expected to adversely affect most neurons, and the critical question is why motor neurons are uniquely sensitive to injury in ALS, and why some motor neurons are relatively resistant to injury. Our own hypothesis focuses on the critical role of intracellular calcium and the inability of vulnerable motor neurons to handle an increased intracellular calcium load, possibly related to the relative paucity of the calcium binding proteins, calbindin D28k and parvalbumin.

Type
Chapter
Information
Neurodegenerative Diseases
Neurobiology, Pathogenesis and Therapeutics
 , pp. 65 - 79
Publisher: Cambridge University Press
Print publication year: 2005

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References

Adalbert, R. J., Engelhardt, J. I. & Siklós, L. (2002). DL-homocysteic acid application disrupts calcium homeostasis and induces degeneration of spinal motoneurons in vivo. Acta Neuropathol., 103, 428–36CrossRefGoogle ScholarPubMed
Alexianu, M. E., Ho, B. K., Mohamed, H., , Bella, V., , Smith, R. G. &Appel, S. H. (1994). The role of calcium-binding proteins in selective motoneuron vulnerability in amyotrophic lateral sclerosis. Ann. Neurol., 36, 846–58CrossRefGoogle ScholarPubMed
Amenta, F., , Cavalotta, D., , Del Valle, M. E.et al. (1994). Calbindin D-28k immunoreactivity in the rat cerebellar cortex: age-related changes. Neurosci. Lett., 178, 131–4CrossRefGoogle Scholar
Appel, S. H., Beers, D., , Siklós, L., , Engelhardt, J. I. &Mosier, D. R. (2001). Calcium: the Darth Vader of ALS. ALS Other Motor Neuron Disord., 2, S47–54Google ScholarPubMed
Baimbridge, K. G., Celio, M. R. & Rogers, J. H. (1992). Calcium-binding proteins in the nervous system. Trends Neurosci., 15, 303–8CrossRefGoogle Scholar
Beck, K. D., Hefti, F., & Widmer, H. R. (1994). Deafferentation removes calretinin immunopositive terminals, but does not induce degeneration of calbindin D-28k and parvalbumin expressing neurons in the hippocampus of adult rats. J. Neurosci. Res., 39, 298–304CrossRefGoogle Scholar
Beers, D. R., Ho, B. K., Siklós, L.et al. (2001). Parvalbumin overexpression alters immune-mediated increases in intracellular calcium, and delays disease onset in a transgenic model of familial amyotrophic lateral sclerosis. J. Neurochem., 79, 499–509CrossRefGoogle Scholar
Bergmann, M., , Volpel, M., & Kuchelmeister, K. (1995). Onuf's nucleus is frequently involved in motor neuron disease/amyotrophic lateral sclerosis. J. Neurol. Sci., 129, 141–6CrossRefGoogle Scholar
Bernardi, P. (1999). Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev., 79, 1127–55CrossRefGoogle ScholarPubMed
Berridge, M. J. (1998). Neuronal calcium signaling. Neuron, 21, 13–26CrossRefGoogle ScholarPubMed
Berridge, M. J., Bootman, M. D. & Lipp, P. (1998). Calcium – a life and death signal. Nature, 395, 645–8CrossRefGoogle ScholarPubMed
Berridge, M. J., Lipp, P., & Bootman, M. D. (2000). The versatility and universality of calcium signalling. Nat. Rev., 1, 11–21CrossRefGoogle ScholarPubMed
Brini, M. & Carafoli, E. (2000). Calcium signalling: a historical account, recent developments and future perspectives. Cell Mol. Life. Sci., 57, 354–70CrossRefGoogle ScholarPubMed
Brini, M., Bano, D., Manni, S., Rizzuto, R. & Carafoli, E. (2000). Effects of PMCA and SERCA pump overexpression on the kinetics of cell Ca2+ signalling. EMBO J., 19, 4926–35CrossRefGoogle Scholar
Brodin, L., Löw, P., Gad, H., Gustaffson, J., Pieribone, V. A. & Shupliakov, O. (1997). Sustained neurotransmitter release: new molecular clues. Eur. J. Neurosci., 9, 2503–11CrossRefGoogle ScholarPubMed
Brustovetsky, N., Brustovetsky, T., Jemmerson, R. & Dubinsky, J. M. (2002). Calcium-induced cytochrome C release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. J. Neurochem., 80, 207–18CrossRefGoogle ScholarPubMed
Burrone, J., Guilherme, N., Gomis, A., Cooke, A. & Lagnado, L. (2002). Endogenous calcium buffers regulate fast exocytosis in the synaptic terminal of retinal bipolar cells. Neuron., 33, 101–12CrossRefGoogle ScholarPubMed
Carafoli, E. & Stauffer, T. (1994). The plasma membrane calcium pump: functional domains, regulation of the activity, and tissue specificity of isoform expression. J. Neurobiol., 25, 312–24CrossRefGoogle ScholarPubMed
Cassina, P., Peluffo, H., Pehar, M.et al. (2002). Peroxynitrite triggers a phenotypic transformation in spinal cord astrocytes that induces motor neuron apoptosis. J. Neurosci. Res., 67, 21–9CrossRefGoogle ScholarPubMed
Celio, M. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience, 35, 375–475CrossRefGoogle ScholarPubMed
Cheung, W. Y. (1980). Calmodulin plays a pivotal role in cellular regulation. Science, 207, 19–27CrossRefGoogle Scholar
Choi, D. W., Maulucci-Gedde, M. & Kriegstein, A. R. (1987). Glutamate neurotoxicity in cortical cell ulture. J. Neurosci., 7, 357–68CrossRefGoogle Scholar
Clapham, D. E. (1995). Calcium signaling. Cell, 80, 259–68CrossRefGoogle ScholarPubMed
Clement, A. M., Nguyen, M. D., Roberts, E. A.et al. (2003). Wild-type nonneural cells extend survival of SOD1 mutant motor neurons in ALS mice. Science, 302, 113–17CrossRefGoogle Scholar
Clementi, E., Racchetti, G., Melino, G. & Meldolesi, J. (1996). Cytosolic Ca2+ buffering, a cell property that in some neurons markedly decreases during aging, has a protective effect against NMDA/nitric oxide-induced excitotoxicity. Life Sci., 59, 389–97CrossRefGoogle Scholar
Cleveland, D. W. (1999). From Charcot to SOD1: mechanisms of selective motor neuron death in ALS. Neuron, 24, 515–20CrossRefGoogle ScholarPubMed
Cleveland, D. W. & Liu, J. (2000). Oxidation versus aggregation – how do SOD1 mutants cause ALS?Nat. Med., 6, 1320–1CrossRefGoogle ScholarPubMed
Cleveland, D. W. & Rothstein, J. D. (2001). From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci., 2, 806–19CrossRefGoogle ScholarPubMed
Colom, L. V., Alexianu, M. E., Mosier, D. R., Smith, R. G. & Appel, S. H. (1997). Amyotrophic lateral sclerosis immunoglobulins increase intracellular calcium in a motoneuron cell line. Exp. Neurol., 146, 354–60CrossRefGoogle Scholar
Corvino, V., Businaro, R., Geloso, M. C.et al. (2003). S100B protein and 4-hydroxynonenal in the spinal cord of wobbler mice. Neurochem. Res., 28, 341–5CrossRefGoogle ScholarPubMed
Cox, D. A. & Matlib, M. A. (1993). Modulation of intramitochondrial free Ca2+ concentration by antagonists of Na+–Ca2+ exchange. Trends Pharm. Sci., 14, 408–13CrossRefGoogle ScholarPubMed
Dassesse, D., Cuvelier, L., Krebs, C.et al. (1998). Differential expression of calbindin and calmodulin in motoneurons after hypoglossal axotomy. Brain Res., 786, 181–8CrossRefGoogle ScholarPubMed
Du, S., Rubin, A., Klepper, S.et al. (1999). Calcium influx and activation of calpain I mediate acute reactive gliosis in injured spinal cord. Exp. Neurol., 157, 96–105CrossRefGoogle ScholarPubMed
Engelhardt, J. I., Siklós, L., Kőműves, L., Smith, R. G. & Appel, S. H. (1995). Antibodies to calcium channels from ALS patients passively transferred to mice selectively increase intracellular calcium and induce ultrastructural changes in motor neurons. Synapse, 20, 185–99CrossRefGoogle Scholar
Elliott, J. L. & Snider, W. D. (1995). Parvalbumin is a marker of ALS-resistant motor neurons. NeuroReport, 6, 449–52CrossRefGoogle ScholarPubMed
Fallah, Z. & Clowry, G. J. (1999). The effect of a peripheral nerve lesion on calbindin D28k immunoreactivity in the cervical ventral horn of developing and adult rats. Exp. Neurol., 156, 111–20CrossRefGoogle ScholarPubMed
Ferrer, I., Soriano, E., Tunon, T., Fonseca, M. & Guionnet, N. (1991). Parvalbumin immunoreactive neurons in normal human temporal neocortex and in patients with Alzheimer's disease. J. Neurol. Sci., 106, 135–41CrossRefGoogle ScholarPubMed
Freund, T. F., Buzsáki, G., Leon, A., Baimbridge, K. G. & Somogyi, P. (1990). Relationship of neural vulnerability and calcium binding protein immunoreactivity in ischemia. Exp. Brain. Res., 83, 55–66CrossRefGoogle Scholar
Fukuda, A., Deshpande, S. B., Shimano, Y. & Nishino, H. (1998). Astrocytes are more vulnerable than neurons to cellular Ca2+ overload induced by a mitochondrial toxin, 3-nitropropionic acid. Neuroscience, 87, 497–507CrossRefGoogle ScholarPubMed
Gad, H., Löw, P., Zotova, E., Brodin, L. & Shupliakov, O. (1998). Dissociation between Ca2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron, 21, 607–16CrossRefGoogle Scholar
Gong, Y. H., Parsadanian, A. S., Andreeva, A., Snider, W. D. & Elliott, J. S. (2000). Restricted expression of G86R Cu/Zn superoxide dismutase in astrocytes results in astrocytosis but does not cause motoneuron degeneration. J. Neurosci., 20, 660–5CrossRefGoogle Scholar
Gunter, T. E. & Pfeiffer, D. R. (1990). Mechanisms by which mitochondria transport calcium. Am. J. Physiol., 27, C755–86CrossRefGoogle Scholar
Gunter, T. E., Buntinas, L., Sparagne, G. C. & Gunter, K. K. (1998). The Ca2+ transport mechanism of mitochondria and Ca2+ uptake from physiological-type Ca2+ transients. Biochim. Biophys. Act., 1366, 5–15CrossRefGoogle ScholarPubMed
Gurney, M. E., Pu, H., Chiu, A. Y.et al. (1994). Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science, 164, 1772–5CrossRefGoogle Scholar
Hartley, D. M., Neve, R. L., Bryan, J.et al. (1996). Expression of the calcium-binding protein, parvalbumin, in cultured cortical neurons using a HSV-1 vector system enhances NMDA neurotoxicity. Brain Res. Mol. Brain Res., 40, 285–96CrossRefGoogle ScholarPubMed
Ho, B. K., Alexianu, M. E., Colom, L. V., Mohamed, A. H., Serrano, F. & Appel, S. H. (1996). Expression of calbindin-D28K in motoneuron hybrid cells after retroviral infection with calbindin-D28K cDNA prevents amyotrophic lateral sclerosis IgG-mediated cytotoxicity. Proc. Natl Acad. Sci., USA, 93, 6796–801CrossRefGoogle ScholarPubMed
Hof, P. R., Cox, K., Young, W. G., Celio, M. R., Rogers, J. & Morrison, J. H. (1991). Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer's disease. J. Neuropathol. Exp. Neurol., 50, 451–62CrossRefGoogle ScholarPubMed
Hofer, A. M., Landolfi, B., Debellis, L., Pozzan, T. & Curci, S. (1998). Free [Ca2+] dynamics measured in agonist-sensitive strores of single living intact cells: a new look at the refilling process. EMBO J., 17, 1986–95CrossRefGoogle Scholar
Howland, D. S., Liu, J., She, Y.et al. (2002). Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl Acad. Sci. USA, 99, 1604–9CrossRefGoogle Scholar
Hoyaux, D., Alao, J., Fuchs, J.et al. (2000). S100A6, a calcium- and zinc-binding protein, is overexpressed in SOD1 mutant mice, a model for amyotrophic lateral sclerosis. Biochim. Biophys. Act., 1498, 264–72CrossRefGoogle ScholarPubMed
Hoyaux, D., Boom, A., Bosch, L.et al. (2002). S100A6 overexpression within astrocytes associated with impaired axons from both ALS mouse model and human patients. J. Neuropathol. Exp. Neurol., 61, 736–44CrossRefGoogle ScholarPubMed
Iacopino, A. M. & Christakos, S. (1990). Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc. Natl Acad. Sci., USA, 87, 4078–82CrossRefGoogle ScholarPubMed
Ince, P., Stout, N., Shaw, P.et al. (1993). Parvalbumin and calbindin D-28k in the human motor system and in motor neuron disease. Neuropathol. Appl. Neurobiol., 19, 291–9CrossRefGoogle ScholarPubMed
Julien, J. P. (2001). Amyotrophic lateral sclerosis: unfolding the toxicity of the misfolded. Cell, 104, 581–91CrossRefGoogle ScholarPubMed
Kawasaki, H., , Nakayama, S., & Kretsinger, R. H. (1998). Classification and evolution of EF-hand proteins. BioMetals, 11, 277–95CrossRefGoogle Scholar
Kirischuk, S. & Verkhratsky, A. (1996). Calcium homostasis in aged neurons. Life Sci., 59, 451–9CrossRefGoogle Scholar
Kishimoto, J., Tsuchiya, T., Cox, H., Emson, P. C. & Nakayama, Y. (1998). Age-related changes of calbindin-D28k, calretinin, and parvalbumin mRNAs in the hamster brain. Neurobiol. Agin., 19, 77–82CrossRefGoogle ScholarPubMed
Klapstein, G. J., Vietla, S., , Lieberman, D. N.et al. (1998). Calbindin-D28k fails to protect hippocampal neurons against ischemia in spite of its cytoplasmic calcium buffering properties: evidence from calbindin-D28k knockout mice. Neuroscience, 85, 361–73CrossRefGoogle ScholarPubMed
Kocsis, J. D., Rand, M. N., Lankford, K. L. & Waxman, S. G. (1993). Intracellular calcium mobilization and neurite outgrowth in mammalian neurons. J. Neurobiol., 25, 252–64CrossRefGoogle Scholar
Koliatsos, V. E. & Price, D. L. (1996). Axotomy as an experimental model of neuronal injury and cell death. Brain Pathol., 6, 447–65CrossRefGoogle ScholarPubMed
Krebs, C., Neiss, W. F., Streppel, M.et al. (1997). Axotomy induces transient calbindin D28K immunoreactivity in hypoglossal motoneurons in vivo. Cell Calcium, 22, 367–72CrossRefGoogle ScholarPubMed
Kroemer, G., Dallaporta, B. & Resche-Rigon, M. (1998). The mitochondrial death/life regulator in apoptosis and necrosis. Ann. Rev. Physiol., 60, 619–42CrossRefGoogle ScholarPubMed
Bella, V., Goodman, J. C. & Appel, S. H. (1997). Increased CSF glutamate following injection of ALS immunoglobulins. Neurology, 48, 1270–2CrossRefGoogle ScholarPubMed
Laslo, P., Lipski, J., Nicholson, L. F. B., Miles, G. B. & Funk, G. D. (2000). Calcium binding proteins in motoneurons at low and high risk for degeneration in ALS. NeuroReport, 11, 3305–8CrossRefGoogle ScholarPubMed
Laslo, P., Lipski, J., Nicholson, L. F. B., Miles, G. B. & Funk, G. D. (2001). GluR2 AMPA receptor subunit expression in motoneurons at low and high risk for degeneration in amyotrophic lateral sclerosis. Exp. Neurol., 169, 461–71CrossRefGoogle ScholarPubMed
Leenders, A. G. M., Scholten, G., Lange, R. P. J., Lopes da Silva, F. H. & Ghijsen, W. E. J. M. (2002). Sequential changes in synaptic vesicle pools and endosome-like organelles during depolarization near the active zone of central nerve terminals. Neuroscience, 109, 195–206CrossRefGoogle ScholarPubMed
Lewit-Bentley, A. & Réty, S. (2000). EF-hand calcium-binding proteins. Curr. Opin. Struct. Biol., 10, 637–43CrossRefGoogle ScholarPubMed
Lino, M. M., Schneider, C. & Caroni, P. (2002). Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J. Neurosci., 22, 4825–32CrossRefGoogle ScholarPubMed
Lledo, P. M., Somasundaram, B., Morton, A. J., Emson, P. C. & Mason, W. T. (1992). Stable transfection of calbindin-D28k into the GH3 cell line alters calcium currents and intracellular calcium homeostasis. Neuron, 9, 943–54CrossRefGoogle ScholarPubMed
Marsden, B. J., Shaw, G. S. & Sykes, B. D. (1990). Calcium binding proteins. Elucidating the contributions to calcium affinity from an analysis of species variants and peptide fragments. Biochem. Cell. Biol., 68, 587–601CrossRefGoogle ScholarPubMed
Mattson, M. P. (1998). Free radicals, calcium, and the synaptic plasticity – cell death continuum: emerging role of the transcription factor NFκB. Int. Rev. Neurobiol., 49, 103–68CrossRefGoogle Scholar
Mattson, M. P. & Kater, S. B. (1987). Calcium regulation of neurite elongation and growth cone mobility. J. Neurosci., 7, 4034–43CrossRefGoogle Scholar
Mattson, M. P., Rychlik, B., Chu, C. & Christakos, S. (1991). Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron, 6, 41–51CrossRefGoogle ScholarPubMed
McMahon, A., , Wong, B. S., Iacopino, A. M., Ng, M. C., Chi, S. & German, D. C. (1998). Calbindin-D28k buffers intracellular calcium and promotes resistance to degeneration in PC12 cells. Mol. Brain Res., 54, 56–63CrossRefGoogle Scholar
McRitchie, D. A. & Halliday, G. M. (1995). Calbindin D28k-containing neurons are restricted to the medial substantia nigra in humans. Neuroscience, 65, 87–91CrossRefGoogle ScholarPubMed
Means, A. R., Tash, J. S. & Chafouleas, J. G. (1982). Physiological implications of the presence, distribution and regulation of calmodulin in eukaryotic cells. Physiol. Rev., 62, 1–39CrossRefGoogle ScholarPubMed
Meldolesi, J. (2001). Rapidly exchanging Ca2+ stores in neurons: molecular, structural and functional properties. Prog. Neurobiol., 65, 309–38CrossRefGoogle ScholarPubMed
Michaelson, D. M., Ophir, I. & Angel, I. (1980). ATP-stimulated Ca2+ transport into cholinergic Torpedo synaptic vesicles. J. Neurochem., 35, 116–24CrossRefGoogle ScholarPubMed
Migheli, A., Cordera, S., Bendotti, C., Atzori, C., Piva, R. & Schiffer, D. (1999). S-100Β protein is upregulated in astrocytes and motor neurons in the spinal cord of patients with amyotrophic lateral sclerosis. Neurosci. Lett., 261, 25–8CrossRefGoogle ScholarPubMed
Miller, R. J. (1995). Regulation of calcium homeostasis in neurons: the role of calcium-binding proteins. Biochem. Soc. Trans., 23, 629–32CrossRefGoogle ScholarPubMed
Miller, R. J. (1998). Mitochondria – the Kraken wakes!Trends Neurosci., 21, 95–7CrossRefGoogle ScholarPubMed
Mogami, H., Nakano, K., Tepikin, A. V. & Petersen, O. H. (1997). Ca2+ flow via tunnels in polarized cells: recharging of apical Ca2+ stores by focal Ca2+ entry through basal membrane patch. Cell, 88, 49–55CrossRefGoogle ScholarPubMed
Morrison, B. M., Janssen, W. G., Gordon, J. W. & Morrison, J. H. (1998). Light and electron microscopic distribution of the AMPA receptor subunit GluR2 in the spinal cord of control and G86R mutant superoxide dismutase transgenic mice. J. Comp. Neurol., 395, 523–343.0.CO;2-3>CrossRefGoogle ScholarPubMed
Mosier, D. R., Baldelli, P., Delbono, O.et al. (1995). Amyotrophic lateral sclerosis immunoglobulins increase Ca2+ currents in a motoneuron cell line. Ann. Neurol., 37, 102–9CrossRefGoogle Scholar
Mosier, D. R., Siklós, L. & Appel, S. H. (2000). Resistance of extraocular motoneuron terminals to effects of amyotrophic lateral sclerosis sera. Neurology, 54, 252–5CrossRefGoogle ScholarPubMed
Murphy, A. N., Fiskum, G. & Beal, M. F. (1999). Mitochondria in neurodegeneration: Bioenergetic function in cell life and death. J. Cereb. Blood Flow Metab., 19, 231–45CrossRefGoogle ScholarPubMed
Neher, E., & Augustine, G. J. (1992). Calcium gradients and buffers in bovine chromaffin cells. J. Physiol., 450, 273–301CrossRefGoogle Scholar
Nicotera, P. & Orrenius, S. (1998). The role of calcium in apoptosis. Cell Calcium, 23, 173–80CrossRefGoogle ScholarPubMed
Obál, I. (2002). Immune-mediated damages and the role of intracellular calcium homeostasis in the degeneration of neurons. PhD Thesis, University of Szeged, Hungary
Parvizi, J. & Damasio, A. R. (2003). Differential distribution of calbindin D28k and parvalbumin among functionally distinctive sets of structures in the macaque brainstem. J. Comp. Neurol., 462, 153–67CrossRefGoogle ScholarPubMed
Paschen, W. & Doutheil, J. (1999). Disturbances of the functioning of endoplasmic reticulum: a key mechanism underlying neuronal cell injury?J. Cereb. B F Metab., 19, 1–18CrossRefGoogle ScholarPubMed
Potier, B., Krzywkowski, P., Lamour, Y. & Dutar, P. (1994). Loss of calbindin-immunoreactivity in CA1 hippocampal stratum radiatum and lacunosum-moleculare interneurons in the aged rat. Brain Res., 661, 181–8CrossRefGoogle ScholarPubMed
Pozzan, T., Rizzuto, R., Volpe, P. & Meldolesi, J. (1994). Molecular and cellular physiology of intracellular calcium stores. Physiol. Rev., 74, 595–636CrossRefGoogle ScholarPubMed
Pramatarova, A., Laganiere, J., Roussel, J., Brisebois, K. & Rouleau, G. A. (2001). Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J. Neurosci., 21, 3369–74CrossRefGoogle Scholar
Puchalski, R. B., Louis, J. C., Brose, N.et al. (1994). Selective RNA editing and subunit assembly of native glutamate receptor. Neuron, 13, 131–47CrossRefGoogle Scholar
Pullen, A. H., Demestre, M., Howard, R. S. & Orrell, R. W. (2004). Passive transfer of purified IgG from patients with amyotrophic lateral sclerosis to mice results in degeneration of motor neurons accompamied by Ca2+ enhancement. Acta Neuropathol., 107, 35–46CrossRefGoogle Scholar
Pullen, A. H. & Humphreys, P. (2000). Ultrastructural analysis of spinal motoneurons from mice treated with IgG from ALS patients, healthy individuals, or disease controls. J. Neurol. Sci., 180, 35–45CrossRefGoogle ScholarPubMed
Rami, A., Rabié, A., Thomasset, M. & Krieglstein, J. (1992). Calbindin-D28K and ischemic damage of pyramidal cells in rat hippocampus. J. Neurosci. Res., 31, 89–95CrossRefGoogle ScholarPubMed
Reaume, A. G., Elliott, J. L., Hoffman, E. K., et al. (1996). Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet., 13, 43–7CrossRefGoogle ScholarPubMed
Reiner, A., Medina, L., Figueredo-Cardenas, G. & Anfinson, S. (1995). Brainstem motoneuron pools that are selectively resistant in amyotrophic lateral sclerosis are preferentially enriched in parvalbumin: Evidence from monkey brainstem for a calcium-mediated mechanism in sporadic ALS. Exp. Neurol., 131, 239–50CrossRefGoogle ScholarPubMed
Ren, K. & Ruda, M. A. (1994). A comparative study of the calcium-binding proteins calbindin-D28K, calretinin, calmodulin and parvalbumin in the rat spinal cord. Brain Res. Rev., 19, 163–79CrossRefGoogle ScholarPubMed
Robb-Gaspers, L. D., Rutter, G. A., Burnett, P., Hajnóczky, G., Denton, R. M. & Thomas, A. P. (1998). Coupling between cytosolic and mitochondrial calcium oscillations: role in the regulation of hepatic metabolism. Biochim. Biophys. Act., 1366, 17–32CrossRefGoogle ScholarPubMed
Rothermundt, M., Peters, M., Prehn, J. H. & Arolt, V. (2003). S100B in brain damage and neuro-degeneration. Microsc. Res. Tech., 60, 614–32CrossRefGoogle Scholar
Rothstein, J. D. (1995). Excitotoxic mechanisms in the pathogenesis of amyotrophic lateral sclerosis. Adv. Neurol., 68, 7–20Google ScholarPubMed
Rowland, L. P. (2000). Six important themes in amyotrophic lateral sclerosis (ALS) research, 1999. J. Neurol. Sci., 180, 2–6CrossRefGoogle Scholar
Rowland, L. P. & Shneider, N. A. (2001). Amyotrophic lateral sclerosis. N. Engl. J. Med., 344, 1688–700CrossRefGoogle ScholarPubMed
Roy, J., Minotti, S., Dong, L., Figlewicz, D. A. & Durham, H. D. (1998). Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by post-synaptic calcium-dependent mechanisms. J. Neurosci., 18, 9673–84CrossRefGoogle Scholar
Sattler, R. & Tymianski, M. (2000). Molecular mechanisms of calcium-dependent excitotoxicity. J. Mol. Med., 78, 3–13CrossRefGoogle ScholarPubMed
Schapira, A. H. V. (1998). Mitochondrial dysfunction in neurodegenerative disorders. Biochim. Biophys. Act., 1366, 225–33CrossRefGoogle ScholarPubMed
Schubert, P., Ogata, T., Marchini, C. & Ferroni, S. (2001). Glia-related pathomechanisms in Alzheimer's disease: a therapeutic target?Mech. Ageing Dev., 123, 47–57CrossRefGoogle ScholarPubMed
Shaw, P. J. & Eggett, C. J. (2000). Molecular factors underlying selective vulnerability of motor neurons to degeneration in amyotrophic lateral sclerosis. J. Neurol., 247(suppl 1), 17–27CrossRefGoogle ScholarPubMed
Siesjö, B. K., Hu, B. & Kristián, T. (1999). Is the cell death pathway triggered by the mitochondrion or the endoplasmic reticulum?J. Cereb. Blood Flow Metab., 19, 19–26CrossRefGoogle ScholarPubMed
Siklós, L., Engelhardt, J., Harati, Y., Smith, R. G., Joó, F. & Appel, S. H. (1996). Ultrastructural evidence for altered calcium in motor nerve terminals in amyotrophic lateral sclerosis. Ann. Neurol., 39, 203–16CrossRefGoogle Scholar
Siklós, L., Engelhardt, J. I., Alexianu, M. E., Gurney, M. E., Siddique, T. & Appel, S. H. (1998). Intracellular calcium parallels motor neuron degeneration in SOD-1 mutant mice. J. Neuropathol. Exp. Neurol., 57, 571–87CrossRefGoogle ScholarPubMed
Siklós, L., Engelhardt, J. I., Adalbert, R. & Appel, S. H. (1999). Calcium-containing endosomes at oculomotor terminals in animal models of ALS. NeuroReport, 10, 2539–45CrossRefGoogle ScholarPubMed
Siklós, L., Engelhardt, J. I., Reaume, A. G.et al. (2000). Altered calcium homeostasis in spinal motoneurons but not in oculomotor neurons of SOD-1 knockout mice. Acta Neuropathol., 99, 517–24Google Scholar
Smith, R. G., Hamilton, S., Hofmann, F.et al. (1992). Serum antibodies to L-type calcium channels in patients with amyotrophic lateral sclerosis. N. Engl. J. Med., 327, 1721–8CrossRefGoogle ScholarPubMed
Smith, R. G., Alexianu, M. E., Crawford, G., Nyormoi, O., Stefani, E. & Appel, S. H. (1994). The cytotoxicity of immunoglobulins from amyotrophic lateral sclerosis patients on an hybrid motoneuron cell line. Proc. Natl Acad. Sci., USA, 91, 3393–7CrossRefGoogle ScholarPubMed
Suarez-Isla, B. A., Pelto, D. J., Thompson, J. M. & Rapoport, S. I. (1984). Blockers of calcium permeability inhibit neurite extension and formation of neuromuscular synapses in cell culture. Dev. Brain Res., 14, 263–70CrossRefGoogle Scholar
Swash, M. & Schwartz, M. S. (1995). Motor neuron disease: the clinical syndrome. In Motor Neuron Disease. Biology and Management, ed. P. N. Leigh & M. Swash. London, Berlin, Heidelberg, New York, Paris, Tokyo, Hong Kong, Barcelona, Budapest: Springer-Verlag. pp. 1–17CrossRef
Takei, K., Mundigl, O., Daniell, L. & Camilli, P. (1996). The synaptic vesicle cycle: A single vesicle budding step involving clathrin and dynamin. J. Cell. Biol., 133, 1237–50CrossRefGoogle ScholarPubMed
Takuma, H., Kwak, S., Yoshizawa, T. & Kanazawa, I. (1999). Reduction of GluR2 RNA editing, a molecular change that increases calcium influx through AMPA receptors, selective in the spinal ventral gray of patients with amyotrophic lateral sclerosis. Ann. Neurol., 46, 806–153.0.CO;2-S>CrossRefGoogle ScholarPubMed
Trotti, D., Rolfs, A., Danbolt, N. C., Brown, R. H. Jr & Hediger, M. A. (1999). SOD1 mutant linked amyotrophic lateral sclerosis selectively inactivate a glial glutamate transporter. Nat. Neurosci., 2, 427–33CrossRefGoogle ScholarPubMed
Tortosa, A. & Ferrer, I. (1993). Parvalbumin immunoreactivity in the hippocampus of the gerbil after transient forebrain ischaemia: a qualitative and quantitative sequential study. Neuroscience, 55, 33–43CrossRefGoogle ScholarPubMed
Tsuboi, K., Kimber, T. A. & Shults, C. W. (2000). Calretinin-containing axons and neurons are resistant to an intrastriatal 6-hydroxydopamine lesion. Brain Res., 866, 55–64CrossRefGoogle Scholar
Tymianski, M., Charlton, M. P., Carlen, P. L. & Tator, C. H. (1993). Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J. Neurosci., 13, 2085–114CrossRefGoogle ScholarPubMed
Vandenberghe, W., Robberecht, W. & Brorson, J. R. (2000). AMPA receptor calcium permeability, GluR2 expression, and selective motoneuron vulnerability. J. Neurosci., 20, 123–32CrossRefGoogle ScholarPubMed
Vandenberghe, W., Bindokas, V. P., Miller, R. J.et al. (2001). Subcellular localization of calcium permeable AMPA receptors in spinal motor neurons. Eur. J. Neurosci., 14, 305–14CrossRefGoogle Scholar
Bosch, L., Vandenberghe, W., Klaassen, H.et al. (2000). Ca2+-permeable AMPA receptors and selective vulnerability of motor neurons. J. Neurol. Sci., 180, 29–34CrossRefGoogle Scholar
Bosch, L., Schwaller, B., Vleminckx, V.et al. (2002). Protective effect of parvalbumin on excitotoxic motor neuron death. Exp. Neurol., 174, 150–61CrossRefGoogle Scholar
Vanselow, B. K. & Keller, B. U. (2000). Calcium dynamics and buffering in oculomotor neurones from mouse that are particularly resistant during amyotrophic lateral sclerosis (ALS)-related motoneurone disease. J. Physiol., 525, 433–45CrossRefGoogle ScholarPubMed
Verkhratsky, A. & Toescu, E. C. (1998). Calcium and neuronal ageing. Trends Neurosci., 21, 2–7CrossRefGoogle ScholarPubMed
Vig, P. J. S., Subramony, S. H., Burright, E. N.et al. (1998). Reduced immunoreactivity to calcium binding proteins in Purkinje cells precedes onset of ataxia in spinocerebellar ataxia-1 transgenic mice. Neurology, 50, 106–13CrossRefGoogle ScholarPubMed
Villa, A., Podini, P., Panzeri, M. C., Racchetti, G. & Meldolesi, J. (1994). Cytosolic Ca2+ binding proteins during rat brain ageing: Loss of calbindin and calretinin in the hippocampus, with no change in the cerebellum. Eur. J. Neurosci., 6, 1491–9CrossRefGoogle ScholarPubMed
Gersdorff, H. & Matthews, G. (1994). Inhibition of endocytosis by elevated internal calcium in synaptic terminal. Nature, 370, 652–5CrossRefGoogle Scholar
Waisman, D. M., Smallwood, J. I., Lafreniere, D., & Rasmussen, H., (1983). Identification of novel calcium-binding proteins of heart and brain 1000,000 x G supernatant. Biochem. Biophys. Res. Commun., 116, 435–41CrossRefGoogle Scholar
Werth, J. L. & Thayer, S. A. (1994). Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons. J. Neurosci., 14, 348–56CrossRefGoogle ScholarPubMed
Williams, T. L., Day, N. C., Ince, P. G.et al. (1997). Calcium-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazole proprionic acid receptors: a molecular determinant of selective vulnerability in amyotrophic lateral sclerosis. Ann. Neurol., 42, 200–7CrossRefGoogle Scholar
Winsky, L. & Kuznicki, J. (1996). Antibody recognition of calcium-binding proteins depends on their calcium-binding status. J. Neurochem., 66, 764–71CrossRefGoogle ScholarPubMed
Yamada, T., McGeer, P. L., Baimbridge, K. G. & McGeer, E. G. (1990). Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28k. Brain Res., 526, 303–7CrossRefGoogle ScholarPubMed
Yap, K. L., Ames, J. B., Swindells, M. B. & Ikura, M., (1999). Diversity of conformational states and changes within the EF-hand protein superfamily. Proteins, 37, 499–5073.0.CO;2-Y>CrossRefGoogle ScholarPubMed

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