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Emerging Functions of the “Ca2+ Buffers” Parvalbumin, Calbindin D-28k and Calretinin in the Brain

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Handbook of Neurochemistry and Molecular Neurobiology

Abstract:

Together with the ubiquitous calmodulin (CaM), the EF-hand containing calcium-binding proteins (CaBPs), parvalbumin (PV), calbindin D-28k (CB), and calretinin (CR), are the most abundantly expressed members of this family in the brain. Formerly, they were classified as simple buffers serving to “clamp” the intracellular calcium concentration [Ca2+]i. But recent studies often using transgenic mice have revealed these molecules to play pivotal roles in Ca2+ homeostasis and signaling. And research conducted during the last 5 years indicates that they are important for synaptic plasticity and related rhythmic activities within neuronal networks. For CB, an additional modulator role in inositol-1,4,5-trisphosphate (IP3)-signaling pathways was reported, indicating additional sensor functions. In this chapter, I summarize the current knowledge on the three CaBPs in the brain revealing their important roles in the CNS.

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Abbreviations

AHS:

Ammon's horn sclerosis

ALS:

amyotrophic lateral sclerosis

BAC:

bacterial chromosome

Ca2+ :

calcium

CaM:

calmodulin

CABPs:

calcium-binding proteins

CB:

calbindin D-28k

CCK:

cholecytokinin

CICR:

Ca2+-induced Ca2+ release

CNS:

central nervous system

CR:

calretinin

FRAP:

fluorescence recovery after photobleaching

EGFP:

enhanced green fluorescent protein

GAD67:

glutamate decarboxylase

IP3 :

inositol-1,4,5-triphosphate

IPSP:

inhibitory postsynaptic potential

LTD:

long-term depression

LTP:

long-term potentiation

MNTB:

medial nucleus of the trapezoid body

NCS:

neuronal calcium sensors

NCXs:

Na+/Ca2+ exchangers

PMCAs:

plasmalemmal Ca2+-ATPases

PTZ:

pentylenetetrazole

PV:

parvalbumin

RTN:

thalamic reticular nucleus

SERCAs:

sarcoplasmic reticulum Ca2+-ATPases

References

  • Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, et al. 1997a. Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D-28k gene. Proc Natl Acad Sci USA 94: 1488–1493.

    Article  CAS  Google Scholar 

  • Airaksinen MS, Thoenen H, Meyer M. 1997b. Vulnerability of midbrain dopaminergic neurons in calbindin D-28k-deficient mice: Lack of evidence for a neuroprotective role of endogenous calbindin in MPTP-treated and weaver mice. Eur J Neurosci 9: 120–127.

    Article  CAS  Google Scholar 

  • Airaksinen L, Virkkala J, Aarnisalo A, Meyer M, Ylikoski J, et al. 2000. Lack of calbindin D-28k does not affect hearing level or survival of hair cells in acoustic trauma. ORL J Otorhinolaryngol Relat Spec 62: 9–12.

    CAS  PubMed  Google Scholar 

  • Allbritton NL, Meyer T, Stryer L. 1992. Range of messenger action of calcium ion and inositol-1,4,5,-trisphophate. Science 258: 1812–1815.

    Article  CAS  PubMed  Google Scholar 

  • Aller MI, Jones A, Merlo D, Paterlini M, Meyer AH, et al. 2003. Cerebellar granule cell Cre recombinase expression. Genesis 36: 97–103.

    Article  CAS  PubMed  Google Scholar 

  • Andressen C, Blümcke I, Celio MR. 1993. Calcium-binding proteins: Selective markers of nerve cells. Cell Tissue Res 271: 181–208.

    Article  CAS  PubMed  Google Scholar 

  • Arai R, Jacobowitz DM, Deura S. 1993. Ultrastructural localization of calretinin immunoreactivity in lobule V of the rat cerebellum. Brain Res 613: 300–304.

    Article  CAS  PubMed  Google Scholar 

  • Arai R, Winsky L, Arai M, Jacobowitz DM. 1991. Immunohistochemical localization of calretinin in the rat hindbrain. J Comp Neurol 310: 21–44.

    Article  CAS  PubMed  Google Scholar 

  • Baimbridge KG, Celio MR, Rogers JH. 1992. Calcium-binding proteins in the nervous system. Trends Neurosci 15: 303–308.

    Article  CAS  PubMed  Google Scholar 

  • Barski JJ, Dethleffsen K, Meyer M. 2000. Cre recombinase expression in cerebellar Purkinje cells. Genesis 28: 93–98.

    Article  CAS  PubMed  Google Scholar 

  • Barski JJ, Hartmann J, Rose CR, Hoebeek F, Morl K, et al. 2003. Calbindin in cerebellar Purkinje cells is a critical determinant of the precision of motor coordination. J Neurosci 23: 3469–3477.

    CAS  PubMed  Google Scholar 

  • Barski JJ, Morl K, Meyer M. 2002. Conditional inactivation of the calbindin D-28k (Calb1) gene by Cre/loxP-mediated recombination. Genesis 32: 165–168.

    Article  CAS  PubMed  Google Scholar 

  • Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, et al. 2002. Fast synaptic inhibition promotes synchronized γ oscillations in hippocampal interneuron networks. Proc Natl Acad Sci USA 99: 13222–13227.

    Article  CAS  PubMed  Google Scholar 

  • Bastianelli E. 2003. Distribution of calcium-binding proteins in the cerebellum. Cerebellum 2: 242–262.

    Article  CAS  PubMed  Google Scholar 

  • Bearzatto B, Servais L, Roussel C, Gall D, Baba-Aissa F, et al. 2006. Targeted calretinin expression in granule cells of calretinin-null mice restores normal cerebellar functions. FASEB J 20: 380–382.

    CAS  PubMed  Google Scholar 

  • Beers DR, Ho BK, Siklos L, Alexianu ME, Mosier DR, 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: 499–509.

    Article  CAS  PubMed  Google Scholar 

  • Belichenko PV, Vogt WD, Myklossy J, Celio MR. 1995. Calretinin-positive Cajal–Retzius cells persist in the adult human neocortex. Neuroreport 6: 1869–1874.

    Article  CAS  PubMed  Google Scholar 

  • Belluardo N, Marko G, Trovato-Salinaro A, Le Gurun S, Charollais A, et al. 2000. Expression of connexin36 in the adult and developing rat brain. Brain Res 865: 121–138.

    Article  CAS  PubMed  Google Scholar 

  • Berggard T, Miron S, Onnerfjord P, Thulin E, Akerfeldt KS, et al. 2002a. Calbindin D-28k exhibits properties characteristic of a Ca2+ sensor. J Biol Chem 28: 28.

    Google Scholar 

  • Berggard T, Szczepankiewicz O, Thulin E, Linse S. 2002b. Myo-inositol monophosphatase is an activated target of calbindin D-28k. J Biol Chem 277: 41954–41959.

    Article  CAS  Google Scholar 

  • Berridge MJ. 1998. Neuronal calcium signaling. Neuron 21: 13–26.

    Article  CAS  PubMed  Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL. 2003. Calcium signaling: Dynamics, homeostasis, and remodeling. Nat Rev Mol Cell Biol 4: 517–529.

    Article  CAS  PubMed  Google Scholar 

  • Blatow M, Caputi A, Burnashev N, Monyer H, Rozov A. 2003a. Ca2+ buffer saturation underlies paired-pulse facilitation in calbindin D-28k-containing terminals. Neuron 38: 79–88.

    Article  CAS  Google Scholar 

  • Blatow M, Rozov A, Katona I, Hormuzdi SG, Meyer AH, et al. 2003b. A novel network of multipolar bursting interneurons generates θ frequency oscillations in neocortex. Neuron 38: 805–817.

    Article  CAS  Google Scholar 

  • Bouilleret V, Schwaller B, Schurmans S, Celio MR, Fritschy JM. 2000. 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 97: 47–58.

    Article  CAS  PubMed  Google Scholar 

  • Braak E, Braak H. 1993. The new monodendritic neuronal type within the adult human cerebellar granule cell layer shows calretinin-immunoreactivity. Neurosci Lett 154: 199–202.

    Article  CAS  PubMed  Google Scholar 

  • Braunewell KH, Gundelfinger ED. 1999. Intracellular neuronal calcium sensor proteins: A family of EF-hand calcium-binding proteins in search of a function. Cell Tissue Res 295: 1–12.

    Article  CAS  PubMed  Google Scholar 

  • Burgoyne RD, Weiss JL. 2001. The neuronal calcium sensor family of Ca2+-binding proteins. Biochem J 353: 1–12.

    Article  CAS  PubMed  Google Scholar 

  • Caillard O, Moreno H, Schwaller B, Llano I, Celio MR, et al. 2000. Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc Natl Acad Sci USA 97: 13372–13377.

    Article  CAS  PubMed  Google Scholar 

  • Celio MR. 1986. Parvalbumin in most γ-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231: 995–997.

    Article  CAS  PubMed  Google Scholar 

  • Celio MR. 1990. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35: 375–475.

    Article  CAS  PubMed  Google Scholar 

  • Celio MR, Blümcke I. 1994. Perineuronal nets—a specialized form of extracellular matrix in the adult nervous system. Brain Res Rev 19: 128–145.

    Article  CAS  PubMed  Google Scholar 

  • Celio MR, Heizmann CW. 1981. Calcium-binding protein parvalbumin as a neuronal marker. Nature 293: 300–302.

    Article  CAS  PubMed  Google Scholar 

  • Celio M, Pauls T, Schwaller B, editors. 1996. Guidebook to the Calcium-Binding Proteins. Oxford: Oxford University Press.

    Google Scholar 

  • Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L. 1998. Perineuronal nets: Past and present. Trends Neurosci 21: 510–515.

    Article  CAS  PubMed  Google Scholar 

  • Chang HC, Seki T, Moriuchi T, Silver J. 1985. Isolation and characterization of mouse Thy-1 genomic clones. Proc Natl Acad Sci USA 82: 3819–3823.

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Carroll S, Racay P, Dick J, Pette D, et al. 2001. Deficiency in parvalbumin increases fatigue resistance in fast-twitch muscle and upregulates mitochondria. Am J Physiol (Cell Physiol) 281: C114–C122.

    CAS  Google Scholar 

  • Cheron G, Gall D, Servais L, Dan B, Maex R, et al. 2004. Inactivation of calcium-binding protein genes induces 160 Hz oscillations in the cerebellar cortex of alert mice. J Neurosci 24: 434–441.

    Article  CAS  PubMed  Google Scholar 

  • Cheung WT, Richards DE, Rogers JH. 1993. Calcium binding by chick calretinin and rat calbindin D-28k synthesized in bacteria. Eur J Biochem 215: 401–410.

    Article  CAS  PubMed  Google Scholar 

  • Cicchetti F, Parent A. 1996. Striatal interneurons in Huntington's disease: Selective increase in the density of calretinin-immunoreactive medium-sized neurons. Mov Disord 11: 619–626.

    Article  CAS  PubMed  Google Scholar 

  • Cohen P, Klee CB. 1988. Calmodulin. Amsterdam-New York-Oxford: Elsevier

    Google Scholar 

  • Collin T, Chat M, Lucas MG, Moreno H, Racay P, et al. 2005. Developmental changes in parvalbumin regulate presynaptic Ca2+ signaling. J Neurosci 25: 96–107.

    Article  CAS  PubMed  Google Scholar 

  • Cox JA. 1996. Techniques for measuring the binding of Ca2+ and Mg2+ to calcium-binding proteins. Guidebook to the Calcium-Binding Proteins. Celio M, Pauls T, Schwaller B, editors. Oxford: Oxford University Press, pp. 1–12.

    Google Scholar 

  • Csillik B, Mihaly A, Krisztin-Peva B, Chadaide Z, Samsam M, et al. 2005. GABAergic parvalbumin-immunoreactive large calyciform presynaptic complexes in the reticular nucleus of the rat thalamus. J Chem Neuroanat 30: 17–26.

    Article  CAS  PubMed  Google Scholar 

  • D'Orlando C, Celio MR, Schwaller B. 2002. Calretinin and calbindin D-28k, but not parvalbumin, protect against glutamate-induced excitotoxicity in transfected N18-RE 105 neuroblastoma–retina hybrid cells. Brain Res 945: 181–190.

    Article  PubMed  Google Scholar 

  • D'Orlando C, Fellay B, Schwaller B, Salicio V, Bloc A, et al. 2001. Calretinin and calbindin D-28k delay the onset of cell death after excitotoxic stimulation in transfected P19 cells. Brain Res 909: 145–158.

    Article  PubMed  Google Scholar 

  • Dargan SL, Parker I. 2003. Buffer kinetics shape the spatiotemporal patterns of IP3-evoked Ca2+ signals. J Physiol 553: 775–788.

    Article  CAS  PubMed  Google Scholar 

  • Dargan SL, Schwaller B, Parker I. 2004. Spatiotemporal patterning of IP3-mediated Ca2+ signals in Xenopus oocytes by Ca2+-binding proteins. J Physiol 556: 447–461.

    Article  CAS  PubMed  Google Scholar 

  • Dekkers J, Bayley P, Dick JR, Schwaller B, Berchtold MW, et al. 2004. Overexpression of parvalbumin in transgenic mice rescues motoneurons from injury-induced cell death. Neuroscience 123: 459–466.

    Article  CAS  PubMed  Google Scholar 

  • Diop AG, Dussartre C, Barthe D, Hugon J. 1996. Neuroprotective properties of calretinin against the HIV-1 gp120 toxicity. Neurosci Res Commun 18: 107–114.

    Article  CAS  Google Scholar 

  • Du J, Zhang L, Weiser M, Rudy B, McBain CJ. 1996. Developmental expression and functional characterization of the potassium channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J Neurosci 16: 506–518.

    CAS  PubMed  Google Scholar 

  • Edmonds B, Reyes R, Schwaller B, Roberts WM. 2000. Calretinin modifies presynaptic calcium signaling in frog saccular hair cells. Nat Neurosci 3: 786–790.

    Article  CAS  PubMed  Google Scholar 

  • Enderlin S, Norman AW, Celio MR. 1987. Ontogeny of the calcium-binding protein calbindin D-28k in the rat nervous system. Anat Embryol 177: 15–28.

    Article  CAS  PubMed  Google Scholar 

  • Faas GC, Schwaller B, Vergara JL, Mody I. 2003. Binding kinetics of calretinin-22k determined by flash photolysis of caged calcium. Soc Neurosci Abstr p. 791.4

    Google Scholar 

  • Felmy F, Schneggenburger R. 2004. Developmental expression of the Ca2+-binding proteins, calretinin and parvalbumin, at the calyx of Held of rats and mice. Eur J Neurosci 20: 1473–1482.

    Article  PubMed  Google Scholar 

  • Ferrer I, Tunon T, Soriano E, del Rio A, Iraizoz I, et al. 1992. Calbindin immunoreactivity in normal human temporal neocortex. Brain Res 572: 33–41.

    Article  CAS  PubMed  Google Scholar 

  • Fierro L, Llano I. 1996. High endogenous calcium buffering in Purkinje cells from rat cerebellar slices. J Physiol 496: 617–625.

    CAS  PubMed  Google Scholar 

  • Floris A, Dino M, Jacobowitz DM, Mugnaini E. 1994. The unipolar brush cells of the rat cerebellar cortex and cochlear nucleus are calretinin-positive: A study by light and electron microscopic immunocytochemistry. Anat Embryol (Berl) 189: 495–520.

    CAS  Google Scholar 

  • Fonseca M, Soriano E. 1995. Calretinin-immunoreactivity neurons in the normal temporal cortex and in Alzheimer's disease. Brain Res 691: 83–91.

    Article  CAS  PubMed  Google Scholar 

  • Frassoni C, Bentivoglio M, Spreafico R, Sanchez MP, Puelles L, et al. 1991. Postnatal development of calbindin and parvalbumin immunoreactivity in the thalamus of the rat. Brain Res Dev Brain Res 58: 243–249.

    Article  CAS  PubMed  Google Scholar 

  • Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6: 347–470.

    Article  CAS  PubMed  Google Scholar 

  • Fukuda T, Kosaka T. 2000. Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J Neurosci 20: 1519–1528.

    CAS  PubMed  Google Scholar 

  • Galarreta M, Hestrin S. 2001. Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2: 425–433.

    Article  CAS  PubMed  Google Scholar 

  • Gall D, Roussel C, Susa I, D&Angelo E, Rossi P, et al. 2003. Altered neuronal excitability in cerebellar granule cells of mice lacking calretinin. J Neurosci 23: 9320–9327.

    CAS  PubMed  Google Scholar 

  • Gibson JR, Beierlein M, Connors BW. 1999. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75–79.

    Article  CAS  PubMed  Google Scholar 

  • Grillner S, Markram H, De Schutter E, Silberberg G, Le Beau FE. 2005. Microcircuits in action—from CPGs to neocortex. Trends Neurosci 28: 525–533.

    Article  CAS  PubMed  Google Scholar 

  • Gulyas AI, Miettinen R, Jacobowitz DM, Freund TF. 1992. Calretinin is present in nonpyramidal cells of the rat hippocampus—I. A new type of neuron specifically associated with the mossy fibre system. Neuroscience 48: 1–27.

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Wang Y, Markram H. 2000. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287: 273–278.

    Article  CAS  PubMed  Google Scholar 

  • Gurden H, Schiffmann SN, Lemaire M, Bohme GA, Parmentier M, et al. 1998. Calretinin expression as a critical component in the control of dentate gyrus long-term potentiation induction in mice. Eur J Neurosci 10: 3029–3033.

    Article  CAS  PubMed  Google Scholar 

  • Hackney CM, Mahendrasingam S, Penn A, Fettiplace R. 2005. The concentrations of calcium-buffering proteins in mammalian cochlear hair cells. J Neurosci 25: 7867–7875.

    Article  CAS  PubMed  Google Scholar 

  • Hefft S, Jonas P. 2005. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron–principal neuron synapse. Nat Neurosci 8: 1319–1328.

    Article  CAS  PubMed  Google Scholar 

  • Heizmann CW, Braun K. 1992. Changes in Ca2+-binding proteins in human neurodegenerative disorders. Trends Neurosci 15: 259–264.

    Article  CAS  PubMed  Google Scholar 

  • Hendrickson AE, Van Brederode JF, Mulligan KA, Celio MR. 1991. Development of the calcium-binding protein parvalbumin and calbindin in monkey striate cortex. J Comp Neurol 307: 626–646.

    Article  CAS  PubMed  Google Scholar 

  • Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, et al. 2005. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3: e159.

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Glezer II, Conde F, Flagg RA, Rubin MB, et al. 1999. Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: Phylogenetic and developmental patterns. J Chem Neuroanat 16: 77–116.

    Article  CAS  PubMed  Google Scholar 

  • Hormuzdi SG, Pais I, Le Beau FE, Towers SK, Rozov A, et al. 2001. Impaired electrical signaling disrupts γ frequency oscillations in connexin 36-deficient mice. Neuron 31: 487–495.

    Article  CAS  PubMed  Google Scholar 

  • Hubbard MJ, McHugh NJ. 1995. Calbindin 28 kDa and calbindin 30 kDa (calretinin) are substantially localized in the particulate fraction of rat brain. FEBS Lett 374: 333–337.

    Article  CAS  PubMed  Google Scholar 

  • Iacopino A, Christakos S, German D, Sonsalla PK, Altar CA. 1992. Calbindin D-28K-containing neurons in animal models of neurodegeneration: Possible protection from excitotoxicity. Brain Res Mol Brain Res 13: 251–261.

    Article  CAS  PubMed  Google Scholar 

  • Ikura M. 1996. Calcium binding and conformational response in EF-hand proteins. Trends Biochem Sci 1: 14–17.

    Google Scholar 

  • Isaacs KR, Wolpoe ME, Jacobowitz DM. 2000. Vulnerability to calcium-induced neurotoxicity in cultured neurons expressing calretinin. Exp Neurol 163: 311–323.

    Article  CAS  PubMed  Google Scholar 

  • Jacobowitz DM, Winsky L. 1991. Immunocytochemical localization of calretinin in the forebrain of the rat. J Comp Neurol 304: 198–218.

    Article  CAS  PubMed  Google Scholar 

  • John LM, Mosquera-Caro M, Camacho P, Lechleiter JD. 2001. Control of IP3-mediated Ca2+ puffs in Xenopus laevis oocytes by the Ca2+-binding protein parvalbumin. J Physiol 535: 3–16.

    Article  CAS  PubMed  Google Scholar 

  • Jones EG, Hendry SH. 1989. Differential calcium-binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur J Neurosci 1: 222–246.

    Article  PubMed  Google Scholar 

  • Jouvenceau A, Potier B, Battini R, Ferrari S, Dutar P, et al. 1999. Glutamatergic synaptic responses and long-term potentiation are impaired in the CA1 hippocampal area of calbindin D-28k-deficient mice. Synapse 33: 172–180.

    Article  CAS  PubMed  Google Scholar 

  • Jouvenceau A, Potier B, Poindessous-Jazat F, Dutar P, Slama A, et al. 2002. Decrease in calbindin content significantly alters LTP but not NMDA receptor and calcium channel properties. Neuropharmacology 42: 444–458.

    Article  CAS  PubMed  Google Scholar 

  • Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7: 476–486.

    Article  CAS  PubMed  Google Scholar 

  • Kawaguchi Y, Kubota Y. 1998. Neurochemical features and synaptic connections of large physiologically identified GABAergic cells in the rat frontal cortex. Neuroscience 85: 677–701.

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki H, Nakayama S, Kretsinger RH. 1998. Classification and evolution of EF-hand proteins. Biometals 11: 277–295.

    Article  CAS  PubMed  Google Scholar 

  • Klapstein GJ, Vietla S, Lieberman DN, Gray PA, Airaksinen MS, et al. 1998. Calbindin D-28k fails to protect hippocampal neurons against ischemia in spite of its cytoplasmic calcium-buffering properties: Evidence from calbindin D-28k knockout mice. Neuroscience 85: 361–373.

    Article  CAS  PubMed  Google Scholar 

  • Korn H, and Axelrad H. 1980. Electrical inhibition of Purkinje cells in the cerebellum of the rat. Proc Natl Acad Sci USA 77: 6244–6247.

    Article  CAS  PubMed  Google Scholar 

  • Kosaka T, Kosaka K, Nakayama T, Hunziker W, Heizmann CW. 1993. Axons and axon terminals of cerebellar Purkinje cells and basket cells have higher levels of parvalbumin immunoreactivity than somata and dendrites: Quantitative analysis by immunogold labeling. Exp Brain Res 93: 483–491.

    Article  CAS  PubMed  Google Scholar 

  • Kreiner L, Lee A. 2005. Endogenous and exogenous Ca2+ buffers differentially modulate Ca2+-dependent inactivation of CAV2.1 Ca2+ channels. J Biol Chem 281: 4691–4698.

    Article  PubMed  CAS  Google Scholar 

  • Kretsinger RH, Nockolds CE. 1973. Carp muscle calcium-binding protein. II. Structure determination and general description. J Biol Chem 248: 3313–3326.

    CAS  PubMed  Google Scholar 

  • Kuznicki J, Isaacs KR, Jacobowitz DM. 1996. The expression of calretinin in transfected PC12 cells provides no protection against Ca2+-overload or trophic factor deprivation. Biochim Biophys Acta 1313: 194–200.

    Article  PubMed  Google Scholar 

  • Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860–921.

    Article  CAS  PubMed  Google Scholar 

  • Leclerc I, Sturchler E, Heizmann CW. 2006. Calcium regulation by EF-hand proteins in the brain. Handbook of Neurochemistry and Molecular Neurobiology 3rd ed. Lajtha A, editor. New York: Springer.

    Google Scholar 

  • Lee A, Wong ST, Gallagher D, Li B, Storm DR, et al. 1999. Ca2+/calmodulin binds to and modulates P/Q-type calcium channels. Nature 399: 155–159.

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Schwaller B, Neher E. 2000. Kinetics of Ca2+ binding to parvalbumin in bovine chromaffin cells: Implications for [Ca2+] transients of neuronal dendrites. J Physiol 525 Pt 2: 419–432.

    Google Scholar 

  • Lewis DA, Hashimoto T, Volk DW. 2005. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6: 312–324.

    Article  CAS  PubMed  Google Scholar 

  • Li-Smerin Y, Levitan ES, Johnson JW. 2001. Free intracellular Mg2+ concentration and inhibition of NMDA responses in cultured rat neurons. J Physiol 533: 729–743.

    Article  CAS  PubMed  Google Scholar 

  • Maeda H, Ellis-Davies GC, Ito K, Miyashita Y, Kasai H. 1999. Supralinear Ca2+ signaling by cooperative and mobile Ca2+ buffering in Purkinje neurons. Neuron 24: 989–1002.

    Article  CAS  PubMed  Google Scholar 

  • Maetzler W, Nitsch C, Bendfeldt K, Racay P, Vollenweider F, et al. 2004. Ectopic parvalbumin expression in mouse forebrain neurons increases excitotoxic injury provoked by ibotenic acid injection into the striatum. Exp Neurol 186: 78–88.

    Article  CAS  PubMed  Google Scholar 

  • Magloczky Z, Freund TF. 2005. Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends Neurosci 28: 334–340.

    Article  CAS  PubMed  Google Scholar 

  • Magloczky Z, Halasz P, Vajda J, Czirjak S, Freund TF. 1997. Loss of calbindin D-28K immunoreactivity from dentate granule cells in human temporal lobe epilepsy. Neuroscience 76: 377–385.

    Article  CAS  PubMed  Google Scholar 

  • Maki M, Kitaura Y, Satoh H, Ohkouchi S, Shibata H. 2002. Structures, functions, and molecular evolution of the penta-EF-hand Ca2+-binding proteins. Biochim Biophys Acta 1600: 51–60.

    CAS  PubMed  Google Scholar 

  • Marenholz I, Heizmann CW, Fritz G. 2004. S100 proteins in mouse and man: From evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 322: 1111–1122.

    Article  CAS  PubMed  Google Scholar 

  • Margrie TW, Meyer AH, Caputi A, Monyer H, Hasan MT, et al. 2003. Targeted whole-cell recordings in the mammalian brain in vivo. Neuron 39: 911–918.

    Article  CAS  PubMed  Google Scholar 

  • Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, et al. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793–807.

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto M, Nakagawa T, Inoue T, Nagata E, Tanaka K, et al. 1996. Ataxia and epileptic seizures in mice lacking type 1 inositol-1,4,5-trisphosphate receptor. Nature 379: 168–171.

    Article  CAS  PubMed  Google Scholar 

  • Meyer AH, Katona I, Blatow M, Rozov A, Monyer H. 2002. In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci 22: 7055–7064.

    CAS  PubMed  Google Scholar 

  • Miettinen R, Gulyas AI, Baimbridge KG, Jacobowitz DM, Freund TF. 1992. Calretinin is present in nonpyramidal cells of the rat hippocampus—II. Coexistence with other calcium-binding proteins and GABA. Neuroscience 48: 29–43.

    Article  CAS  PubMed  Google Scholar 

  • Mihaly A, Szente M, Dubravcsik Z, Boda B, Kiraly E, et al. 1997. Parvalbumin- and calbindin-containing neurons express c-fos protein in primary and secondary (mirror) epileptic foci of the rat neocortex. Brain Res 761: 135–145.

    Article  CAS  PubMed  Google Scholar 

  • Möckel V, Fischer G. 1994. Vulnerability to excitotoxic stimuli of cultured rat hippocampal neurons containing the calcium-binding proteins calretinin and calbindin D-28k. Brain Res 648: 109–120.

    Article  PubMed  Google Scholar 

  • Molinari S, Battini R, Ferrari S, Pozzi L, Killcross AS, et al. 1996. Deficits in memory and hippocampal long-term potentiation in mice with reduced calbindin D-28k expression. Proc Natl Acad Sci USA 93: 8028–8033.

    Article  CAS  PubMed  Google Scholar 

  • Morris SA, Correa V, Cardy TJ, O'Beirne G, Taylor CW. 1999. Interactions between inositol trisphosphate receptors and fluorescent Ca2+ indicators. Cell Calcium 25: 137–142.

    Article  CAS  PubMed  Google Scholar 

  • Mouatt-Prigent A, Agid Y, Hirsch EC. 1994. Does the calcium-binding protein calretinin protect dopaminergic neurons against degeneration in Parkinson's disease? Brain Res 668: 62–70.

    Article  CAS  PubMed  Google Scholar 

  • Muller A, Kukley M, Stausberg P, Beck H, Muller W, et al. 2005. Endogenous Ca2+ buffer concentration and Ca2+ microdomains in hippocampal neurons. J Neurosci 25: 558–565.

    Article  PubMed  CAS  Google Scholar 

  • Nagerl UV, Mody I. 1998. Calcium-dependent inactivation of high-threshold calcium currents in human dentate gyrus granule cells. J Physiol 509 (Pt 1): 39–45.

    Article  CAS  PubMed  Google Scholar 

  • Nagerl UV, Mody I, Jeub M, Lie AA, Elger CE, et al. 2000a. Surviving granule cells of the sclerotic human hippocampus have reduced Ca2+ influx because of a loss of calbindin D-28k in temporal lobe epilepsy. J Neurosci 20: 1831–1836.

    CAS  Google Scholar 

  • Nagerl UV, Novo D, Mody I, Vergara JL. 2000b. Binding kinetics of calbindin D-28k determined by flash photolysis of caged Ca2+. Biophys J 79: 3009–3018.

    Article  CAS  Google Scholar 

  • Naraghi M. 1997. T-jump study of calcium-binding kinetics of calcium chelators. Cell Calcium 22: 255–268.

    Article  CAS  PubMed  Google Scholar 

  • Nelson MR, Chazin WJ. 1998. Structures of EF-hand Ca2+-binding proteins: Diversity in the organization, packing, and response to Ca2+ binding. Biometals 11: 297–318.

    Article  CAS  PubMed  Google Scholar 

  • Nelson MR, Thulin E, Fagan PA, Forsen S, Chazin WJ. 2002. The EF-hand domain: A globally cooperative structural unit. Protein Sci 11: 198–205.

    Article  CAS  PubMed  Google Scholar 

  • Palay SL, Chan-Palay V. 1974. The Cerebellum. Berlin-New York: Springer Verlag.

    Google Scholar 

  • Palecek J, Lips MB, Keller BU. 1999. Calcium dynamics and buffering in motoneurons of the mouse spinal cord. J Physiol (Lond) 520 Pt 2: 485–502.

    Article  CAS  Google Scholar 

  • Pasti L, Carmignoto G, Pozzan T, Battini R, Ferrari S, et al. 1999. Cellular calcium handling in brain slices from calbindin D-28k-deficient mice. Neuroreport 10: 2367–2372.

    Article  CAS  PubMed  Google Scholar 

  • Pike CJ, Cotman CW. 1995. Calretinin-immunoreactivity neurons are resistant to β-amyloid toxicity in vitro. Brain Res 671: 293–298.

    Article  CAS  PubMed  Google Scholar 

  • Plogmann D, Celio MR. 1993. Intracellular concentration of parvalbumin in nerve cells. Brain Res 600: 273–279.

    Article  CAS  PubMed  Google Scholar 

  • Raymackers JM, Gailly P, Schoor MC, Pette D, Schwaller B, et al. 2000. Tetanus relaxation of fast skeletal muscles of the mouse made parvalbumin deficient by gene inactivation. J Physiol 527: 355–364.

    Article  CAS  PubMed  Google Scholar 

  • Résibois A, Rogers JH. 1992. Calretinin in rat brain: An immunohistochemical study. Neurosci 46: 101–134.

    Article  Google Scholar 

  • Roberts WM. 1994. Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J Neurosci 14: 3246–3262.

    CAS  PubMed  Google Scholar 

  • Rozov A, Burnashev N, Sakmann B, Neher E. 2001. Transmitter release modulation by intracellular Ca2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531: 807–826.

    Article  CAS  PubMed  Google Scholar 

  • Sampson VL, Morrison JH, Vickers JC. 1997. The cellular basis for the relative resistance of parvalbumin- and calretinin-immunoreactive neocortical neurons to the pathology of Alzheimer's disease. Exp Neurol 145: 295–302.

    Article  CAS  PubMed  Google Scholar 

  • Schiffmann SN, Cheron G, Lohof A, d&Alcantara P, Meyer M, et al. 1999. Impaired motor coordination and Purkinje cell excitability in mice lacking calretinin. Proc Natl Acad Sci USA 96: 5257–5262.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt H, Brown EB, Schwaller B, Eilers J. 2003a. Diffusional mobility of parvalbumin in spiny dendrites of cerebellar Purkinje neurons quantified by fluorescence recovery after photobleaching. Biophys J 84: 2599–2608.

    Article  CAS  Google Scholar 

  • Schmidt H, Schwaller B, Eilers J. 2005. Calbindin D-28k targets myo-inositol monophosphatase in spines and dendrites of cerebellar Purkinje neurons. Proc Natl Acad Sci USA 102: 5850–5855.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt H, Stiefel KM, Racay P, Schwaller B, Eilers J. 2003b. Mutational analysis of dendritic Ca2+ kinetics in rodent Purkinje cells: Role of parvalbumin and calbindin D-28k. J Physiol 551: 13–32.

    Article  CAS  Google Scholar 

  • Schneggenburger R, Neher E. 2000. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406: 889–893.

    Article  CAS  PubMed  Google Scholar 

  • Schurmans S, Schiffmann SN, Gurden H, Lemaire M, Lipp H-P, et al. 1997. Impaired LTP induction in the dentate gyrus of calretinin-deficient mice. Proc Natl Acad Sci USA 94: 10415–10420.

    Article  CAS  PubMed  Google Scholar 

  • Schwaller B. 2004. Calcium-binding Proteins. In Nature Encyclopedia of Life Sciences, p. E0390502 (doi:0390510.0391038/npg.els.0003905) http://www.els.net/. London: Nature Publishing Group.

  • Schwaller B, Bruckner G, Celio MR, Hartig W. 1999a. A polyclonal goat antiserum against the calcium-binding protein calretinin is a versatile tool for various immunochemical techniques. J Neurosci Methods 92: 137–144.

    Article  CAS  Google Scholar 

  • Schwaller B, Celio MR, Hunziker W. 1995. Alternative splicing of calretinin mRNA leads to different forms of calretinin. Eur J Biochem 230: 424–430.

    Article  CAS  PubMed  Google Scholar 

  • Schwaller B, Dick J, Dhoot G, Carroll S, Vrbova G, et al. 1999b. Prolonged contraction–relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. Am J Physiol (Cell Physiol) 276: C395–403.

    CAS  Google Scholar 

  • Schwaller B, Durussel I, Jermann D, Herrmann B, Cox JA. 1997. Comparison of the Ca2+-binding properties of human recombinant calretinin-22k and calretinin. J Biol Chem 272: 29663–29671.

    Article  CAS  PubMed  Google Scholar 

  • Schwaller B, Meyer M, Schiffmann SN. 2002. “New” functions for “old” proteins: The role of the calcium-binding proteins calbindin D-28k, calretinin, and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1: 241–258.

    Article  CAS  PubMed  Google Scholar 

  • Schwaller B, Tetko IV, Tandon P, Silveira DC, Vreugdenhil M, et al. 2004. Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures. Mol Cell Neurosci 25: 650–663.

    Article  CAS  PubMed  Google Scholar 

  • Servais L, Bearzatto B, Schwaller B, Dumont M, De Saedeleer C, et al. 2005. Mono- and dual-frequency fast cerebellar oscillation in mice lacking parvalbumin and/or calbindin D-28k. Eur J Neurosci 22: 861–870.

    Article  CAS  PubMed  Google Scholar 

  • Seto-Ohshima A, Emson PC, Berchtold MW, Heizmann CW. 1989. Localization of parvalbumin mRNA in rat brain by in situ hybridization histochemistry. Exp Brain Res 75: 653–658.

    Article  CAS  PubMed  Google Scholar 

  • Skelton NJ, Kördel J, Akke M, Forsén S, Chazin WJ. 1994. Signal transduction versus buffering activity in Ca++-binding proteins. Nat Struct Biol 1: 239–245.

    Article  CAS  PubMed  Google Scholar 

  • Skelton NJ, Kordel J, Chazin WJ. 1995. Determination of the solution structure of Apo calbindin D-9k by NMR spectroscopy. J Mol Biol 249: 441–462.

    Article  CAS  PubMed  Google Scholar 

  • Sloviter RS, Sollas AL, Barbaro NM, Laxer KD. 1991. Calcium-binding protein (calbindin D-28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J Comp Neurol 308: 381–396.

    Article  CAS  PubMed  Google Scholar 

  • Solbach S, Celio MR. 1991. Ontogeny of the calcium-binding protein parvalbumin in the rat nervous system. Anat Embryol 184: 103–124.

    Article  CAS  PubMed  Google Scholar 

  • Stern MD. 1992. Buffering of calcium in the vicinity of a channel pore. Cell Calcium 13: 183–192.

    Article  CAS  PubMed  Google Scholar 

  • Stevens J, Rogers JH. 1997. Chick calretinin: Purification, composition, and metal-binding activity of native and recombinant forms. Protein Expr Purif 9: 171–181.

    Article  CAS  PubMed  Google Scholar 

  • Toledo-Rodriguez M, Goodman P, Illic M, Wu C, Markram H. 2005. Neuropeptide and calcium-binding protein gene expression profiles predict neuronal anatomical type in the juvenile rat. J Physiol 567: 401–413.

    Article  CAS  PubMed  Google Scholar 

  • Van Den Bosch L, Schwaller B, Vleminckx V, Meijers B, Stork S, et al. 2002. Protective effect of parvalbumin on excitotoxic motor neuron death. Exp Neurol 174: 150–161.

    Article  CAS  PubMed  Google Scholar 

  • Vanselow BK, Keller BU. 2000. Calcium dynamics and buffering in oculomotor neurons from mouse that are particularly resistant during amyotrophic lateral sclerosis (ALS)-related motoneuron disease. J Physiol 525 Pt 2: 433–445.

    Article  CAS  PubMed  Google Scholar 

  • Vecellio M, Schwaller B, Meyer M, Hunziker W, Celio MR. 2000. Alterations in Purkinje cell spines of calbindin D-28k and parvalbumin knockout mice. Eur J Neurosci 12: 945–954.

    Article  CAS  PubMed  Google Scholar 

  • Vogt Weisenhorn DM, Prieto EW, Celio MR. 1994. Localization of calretinin in cells of layer I (Cajal–Retzius cells) of the developing cortex of the rat. Dev Brain Res 82: 293–297.

    Article  CAS  Google Scholar 

  • Vreugdenhil M, Jefferys JGR, Celio MR, Schwaller B. 2003. Parvalbumin-deficiency facilitates repetitive IPSCs and γ oscillations in the hippocampus. J Neurophysiol 89: 1414–1422.

    Article  PubMed  Google Scholar 

  • Wassle H, Peichl L, Airaksinen MS, Meyer M. 1998. Calcium-binding proteins in the retina of a calbindin-null mutant mouse. Cell Tissue Res 292: 211–218.

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Konishi M. 2001. Intracellular calibration of the fluorescent Mg2+ indicator furaptra in rat ventricular myocytes. Pflugers Arch 442: 35–40.

    Article  CAS  PubMed  Google Scholar 

  • Winsky L, Kuznicki J. 1996. Antibody recognition of calcium-binding proteins depends on their calcium-binding status. J Neurochem 66: 1–8.

    Google Scholar 

  • Winsky L, Nakata H, Martin BM, Jacobowitz DM. 1989. Isolation, partial amino acid sequence, and immunohistochemical localization of a brain-specific calcium-binding protein. Proc Natl Acad Sci USA 86: 10139–10143.

    Article  CAS  PubMed  Google Scholar 

  • Yamakuni T, Kuwano R, Odani S, Miki N, Yamaguchi K, et al. 1987. Molecular cloning of cDNA to mRNA for a cerebellar spot 35 protein. J Neurochem 48: 1590–1596.

    Article  CAS  PubMed  Google Scholar 

  • Yenari MA, Minami M, Sun GH, Meier TJ, Kunis DM, et al. 2001. Calbindin D-28k overexpression protects striatal neurons from transient focal cerebral ischemia. Stroke 32: 1028–1035.

    CAS  PubMed  Google Scholar 

  • Zaitsev AV, Gonzalez-Burgos G, Povysheva NV, Kroner S, Lewis DA, et al. 2005. Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. Cereb Cortex 15: 1178–1186.

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann L, Schwaller B. 2002. Monoclonal antibodies recognizing epitopes of calretinins: Dependence on Ca2+-binding status and differences in antigen accessibility in colon cancer cells. Cell Calcium 31: 13–25.

    Article  CAS  PubMed  Google Scholar 

  • Zühlke RD, Pitt GS, Deisseroth K, Tsien RW, Reuter H. 1999. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature 399: 159–162.

    Article  PubMed  Google Scholar 

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Acknowledgments

The help of M. Celio, Fribourg, Switzerland and I. Llano, Paris, France, for the critical reading of the manuscript is highly appreciated. Figure 5-3 was provided by M. Chat, INSERM, UMR 8118, Paris, France. This work was partially supported by a grant from the Swiss National Science Foundation (no. 3100A0-100400/1 to B. S.).

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  1. B. Schwaller
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  1. Center for Neurochemistry, Nathan S. Kline Institute for Psychiatric Research, 140 Old Orangeburg Road, Orangeburg, Newyork, 10962, USA

    Abel Lajtha (Director) (Director)

  2. Department of Neurosciences Division of Neurology, Medical University of South Carolina, 96 Jonathan Lucas Street Suite 309, Charleston, SC 29425, USA

    Naren Banik (Professor) (Professor)

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Schwaller, B. (2007). Emerging Functions of the “Ca2+ Buffers” Parvalbumin, Calbindin D-28k and Calretinin in the Brain. In: Lajtha, A., Banik, N. (eds) Handbook of Neurochemistry and Molecular Neurobiology. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-30379-6_5

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