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The Cerebellum

, Volume 2, Issue 4, pp 242–262 | Cite as

Distribution of calcium-binding proteins in the cerebellum

  • Enrico BastianelliEmail author
Scientific Papers

Abstract

Calcium plays a fundamental role in the cell as second messenger and is principally regulated by calcium-binding proteins. Although these proteins share in common their ability to bind calcium, they belong to different subfamilies. They present, in general, specific developmental and distribution patterns. Most Purkinje cells express the fast and slow calcium buffer proteins calbindin-D28k and parvalbumin, whereas basket, stellate and Golgi cells the slow buffer parvalbumin only. They are, almost all, calretinin negative. Granule, Lugaro and unipolar brush cells present an opposite immunoreactivity profile, most of them being calretinin positive while lacking calbindin-D28k and parvalbumin. The developmental pattern of appearance of these proteins seems to follow the maturation of neurons. Calbindin-D28k appears early, shortly after cessation of mitosis when neurons become ready to start migration and differentiation while parvalbumin is expressed later in parallel with an increase in neuronal activity. The other proteins are generally detected later. During development, some of these proteins, like calretinin, are transiently expressed in specific cellular subpopulations. The function of these proteins is not fully understood, although strong evidence supports a prominent role in physiological settings with altered calcium concentrations. These proteins regulate and are regulated by intracellular calcium level. For example, they may directly or indirectly enable sensitization or desensitization of calcium channels, and may further block calcium entry into the cells, like the calcium-sensor proteins, that have been shown to be potent and specific modulators of ion channels, which may allow for feedback control of current function and hence signaling. The absence of calcium buffer proteins results in marked abnormalities in cell firing; with alterations in simple and complex spikes or transformation of depressing synapses into facilitating synapses. Calcium-binding protein implication in resistance to degeneration is still a controversial issue. Neurons rich in calcium-binding proteins, especially calbindin-D28k and parvalbumin, seem to be relatively resistant to degeneration in a variety of acute and chronic disorders. However other data support that an absence of calcium-binding proteins may also have a neuroprotective effect. It is not unlikely that neurons may face a dual action mechanism where a decrease in calcium-binding proteins has a first short-term beneficial effect while it becomes detrimental for the cell over the long term.

Keywords

calcium calcium-binding proteins cerebellum Purkinje cells 

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References

  1. 1.
    Evenas J, et al. Calcium. Cur Opinion in Chem Biol 1998; 2: 293–302.Google Scholar
  2. 2.
    Carafoli E. Intracellular calcium homeostasis. Annu Rev Biochem 1987; 56: 395–433.PubMedGoogle Scholar
  3. 3.
    Meldolesi J, Pozzan T. The endoplasmic reticulum Ca2+ store: a view from the lumen. Trends in Biochem. Sci 1998; 23: 10–14.Google Scholar
  4. 4.
    Krebs J. The role of calcium in apoptosis. BioMetals 1998; 11: 375–382.PubMedGoogle Scholar
  5. 5.
    Kawasaki H, et al. Classification and evolution of EF-hand proteins. BioMetals 1998; 11: 277–295.PubMedGoogle Scholar
  6. 6.
    Sallese M, et al. Regulation of G protein-coupled receptor kinase subtypes by calcium sensor proteins. Biochim Biophys Acta 2000; 1498: 112–121.PubMedGoogle Scholar
  7. 7.
    Ni B, et al. Molecular cloning of calmodulin mRNA species which are preferentially expressed in neurons of the rat brain. Mol Brain Res 1992; 13: 7–13.PubMedGoogle Scholar
  8. 8.
    Agell N, et al. New nuclear functions for calmodulin. Cell Calcium 1998; 23: 115–121.PubMedGoogle Scholar
  9. 9.
    Gruver CL, et al. Targeted developmental overexpression of calmodulin induces proliferative and hypertrophic growth of cardiomyocytes in transgenic mice. Endocrinology 1993; 133: 376–388.PubMedGoogle Scholar
  10. 10.
    Goodman M, et al. Evolutionary diversification of structure and function in the family of intracellular calcium-binding proteins. J Mol Evol 1979; 13: 331–352.PubMedGoogle Scholar
  11. 11.
    Parmentier M. Structure of the human cDNAs and genes coding for calbindin D28K and calretinin. Adv Exp Med Biol 1990; 269: 27–34.PubMedGoogle Scholar
  12. 12.
    Jande SS, et al. Immunohistochemical mapping of vitamin D-dependent calcium-binding protein in Brain. Nature 1981; 294: 765–767.PubMedGoogle Scholar
  13. 13.
    Garcia-Segura LM, et al. Immunohistochemical mapping of calcium-binding protein in the rat central nervous system. Brain Res 1984; 296: 75–86.PubMedGoogle Scholar
  14. 14.
    Rogers JH. Two calcium-binding proteins mark many chick sensory neurons. Neuroscience 1989; 31: 697–709.PubMedGoogle Scholar
  15. 15.
    Heizmann CW. Ca2+-binding S100 proteins in the central nervous system. Neurochem. Res 1999; 24: 1097–1100.PubMedGoogle Scholar
  16. 16.
    Schäfer BW, Heizmann CW. The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends in Biochem Sci 1996; 21: 134–140.Google Scholar
  17. 17.
    Garbuglia M, et al. The calcium-modulated proteins, S100A1 and S100B, as potential regulators of the dynamics of type III intermediate filaments. Braz J Med Biol Res 1999; 32: 1177–1185.PubMedGoogle Scholar
  18. 18.
    Dizhoor AM, et al. Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase. Science 1991; 251: 915–918.PubMedGoogle Scholar
  19. 19.
    Braunewell KH, Gundelfinger ED. Intracellular neuronal calcium sensor proteins: a family of EF-hand calcium-binding proteins in search of a function. Cell Tiss Res 1999; 295: 1–12.Google Scholar
  20. 20.
    Iacovelli L, et al. Regulation of G-protein-coupled receptor kinase subtypes by calcium sensor proteins. Fedn Am Socs Exp Biol 1999; 13: 1–8.Google Scholar
  21. 21.
    Tatu U, Helenius A. Interactions between newly synthesized glycoproteins, calnexin and a network of resident chaperones in the endoplasmic reticulum. J Cell Biol 1997; 136: 555–565.PubMedGoogle Scholar
  22. 22.
    Coppolino MG, Dedhar S, Calreticulin. Int J. Biochem Cell Biol 1998; 30: 553–558.PubMedGoogle Scholar
  23. 23.
    Ozawa M, Muramatsu T. Reticulocalbin, a novel endoplasmic reticulum resident Ca(2+)-binding protein with multiple EF-hand motifs and a carboxyl-terminal HDEL sequence. J Biol Chem 1993; 268: 699–705.PubMedGoogle Scholar
  24. 24.
    Weis K, et al. The endoplasmic reticulum calcium-binding protein of 55 kD is a novel EF-hand protein retained in the endoplasmic reticulum by a carboxyl-terminal His-Asp-Glu-Leu motif. J Biol Chem 1994; 269: 19142–19150.PubMedGoogle Scholar
  25. 25.
    Hseu MJ, et al. Crocalbin: a new calcium-binding protein that is also a binding protein for crotoxin, a neurotoxic phospholipase A2. FEBS Lett 1999; 445: 440–444.PubMedGoogle Scholar
  26. 26.
    Scherer PE, et al. Cab45, a novel (Ca2+)-binding protein localized to the Golgi lumen. J Cell Biol 1996; 133: 257–268.PubMedGoogle Scholar
  27. 27.
    Yabe D, et al. Calumenin, a Ca2+-binding protein retained in the endoplasmic reticulum with a novel carboxyl-terminal sequence, HDEF. J Biol Chem 1997; 272: 18232–18239.PubMedGoogle Scholar
  28. 28.
    Kent J, et al. The reticulocalbin gene maps to the WAGR region in human and to the Small eye Harwell deletion in mouse. Genomics 1997; 42: 260–267.PubMedGoogle Scholar
  29. 29.
    Beckingham K, et al. Calcium-binding proteins and development. BioMetals 1998; 11: 359–373.PubMedGoogle Scholar
  30. 30.
    Sotelo C, Chedotal A. Development of the olivocerebellar projection. Persp on Dev Neurobiol 1997; 5: 57–67.Google Scholar
  31. 31.
    Braak E, Braak H. The new monodendritic neuronal type within the adult human cerebellar granule cell layer shows calretininimmunoreactivity. Neurosci Lett 1993; 154: 199–202.PubMedGoogle Scholar
  32. 32.
    Diño M, et al. Distribution of unipolar brush cells and other calretinin immunoreactive components in the mammalian cerebellar cortex. J Neurocytology 1999; 28: 99–123.Google Scholar
  33. 33.
    Résibois A, Rogers JH. Calretinin in rat brain: an immunohistochemical study. Neuroscience 1992; 46: 101–134.PubMedGoogle Scholar
  34. 34.
    De Castro F, et al. Calretinin in pretecto and olivocerebellar projections in the chick: immunohistochemical and experimental study. J Comp Neurol 1998; 397: 149–162.PubMedGoogle Scholar
  35. 35.
    Lenz SE, et al. Localization of the neural calcium-binding protein VILIP (visinin-like protein) in neurons of the chick visual system and cerebellum. Cell Tiss Res 1996; 283: 413–424.Google Scholar
  36. 36.
    Yan X, Garey LJ. Complementary distributions of calbindin, parvalbumin and caretinin in the cerebellar vermis of the adult cat. J Brain Res 1998; 1: 9–14.Google Scholar
  37. 37.
    Jaarsma D, et al. Cerebellar choline acetyltransferase positive mossy fibres and their granule and unipolar brush cell targets: a model for central cholinergic nicotinic neurotransmission. J Neurocytology 1996; 25: 829–842.Google Scholar
  38. 38.
    Lin CT, et al. Localization of calmodulin in rat cerebellum by immunoelectron microscopy. J Cell Biol 1980; 85: 473–480.PubMedGoogle Scholar
  39. 39.
    Goto S, et al. A comparative immunohistochemical study of calcineurin and S-100 protein in mammalian and avian brains. Exp Brain Res 1988; 69: 645–650.PubMedGoogle Scholar
  40. 40.
    Messer A, et al. Staggerer mutant mouse Purkinje cells do not contain detectable calmodulin mRNA. J Neurochem 1990; 55: 293–302.PubMedGoogle Scholar
  41. 41.
    Lal S, et al. Immunohistochemical localization of calmodulindependent cyclic phosphodiesterase in the human brain. Neurochem Res 1999; 24: 43–49.PubMedGoogle Scholar
  42. 42.
    Scotti AL, Nitsch C. Differential Ca2+ binding properties in the human cerebellar cortex: distribution of parvalbumin and calbindin D-28k immunoreactivity. Anat Embryol 1992; 185: 163–167.PubMedGoogle Scholar
  43. 43.
    Celio MR. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 1990; 35: 375–475.PubMedGoogle Scholar
  44. 44.
    Fortin M, et al. Calcium-binding proteins in primate cerebellum. Neuroscience Res 1998; 30: 155–168.Google Scholar
  45. 45.
    Rickmann M, Wolff JR. S100 protein expression in subpopulations of neurons of rat brains. Neuroscience 1995; 67: 977–991.PubMedGoogle Scholar
  46. 46.
    Paterlini M, et al. Expression of the neuronal calcium sensor protein family in the rat brain. Neuroscience 2000; 99: 205–216.PubMedGoogle Scholar
  47. 47.
    Saitoh S, et al. Distribution of hippocalcin mRNA and immunoreactivity in rat brain. Neurosci Lett 1993; 171: 155–158.Google Scholar
  48. 48.
    Spilker C, et al. The neuronal EF-hand calcium-binding protein visinin-like protein-3 is expressed in cerebellar Purkinje cells and shows a calcium-dependent membrane association. Neuroscience 2000; 96: 121–129.PubMedGoogle Scholar
  49. 49.
    Alonso JR, et al. Parvalbumin immunoreactive neurons and fibres in the teleost cerebellum. Anat Embryol 1992; 185: 355–361.PubMedGoogle Scholar
  50. 50.
    Nieuwenhuys R, et al. The neuronal organization of cerebellar lobe C1 in the mormyrid fish Gnathonemus petersii (Teleostei). Z Anat Entwicklungsgesch 1974; 144: 315–336.PubMedGoogle Scholar
  51. 51.
    Arai R, et al. Ultrastructural localization of calretinin immunoreactivity in lobule V of the rat cerebellum. Brain Res 1993; 613: 300–304.PubMedGoogle Scholar
  52. 52.
    Filipek A, et al. Calcyclin—Ca(2+)-binding protein homologous to glial S-100 beta is present in neurones. NeuroReport 1993; 4: 383–386.PubMedGoogle Scholar
  53. 53.
    Bastianelli E, Pochet R. Transient expression of calretinin during development of chick cerebellum. Neurosci Res 1993; 17: 53–61.PubMedGoogle Scholar
  54. 54.
    Lenz SE, et al. VILIP, a cognate protein of the retinal calciumbinding proteins visinin and recoverin, is expressed in the developing chicken brain. Mol Brain Res 1992; 15: 133–140.PubMedGoogle Scholar
  55. 55.
    Nakamura TY, et al. A role for frequenin, a CA2+-binding protein, as a regulator of Kv4 K+-currents. PNAS 2001; 98 (22): 12808–12813.PubMedGoogle Scholar
  56. 56.
    Marr DA. A theory of cerebellar cortex. J Physiol 1969; 202: 437–470.PubMedGoogle Scholar
  57. 57.
    De Schutter E, et al. The function of cerebellar Golgi cells revisited. Progress in Brain Res 2000; 124: 81–93.Google Scholar
  58. 58.
    Edgley SA, Lidierth M. The discharge of cerebellar Golgi cells during locomotion in the cat. J Physiol 1987; 392: 315–332.PubMedGoogle Scholar
  59. 59.
    Lainé J, Axelrad H. Lugaro cells target basket and stellate cells in the cerebellar cortex. NeuroReport 1998; 9: 2399–2403.PubMedGoogle Scholar
  60. 60.
    Bishop GA, et al. An analysis of GABAergic afferents to basket cell bodies in the cat’s cerebellum. Brain Res 1993; 623: 293–298.PubMedGoogle Scholar
  61. 61.
    Ito M. The Cerebellum and Neural Control. New York: Raven Press, 1984.Google Scholar
  62. 62.
    Axelrad H, Korn H. Electrical inhibition of Purkinje cells in the cerebellum of the rat. Proc Natl Acad Sci USA 1980; 77: 6244–6247.PubMedGoogle Scholar
  63. 63.
    Martone ME, et al. Cellular and subcellular distribution of the calcium-binding protein NCS-1 in the central nervous system of the rat. Cell Tiss Res 1999; 295: 395–407.Google Scholar
  64. 64.
    Marini A, et al. Calretinin-containing neurons in rat cerebellar granule cell cultures. Brain Res Bull 1997; 42: 279–288.PubMedGoogle Scholar
  65. 65.
    Dino M, et al. Unipolar brush cell: a potential feedforward excitatory interneuron of the cerebellum. Neuroscience 2000; 98: 625–636.PubMedGoogle Scholar
  66. 66.
    Yew DT, et al. Differential expression of calretinin, calbindin D28K and parvalbumin in the developing human cerebellum. Dev Brain Res 1997; 103: 37–45.Google Scholar
  67. 67.
    Milosevic A, Zecevic N. Developmental changes in human cerebellum: expression of intracellular calcium receptors, calcium-binding proteins, and phosphorylated and nonphosphorylated neurofilament protein. J Comp Neurol 1998; 396: 442–460.PubMedGoogle Scholar
  68. 68.
    Ghandour MS, et al. A biochemical and immunohistological study of S100 protein in developing rat cerebellum. Dev Neurosci 1981; 4: 98–109.PubMedGoogle Scholar
  69. 69.
    Tapas C, et al. Calbindin immunoreactivity in the developing and adult human cerebellum. J Chem Neuroanatomy 1999; 17: 1–12.Google Scholar
  70. 70.
    Yu MC, et al. Immunohistochemical studies of gaba and parvalbumin in the developing human cerebellum. Neuroscience 1996; 70: 267–276.PubMedGoogle Scholar
  71. 71.
    Enderlin S, et al. Ontogeny of the calcium-binding protein calbindin D-28k in the rat nervous system. Anat Embryol 1987; 177: 15–28.PubMedGoogle Scholar
  72. 72.
    Endo T, et al. Parvalbumin in rat cerebrum, cerebellum and retina during postnatal devlopment. Neurosci Lett 1985; 60: 279–282.PubMedGoogle Scholar
  73. 73.
    Hendrickson AE, et al. Development of the calcium-binding proteins parvalbumin and calbindin in monkey striate cortex. J Comp Neurol 1991; 307: 626–646.PubMedGoogle Scholar
  74. 74.
    Airman J. Autoradiographic and histological studies of postnatal neurogenesis. III. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 1969; 136: 269–294.Google Scholar
  75. 75.
    Clemens TL, et al. Tissue-specific regulations of avian vitamin D-dependent calcium binding protein 28 kDa mRNA by 1,25 dihydroxy vitamin D3. J Biol Chem 1988; 263: 13112–13116.PubMedGoogle Scholar
  76. 76.
    Airman J. Postnatal development of cerebellar cortex in the rat. J Comp Neurol 1972; 145: 353–464.Google Scholar
  77. 77.
    Saitoh S, et al. Expression of hippocalcin in the developing rat brain. Dev Brain Res 1994; 80: 199–208.Google Scholar
  78. 78.
    Arnold D, Heintz N. a calcium responsive element that regulates expression of two calcium binding proteins in Purkinje cells. PNAS 1997; 94: 8842–8847.PubMedGoogle Scholar
  79. 79.
    Treisman R. Journey to the surface of the cell: fos regulation and the SRE. EMBO J 1995; 14: 4905–4913.PubMedGoogle Scholar
  80. 80.
    Mugnaini E. In: Llinas R, editor. Neurobiology of cerebellar evolution and development. Chicago: American Medical Association Education Research Fund, 1969: 749–782.Google Scholar
  81. 81.
    Bertossi M, et al. Process of differentiation of cerebellar Purkinje neurons in the chick embryo. Anat Embryol 1986; 175: 25–34.PubMedGoogle Scholar
  82. 82.
    Porteros A, et al. Parvalbumin immunoreactivity during the development of the cerebellum of the rainbow trout. Dev Brain Res 1998; 109: 221–227.Google Scholar
  83. 83.
    Cimino M, et al. Ontogenetic development of calmodulin mRNA in rat brain using in situ hybridization histochemistry. Brain Res 1990; 54: 43–49.Google Scholar
  84. 84.
    Celio M. Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat Embryol 1991; 184: 103–124.PubMedGoogle Scholar
  85. 85.
    Bell CC, Dow RS. Cerebellar circuitry. Neuro Sci Res Prog Bull 1967; 5: 121–222.Google Scholar
  86. 86.
    Abbott LC, Jacobowitz DM. Development of calretinin-immunoreactive unipolar brush-like cells and an afferent pathway to the embryonic and early postnatal mouse cerebellum. Anat Embryol 1995; 191: 541–559.PubMedGoogle Scholar
  87. 87.
    West AE, et al. Calcium regulation of neuronal gene expression. PNAS 2001; 98 (20): 11024–11031.PubMedGoogle Scholar
  88. 88.
    Boukhaddaoui H, et al. Q and L-type calcium channels control the development of calbindin phenotype in hippocampal pyramidal neurons in vitro. Eur J Neurosci 2000; 12: 2068–2078.PubMedGoogle Scholar
  89. 89.
    Dove LS, et al. Altered calcium homeostasis in cerebellar Purkinje cells of Leaner mutant mice. J Neurophysiol 2000; 84: 513–524.PubMedGoogle Scholar
  90. 90.
    Baurle J, et al. Dependence of parvalbumin expression on Purkinje cell input on the deep cerebellar nuclei. J Comp Neurol 1998; 392: 499–514.PubMedGoogle Scholar
  91. 91.
    Zhuchenko O, et al. Autosomal dominant cerebellar ataxia (SCA6) associated with small polyglutamine expansions in the alpha 1A-voltage-dependent calcium channel. Nat Genet 1997; 15: 62–69.PubMedGoogle Scholar
  92. 92.
    Vig PJS, et al. The effect of calbindin D-28K and the parvalbumin antisense oligonucleotides on the survival of cultured Purkinje cells. Res Com Mol Pathol Pharmacol 1999; 103: 249–259.Google Scholar
  93. 93.
    Vig PJS, et al. Reduced immunoreactivity to calcium-binding proteins in Purkinje cells precedes onset of ataxia in spinocerebellar ataxin-1 transgenic mice. Neurology 1998; 50: 106–113.PubMedGoogle Scholar
  94. 94.
    Batini C, et al. Upregulation of calbindin-D28k immunoreactivity by excitatory aminoacids. Arch Ital Biol 1997; 135: 385–397.PubMedGoogle Scholar
  95. 95.
    Rico B, et al. TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat. Neurosci 2000; 5: 225–233.Google Scholar
  96. 96.
    Fiumelli H, et al. Opposite regulation of calbindin and calretinin expression by brain-derived neurotrophic factor in cortical neurons. J Neurochem 2000; 74: 1870–1877.PubMedGoogle Scholar
  97. 97.
    Du J, et al. Activity and Ca2+ dependent modulation of surface expression of brain-derived neurotrophic factors in hippocampal neurons. J Cell Biol 2000; 150: 1423–1433.PubMedGoogle Scholar
  98. 98.
    Gross M, Kumar R. Physiology and biochemistry of vitamin D-dependent calcium binding proteins. Am J Physiol 1990; 259: F195–209.PubMedGoogle Scholar
  99. 99.
    Sechman A, et al. Tissue-specific expression of calbindin-D28K gene during ontogeny of the chicken. J Exp Zool 1994; 269: 450–457.PubMedGoogle Scholar
  100. 100.
    Matsumoto K, et al. Role of retinoic acid in regulation of mRNA expression of CaBP-D28K in the cerebellum of the chicken. Comp Biochem Physiol 1998; 120: 237–242.Google Scholar
  101. 101.
    Lephart ED, et al. Brain androgen and progesterone metabolizing enzymes: biosynthesis, distribution and function. Brain Res Dev Brain Res Rev 2001; 37: 25–37.Google Scholar
  102. 102.
    Joels M. Steroid hormones and excitability in the mammalian brain. Front Neuroendocrinol 1997; 18: 2–48.PubMedGoogle Scholar
  103. 103.
    Arnold DB, Heintz N. A calcium responsive element that regulates expression of two calcium binding-proteins in Purkinje cells. PNAS 1997; 94: 8842–8847.PubMedGoogle Scholar
  104. 104.
    Pascual R, et al. Early social isolation decreases the expression of calbindin D-28K in rat cerebellar Purkinje cells. Neurosci Lett 1999; 272: 171–174.PubMedGoogle Scholar
  105. 105.
    Pascual R, et al. Purkinje cell impairment induced by early movement restriction. Biol Neonate 1998; 73: 47–51.PubMedGoogle Scholar
  106. 106.
    Chard P, et al. Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J Physiol 1993; 472: 341–357.PubMedGoogle Scholar
  107. 107.
    Lledo P, et al. Stable transfection of calbindin-D28k into the GH3 cell line alters calcium currents and intracellular calcium homeostasis. Neuron 1992; 9: 943–954.PubMedGoogle Scholar
  108. 108.
    Maeda H, et al. Supralinear calcium signaling by by cooperative and mobile calcium buffering in Purkinje neurons. Neuron 1999; 24: 989–1002.PubMedGoogle Scholar
  109. 109.
    Nunzi MG, et al. Differential expression of calretinin and metabotropic glutamate receptor mGluRl alpha defines subsets of unipolar brush cells in mouse cerebellum. J Comp Neurol 2002; 451: 189–199.PubMedGoogle Scholar
  110. 110.
    Lokuta AJ, et al. Modulation of cardiac ryanodine receptors by sorcin. J Biol Chem 1997; 272 (40): 25333–25338.PubMedGoogle Scholar
  111. 111.
    Airaksinen MS, et al. Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. PNAS 1997; 94: 1488–1493.PubMedGoogle Scholar
  112. 112.
    Caillard O, et al. Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. PNAS 2000; 97 (24): 13372–13377.PubMedGoogle Scholar
  113. 113.
    Suk-Ho et al. Kinetics of calcium binding to parvalbumin in bovine chromaffin cells: implications for calcium transients in neuronal dendrites. J Physiol 2000; 525: 410–432.Google Scholar
  114. 114.
    Figueredo-Cardenas G, et al. Relative resistance of striatal neurons containing calbindin or parvalbumin to quinolinic acidmediated excitotoxicity compared to other striatal neuron types. Exp Neurol 1998; 149: 356–372.PubMedGoogle Scholar
  115. 115.
    Vecellio M, et al. Alterations in Purkinje cell spines of calbindin D-28 k and parvalbumin knock-out mice. Eur J Neuroscience 2000; 12: 945–954.Google Scholar
  116. 116.
    Schurmans S, et al. Impaired long-term potentiation induction in dentate gyrus of calretinin-deficient mice. PNAS 1997; 94: 10415–10420.PubMedGoogle Scholar
  117. 117.
    Baimbridge KG, at al.. Calcium binding proteins in the nervous system. Trends Neurosci 1992; 15: 303–308.PubMedGoogle Scholar
  118. 118.
    Heizmann CW, Braun K. Changes in Ca2+-binding proteins in human neurodegenerative disorders. Trend Neurosci 1992; 15: 259–264.PubMedGoogle Scholar
  119. 119.
    Ho BK, et al. Expression of calbindin-D28K in motoneuron hybrid cells after retroviral infection with calbindin-D28K cDNA prevents amyotrophic lateral sclerosis IgG-mediated cytotoxicity. PNAS 1996; 93: 6796–6801.PubMedGoogle Scholar
  120. 120.
    Iacopino AM, Christakos S. Specific reduction of calcium-binding protein (28-kilodalton, calbindin-D) gene expression in aging and neurodegenerative diseases. PNAS 1990; 87: 4078–4082.PubMedGoogle Scholar
  121. 121.
    Elliott J, Snider W. Parvalbumin is a marker of ALS-resistant motor neurons. Neuroreport 1995; 6: 449–452.PubMedGoogle Scholar
  122. 122.
    Bellido T, et al. Calbindin-D28k is expressed in osteoblastic cells and suppresses their apoptosis by inhibiting caspase-3 activity. J Biol Chem 2000; 275: 26328–26332.PubMedGoogle Scholar
  123. 123.
    Egea J, et al. Neuronal survival induced by neurotrophins requires calmodulin. J Cell Biol 2001; 154: 585–597.PubMedGoogle Scholar
  124. 124.
    Mikkelsen SE, et al. S100A12 protein is a strong inducer of neurite outgrowth from primary hippocampal neurons. J Neurochem 2001; 79: 767–776.PubMedGoogle Scholar
  125. 125.
    Choi WS, et al. Overexpression of calbindin-D28K induces neurite outgrowth in dopaminergic neuronal cells via activation of p38 MAPK. BBRC 2001; 287: 656–661.PubMedGoogle Scholar
  126. 126.
    Braunewell KH, et al. Intracellular neuronal calcium sensor (NCS) protein VILIP-1 modulates cGMP signalling pathways in transfected neural cells and cerebellar granule neurones. J Neurochem 2001; 78: 1277–1286.PubMedGoogle Scholar
  127. 127.
    Bouilleret V, et al. Neurodegenerative and morphogenic changes in a mouse model of temporal lobe epilepsy do not depend on the expression of the calcium-binding proteins parvalbumin, calbindin, or calretinin. Neuroscience 2000; 97: 47–58.PubMedGoogle Scholar
  128. 128.
    Klapstein GJ, et al. Calbindin-D28k fails to protect hippocampal neurons against ischemia in spite of cytoplasmic calcium buffering properties: evidence from knock-out mice. Neuroscience 1998; 85: 361–373.PubMedGoogle Scholar
  129. 129.
    Isaacs KR, et al. Vulnerability to calcium-induced neurotoxicity in cultured neurons expressing calretinin. Exp Neurol 2000; 163: 311–323.PubMedGoogle Scholar
  130. 130.
    Nagerl UV, et al. Surviving granule cells of the sclerotic human hippocampus have reduced calcium influx because of a loss of calbindin-D28k in temporal lobe epilepsy. J Neurosci 2000; 20: 1831–1836.PubMedGoogle Scholar
  131. 131.
    Kang TC, et al. The decreases in calcium binding proteins and neurofilament immunoreactivities in the Purkinje cell of the seizure sensitive gerbils. Neurochem Int 2002; 40: 115–122.PubMedGoogle Scholar
  132. 132.
    Andressen C, et al. Changes in shape and motility of cells transfected with parvalbumin cDNA. Exp Cell Res 1995; 219: 420–426.PubMedGoogle Scholar
  133. 133.
    Barger SW, Van Eldik LJ. S1000beta stimulates calcium fluxes in glial and neuronal cells. J Biol Chem 1992; 267: 9689–9694.PubMedGoogle Scholar
  134. 134.
    Huttunen HJ, et al. Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (Rage) activation. J Biol Chem. 2000; 275 (51): 40096–40105.PubMedGoogle Scholar
  135. 135.
    Fulle S, et al. Calcium and fos involvement in brain-derived Ca(2+)-binding protein (S100)-dependent apoptosis in rat phaeochromocytoma cells. Exp Physiol 2000; 85: 243–253.PubMedGoogle Scholar
  136. 136.
    Heizmann CW, et al. S100 pro teins: structure, functions and pathology. Front Biosci 2002; 7: dl356–1368.Google Scholar
  137. 137.
    Mikkelsen SE, et al. S100A12 protein is a strong inducer of neurite outgrowth from primary hippocampal neurons. J Neurochem 2001; 79: 767–776.PubMedGoogle Scholar
  138. 138.
    Saimi Y, Kung C. Calmodulin as ion channel subunit. Annu Rev Physiol 2002; 64: 289–311.PubMedGoogle Scholar
  139. 139.
    Haeseleer F, et al. Five members of a novel calcium-binding subfamily with similarities with calmodulin. J Biochem 2000; 14: 1247–1260.Google Scholar

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© Taylor & Francis 2003

Authors and Affiliations

  1. 1.VP Corporate DevelopmentProSkelia PharmaceuticalsRomainvilleFrance

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