The use of transgenic mouse models to reveal the functions of Ca 2 + buffer proteins in excitable cells

Biochimica et Biophysica Acta - General Subjects

Volumn 1820, Issue 8, 2012, Pages 1294-1303

  Schwaller, Beat ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Calbindin D28k; Calcium buffer; Calcium homeostasome; Calcium binding protein; Calretinin; Parvalbumin

Indexed keywords

CALBINDIN; CALCIUM BINDING PROTEIN; CALCIUM BUFFER PROTEIN; CALRETININ; INTRACELLULAR CALCIUM SENSING PROTEIN; ONCOMODULIN; PARVALBUMIN; SECRETAGOGIN; UNCLASSIFIED DRUG;

CALCIUM BINDING; CALCIUM SIGNALING; CELL STRUCTURE; CONFORMATIONAL TRANSITION; DISEASE MODEL; EXPERIMENTAL MODEL; FAST MUSCLE; FUNCTIONAL MORPHOLOGY; HUMAN; IN VIVO STUDY; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; MITOCHONDRIAL VOLUME; MUSCLE CONTRACTION; MUSCLE EXCITATION; NERVE EXCITABILITY; NEUROPROTECTION; NONHUMAN; OSCILLATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; REGULATORY MECHANISM; REVIEW; SPINE DENSITY; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ANIMALS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; HUMANS; MICE; MICE, TRANSGENIC; MITOCHONDRIA, MUSCLE; NEURONS; PARVALBUMINS; PHENOTYPE;

MUS; MUS MUSCULUS;

EID: 84862128819     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2011.11.008     Document Type: Review

References (106)

1. B. Schwaller Calcium-binding proteins Nature Encyclopedia of Life Sciences vol. 4 2004 Nature Publishing Group London E0390502 [ http://www.els.net/ [doi:0390510.0391038/npg.els.0003905]
2. D. Prins, and M. Michalak Organellar calcium buffers Cold Spring Harb. Perspect. Biol. 3 2011
3. H. Kawasaki, S. Nakayama, and R.H. Kretsinger Classification and evolution of EF-hand proteins Biometals 11 1998 277 295 (Pubitemid 29121537)
4. R.H. Kretsinger, and C.E. Nockolds Carp muscle calcium-binding protein. II. Structure determination and general description J. Biol. Chem. 248 1973 3313 3326
5. 2 +-binding proteins Biochim. Biophys. Acta 1600 2002 51 60 (Pubitemid 38224398)
6. 2 +-binding helix-loop-helix EF-hand motifs Biochem. J. 405 2007 199 221 (Pubitemid 47075156)
7. K.L. Yap, J.B. Ames, M.B. Swindells, and M. Ikura Diversity of conformational states and changes within the EF-hand protein superfamily Proteins 37 1999 499 507 (Pubitemid 29519739)
8. 2 + buffers Cold Spring Harb. Perspect. Biol. 2 2010 a004051
9. H. Schmidt, B. Schwaller, and J. Eilers Calbindin D28k targets myo-inositol monophosphatase in spines and dendrites of cerebellar Purkinje neurons Proc. Natl. Acad. Sci. U. S. A. 102 2005 5850 5855 (Pubitemid 40559648)
10. 2 + signals Nat. Neurosci. 14 2011 301 304
11. 2 +-binding proteins Nat. Struct. Biol. 1 1994 239 245
12. E. Bockamp, M. Maringer, C. Spangenberg, S. Fees, S. Fraser, L. Eshkind, F. Oesch, and B. Zabel Of mice and models: improved animal models for biomedical research Physiol. Genomics 11 2002 115 132
13. X. Gao, and P. Zhang Transgenic RNA interference in mice Physiology (Bethesda) 22 2007 161 166
14. A. Kleinhammer, J. Deussing, W. Wurst, and R. Kuhn Conditional RNAi in mice Methods 53 2011 142 150
15. C. Lundberg, T. Bjorklund, T. Carlsson, J. Jakobsson, P. Hantraye, N. Deglon, and D. Kirik Applications of lentiviral vectors for biology and gene therapy of neurological disorders Curr. Gene Ther. 8 2008 461 473
16. Y. Sun, X. Chen, and D. Xiao Tetracycline-inducible expression systems: new strategies and practices in the transgenic mouse modeling Acta Biochim. Biophys. Sin. (Shanghai) 39 2007 235 246 (Pubitemid 46625305)
17. M.J. Berridge, M.D. Bootman, and H.L. Roderick Calcium signalling: dynamics, homeostasis and remodelling Nat. Rev. Mol. Cell Biol. 4 2003 517 529 (Pubitemid 36773404)
18. 2 + homeostasome Adv. Exp. Med. Biol. 740 2012 1 25
19. C.W. Heizmann, M.W. Berchtold, and A.M. Rowlerson Correlation of parvalbumin concentration with relaxation speed in mammalian muscles Proc. Natl. Acad. Sci. U. S. A. 79 1982 7243 7247
20. M.R. Celio Calbindin D-28k and parvalbumin in the rat nervous system Neuroscience 35 1990 375 475 (Pubitemid 20176750)
21. P.R. Schneeberger, and C.W. Heizmann Parvalbumin in rat kidney. Purification and localization FEBS Lett. 201 1986 51 56 (Pubitemid 16072353)
22. B. Schwaller, J. Dick, G. Dhoot, S. Carroll, G. Vrbova, P. Nicotera, D. Pette, A. Wyss, H. Bluethmann, W. Hunziker, and M.R. Celio Prolonged contraction-relaxation cycle of fast-twitch muscles in parvalbumin knockout mice Am. J. Physiol. Cell Physiol. 276 1999 C395 C403
23. M. Muntener, L. Kaser, J. Weber, and M.W. Berchtold Increase of skeletal muscle relaxation speed by direct injection of parvalbumin cDNA Proc. Natl. Acad. Sci. U. S. A. 92 1995 6504 6508
24. G. Chen, S. Carroll, P. Racay, J. Dick, D. Pette, I. Traub, G. Vrbova, P. Eggli, M. Celio, and B. Schwaller Deficiency in parvalbumin increases fatigue resistance in fast-twitch muscle and upregulates mitochondria Am. J. Physiol. Cell Physiol. 281 2001 C114 C122
25. B. Billups, and I.D. Forsythe Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses J. Neurosci. 22 2002 5840 5847 (Pubitemid 35387628)
26. V.K. Mootha, J. Bunkenborg, J.V. Olsen, M. Hjerrild, J.R. Wisniewski, E. Stahl, M.S. Bolouri, H.N. Ray, S. Sihag, M. Kamal, N. Patterson, E.S. Lander, and M. Mann Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria Cell 115 2003 629 640 (Pubitemid 37508523)
27. P. Racay, P. Gregory, and B. Schwaller Parvalbumin deficiency in fast-twitch muscles leads to increased 'slow-twitch type' mitochondria, but does not affect the expression of fiber specific proteins FEBS J. 273 2006 96 108
28. G. Chen, P. Racay, S. Bichet, M.R. Celio, P. Eggli, and B. Schwaller Deficiency in parvalbumin, but not in calbindin D-28k upregulates mitochondrial volume and decreases smooth endoplasmic reticulum surface selectively in a peripheral, subplasmalemmal region in the soma of Purkinje cells Neuroscience 142 2006 97 105 (Pubitemid 44354986)
29. M.K. Park, M.C. Ashby, G. Erdemli, O.H. Petersen, and A.V. Tepikin Perinuclear, perigranular and sub-plasmalemmal mitochondria have distinct functions in the regulation of cellular calcium transport EMBO J. 20 2001 1863 1874 (Pubitemid 32397389)
30. 2 +-binding proteins J. Physiol. 556 2004 447 461 (Pubitemid 38578999)
31. 2 + signals J. Physiol. 553 2003 775 788 (Pubitemid 38035621)
32. 2 + signaling in cerebellar Purkinje neurons J. Neurosci. Res. 88 2010 275 289
33. J. Eilers, G. Callewaert, C. Armstrong, and A. Konnerth Calcium signaling in a narrow somatic submembrane shell during synaptic activity in cerebellar Purkinje neurons Proc. Natl. Acad. Sci. U. S. A. 92 1995 10272 10276
34. 2 + kinetics in rodent Purkinje cells: role of parvalbumin and calbindin D28k J. Physiol. 551 2003 13 32 (Pubitemid 37062909)
35. B. Schwaller, I.V. Tetko, P. Tandon, D.C. Silveira, M. Vreugdenhil, T. Henzi, M.C. Potier, M.R. Celio, and A.E. Villa Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures Mol. Cell. Neurosci. 25 2004 650 663 (Pubitemid 38481474)
36. M.S. Airaksinen, J. Eilers, O. Garaschuk, H. Thoenen, A. Konnerth, and M. Meyer Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene Proc. Natl. Acad. Sci. U. S. A. 94 1997 1488 1493 (Pubitemid 27087878)
37. W. Maetzler, C. Nitsch, K. Bendfeldt, P. Racay, F. Vollenweider, and B. Schwaller Ectopic parvalbumin expression in mouse forebrain neurons increases excitotoxic injury provoked by ibotenic acid injection into the striatum Exp. Neurol. 186 2004 78 88 (Pubitemid 38229907)
38. 2 +-buffers R.A.a.D. E.A. Bradshaw, Handbook of Cell Signaling vol. 2 2009 Academic Press Oxford 955 962
39. O. Caillard, H. Moreno, B. Schwaller, I. Llano, M.R. Celio, and A. Marty Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity Proc. Natl. Acad. Sci. U. S. A. 97 2000 13372 13377
40. 2 + transients of neuronal dendrites J. Physiol. 525 2000 419 432 (Pubitemid 30398371)
41. 2 + signaling J. Neurosci. 25 2005 96 107 (Pubitemid 40110770)
42. 2 + buffer parvalbumin affects transmitter release in nanodomain coupling regimes at GABAergic synapses Nature Neurosci. 15 2011 20 22
43. M. Vreugdenhil, J.G. Jefferys, M.R. Celio, and B. Schwaller Parvalbumin-deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus J. Neurophysiol. 89 2003 1414 1422 (Pubitemid 36323988)
44. 2 + and short-term facilitation J. Neurosci. 27 2007 2261 2271 (Pubitemid 46340950)
45. F. Manseau, S. Marinelli, P. Mendez, B. Schwaller, D.A. Prince, J.R. Huguenard, and A. Bacci Desynchronization of neocortical networks by asynchronous release of GABA at autaptic and synaptic contacts from fast-spiking interneurons PLoS Biol. 8 2010
46. 2 + sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse Neuron 57 2008 536 545 (Pubitemid 351273992)
47. R. Franconville, G. Revet, G. Astorga, B. Schwaller, and I. Llano Somatic calcium level reports integrated spiking activity of cerebellar interneurons in vitro and in vivo J. Neurophysiol. 106 2011 1793 1805
48. T. Kosaka, K. Kosaka, T. Nakayama, W. Hunziker, and C.W. Heizmann 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 1993 483 491 (Pubitemid 23168075)
49. 2 + buffering by calretinin PLoS Biol. 5 2007 e311 doi:310.1371/journal.pbio.0050311 (Pubitemid 350276936)
50. M.A. Farre-Castany, B. Schwaller, P. Gregory, J. Barski, C. Mariethoz, J.L. Eriksson, I.V. Tetko, D. Wolfer, M.R. Celio, I. Schmutz, U. Albrecht, and A.E. Villa Differences in locomotor behavior revealed in mice deficient for the calcium-binding proteins parvalbumin, calbindin D-28k or both Behav. Brain Res. 178 2007 250 261 (Pubitemid 46341442)
51. L. Servais, B. Bearzatto, B. Schwaller, M. Dumont, C. De Saedeleer, B. Dan, J.J. Barski, S.N. Schiffmann, and G. Cheron Mono- and dual-frequency fast cerebellar oscillation in mice lacking parvalbumin and/or calbindin D-28k Eur. J. Neurosci. 22 2005 861 870 (Pubitemid 41243327)
52. G. Cheron, D. Gall, L. Servais, B. Dan, R. Maex, and S.N. Schiffmann Inactivation of calcium-binding protein genes induces 160 Hz oscillations in the cerebellar cortex of alert mice J. Neurosci. 24 2004 434 441 (Pubitemid 38112374)
53. B. Bearzatto, L. Servais, C. Roussel, D. Gall, F. Baba-Aissa, S. Schurmans, A. de Kerchove d'Exaerde, G. Cheron, and S.N. Schiffmann Targeted calretinin expression in granule cells of calretinin-null mice restores normal cerebellar functions FASEB J. 20 2006 380 382 (Pubitemid 46671178)
54. V.S. Sohal, F. Zhang, O. Yizhar, and K. Deisseroth Parvalbumin neurons and gamma rhythms enhance cortical circuit performance Nature 459 2009 698 702
55. J.A. Cardin, M. Carlen, K. Meletis, U. Knoblich, F. Zhang, K. Deisseroth, L.H. Tsai, and C.I. Moore Driving fast-spiking cells induces gamma rhythm and controls sensory responses Nature 459 2009 663 667
56. S. Hippenmeyer, E. Vrieseling, M. Sigrist, T. Portmann, C. Laengle, D.R. Ladle, and S. Arber A developmental switch in the response of DRG neurons to ETS transcription factor signaling PLoS Biol. 3 2005 e159
57. E.C. Fuchs, A.R. Zivkovic, M.O. Cunningham, S. Middleton, F.E. Lebeau, D.M. Bannerman, A. Rozov, M.A. Whittington, R.D. Traub, J.N. Rawlins, and H. Monyer Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior Neuron 53 2007 591 604 (Pubitemid 46216760)
58. A.H. Meyer, I. Katona, M. Blatow, A. Rozov, and H. Monyer In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons J. Neurosci. 22 2002 7055 7064 (Pubitemid 35379161)
59. C. Tanahira, S. Higo, K. Watanabe, R. Tomioka, S. Ebihara, T. Kaneko, and N. Tamamaki Parvalbumin neurons in the forebrain as revealed by parvalbumin-Cre transgenic mice Neurosci. Res. 63 2009 213 223
60. S. Molinari, R. Battini, S. Ferrari, L. Pozzi, A.S. Killcross, T.W. Robbins, A. Jouvenceau, J.M. Billard, P. Dutar, Y. Lamour, W.A. Baker, H. Cox, and P.C. Emson Deficits in memory and hippocampal long-term potentiation in mice with reduced calbindin D-28K expression Proc. Natl. Acad. Sci. U. S. A. 93 1996 8028 8033
61. A. Jouvenceau, B. Potier, R. Battini, S. Ferrari, P. Dutar, and J.M. Billard Glutamatergic synaptic responses and long-term potentiation are impaired in the CA1 hippocampal area of calbindin D(28k)-deficient mice Synapse 33 1999 172 180 (Pubitemid 29372844)
62. A. Jouvenceau, B. Potier, F. Poindessous-Jazat, P. Dutar, A. Slama, J. Epelbaum, and J. Billard Decrease in calbindin content significantly alters LTP but not NMDA receptor and calcium channel properties Neuropharmacology 42 2002 444 458 (Pubitemid 34304238)
63. L. Pasti, G. Carmignoto, T. Pozzan, R. Battini, S. Ferrari, G. Lally, and P.C. Emson Cellular calcium handling in brain slices from calbindin D28k-deficient mice Neuroreport 10 1999 2367 2372 (Pubitemid 29367940)
64. 2 + buffers parvalbumin, calbindin D-28k and calretinin in the brain A. Lajtha, N. Banik, Handbook of Neurochemistry and Molecular Neurobiology Neural Protein Metabolism and Function vol. 7 (11) 2007 Springer 233 Spring Street, New York, New York 10013-1578 USA 197 222
65. R.S. Sloviter, A.L. Sollas, N.M. Barbaro, and K.D. Laxer Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus J. Comp. Neurol. 308 1991 381 396
66. 2 + influx because of a loss of calbindin-D(28k) in temporal lobe epilepsy J. Neurosci. 20 2000 1831 1836 (Pubitemid 30220380)
67. U.V. Nagerl, and I. Mody Calcium-dependent inactivation of high-threshold calcium currents in human dentate gyrus granule cells J. Physiol. 509 1998 39 45 (Pubitemid 28252009)
68. G.J. Klapstein, S. Vietla, D.N. Lieberman, P.A. Gray, M.S. Airaksinen, H. Thoenen, M. Meyer, and I. Mody 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 1998 361 373 (Pubitemid 28218658)
69. H. Moreno, N.S. Burghardt, D. Vela, J. Mascotti, F. Hua, A.A. Fenton, B. Schwaller, and S.A. Small Reductions in the calcium-buffering protein calbindin correlate with age-related hippocampal metabolic decline Hippocampus 2011 10.1002/hipo.20957 [Epub ahead of print]
70. M. Blatow, A. Rozov, I. Katona, S.G. Hormuzdi, A.H. Meyer, M.A. Whittington, A. Caputi, and H. Monyer A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex Neuron 38 2003 805 817 (Pubitemid 36694786)
71. J.J. Barski, K. Morl, and M. Meyer Conditional inactivation of the calbindin D-28k (Calb1) gene by Cre/loxP-mediated recombination Genesis 32 2002 165 168 (Pubitemid 34211729)
72. J.J. Barski, K. Dethleffsen, and M. Meyer Cre recombinase expression in cerebellar Purkinje cells Genesis 28 2000 93 98
73. J.J. Barski, J. Hartmann, C.R. Rose, F. Hoebeek, K. Morl, M. Noll-Hussong, C.I. De Zeeuw, A. Konnerth, and M. Meyer Calbindin in cerebellar Purkinje cells is a critical determinant of the precision of motor coordination J. Neurosci. 23 2003 3469 3477 (Pubitemid 36531989)
74. M. Matsumoto, T. Nakagawa, T. Inoue, E. Nagata, K. Tanaka, H. Takano, O. Minowa, J. Kuno, S. Sakakibara, M. Yamada, H. Yoneshima, A. Miyawaki, Y. Fukuuchi, T. Furuichi, H. Okano, K. Mikoshiba, and T. Noda Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5- trisphosphate receptor Nature 379 1996 168 171 (Pubitemid 26020199)
75. M. Vecellio, B. Schwaller, M. Meyer, W. Hunziker, and M.R. Celio Alterations in Purkinje cell spines of calbindin D-28 k and parvalbumin knock-out mice Eur. J. Neurosci. 12 2000 945 954 (Pubitemid 30168772)
76. 2 + Biophys. J. 79 2000 3009 3018
77. H. Schmidt, E.B. Brown, B. Schwaller, and J. Eilers Diffusional mobility of parvalbumin in spiny dendrites of cerebellar purkinje neurons quantified by fluorescence recovery after photobleaching Biophys. J. 84 2003 2599 2608 (Pubitemid 36373580)
78. H. Schmidt, O. Arendt, E.B. Brown, B. Schwaller, and J. Eilers Parvalbumin is freely mobile in axons, somata and nuclei of cerebellar Purkinje neurones J. Neurochem. 100 2007 727 735 (Pubitemid 46095622)
79. 2 +-binding proteins J. Physiol. 581 2007 619 629 (Pubitemid 46831760)
80. H. Schmidt, and J. Eilers Spine neck geometry determines spino-dendritic cross-talk in the presence of mobile endogenous calcium binding proteins J. Comput. Neurosci. 27 2009 229 243
81. 2 + channels J. Biol. Chem. 281 2005 4691 4698 (Pubitemid 43847728)
82. 2 + channels in cerebellar Purkinje neurons lacking parvalbumin and calbindin D-28k J. Neurophysiol. 103 2010 371 381
83. F. Barinka, and R. Druga Calretinin expression in the mammalian neocortex: a review Physiol. Res. 59 2010 665 677
84. E. Bastianelli Distribution of calcium-binding proteins in the cerebellum Cerebellum 2 2003 242 262 (Pubitemid 38280282)
85. J. Rogers, M. Khan, and J. Ellis Calretinin and other CaBPs in the nervous system Adv. Exp. Med. Biol. 269 1990 195 203
86. S. Schurmans, S.N. Schiffmann, H. Gurden, M. Lemaire, H.-P. Lipp, V. Schwam, R. Pochet, A. Imperato, G.A. Böhme, and M. Parmentier Impaired LTP induction in the dentate gyrus of calretinin-deficient mice Proc. Natl. Acad. Sci. 94 1997 10415 10420 (Pubitemid 27407056)
87. D. Gall, C. Roussel, I. Susa, E. D'Angelo, P. Rossi, B. Bearzatto, M.C. Galas, D. Blum, S. Schurmans, and S.N. Schiffmann Altered neuronal excitability in cerebellar granule cells of mice lacking calretinin J. Neurosci. 23 2003 9320 9327 (Pubitemid 37323031)
88. C. Roussel, T. Erneux, S.N. Schiffmann, and D. Gall Modulation of neuronal excitability by intracellular calcium buffering: from spiking to bursting Cell Calcium 39 2006 455 466
89. S.N. Schiffmann, G. Cheron, A. Lohof, P. d'Alcantara, M. Meyer, M. Parmentier, and S. Schurmans Impaired motor coordination and Purkinje cell excitability in mice lacking calretinin Proc. Natl. Acad. Sci. U. S. A. 96 1999 5257 5262 (Pubitemid 29214570)
90. G. Cheron, L. Servais, B. Dan, D. Gall, C. Roussel, and S.N. Schiffmann Fast oscillation in the cerebellar cortex of calcium binding protein-deficient mice: a new sensorimotor arrest rhythm Prog. Brain Res. 148 2005 165 180
91. J. Palecek, M.B. Lips, and B.U. Keller Calcium dynamics and buffering in motoneurones of the mouse spinal cord J. Physiol. (Lond.) 520 Pt 2 1999 485 502 (Pubitemid 29511912)
92. L. Van Den Bosch, B. Schwaller, V. Vleminckx, B. Meijers, S. Stork, T. Ruehlicke, E. Van Houtte, H. Klaassen, M.R. Celio, L. Missiaen, W. Robberecht, and M.W. Berchtold Protective effect of parvalbumin on excitotoxic motor neuron death Exp. Neurol. 174 2002 150 161 (Pubitemid 34293445)
93. J. Dekkers, P. Bayley, J.R. Dick, B. Schwaller, M.W. Berchtold, and L. Greensmith Over-expression of parvalbumin in transgenic mice rescues motoneurons from injury-induced cell death Neuroscience 123 2004 459 466 (Pubitemid 38032922)
94. W. Maetzler, H. Stünitz, K. Bendfeldt, F. Vollenweider, B. Schwaller, and C. Nitsch Microcalcification after excitotoxicity is enhanced in transgenic mice expressing parvalbumin in all neurons, may commence in neuronal mitochondria, and undergoes structural modifications over time Neuropathol. Appl. Neurobiol. 186 2009 78 88
95. V. Bouilleret, B. Schwaller, S. Schurmans, M.R. Celio, and J.M. Fritschy 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 2000 47 58 (Pubitemid 30195875)
96. M.A. Yenari, M. Minami, G.H. Sun, T.J. Meier, D.M. Kunis, J.R. McLaughlin, D.Y. Ho, R.M. Sapolsky, and G.K. Steinberg Calbindin d28k overexpression protects striatal neurons from transient focal cerebral ischemia Stroke 32 2001 1028 1035 (Pubitemid 32285178)
97. F.B. Freimann, O. Crome, Z. Shevtsova, M. Bahr, and S. Kugler Evaluation of long-term upregulation of Calbindin D28K as a preventive approach for ischaemic stroke Int. J. Stroke 5 2011 319 320
98. T. Voigtländer, U. Unterberger, G.M.B. Schwaller, M.R. Celio, M. Meyer, and H. Budka The role of parvalbumin and calbindin D28k in experimental scrapie Neuropathol. Appl. Neurobiol. 34 2007 435 445
99. M.R. Celio, and I. Blümcke Perineuronal nets - a specialized form of extracellular matrix in the adult nervous system Brain Res. Rev. 19 1994 128 145 (Pubitemid 24024086)
100. B. Csillik, B. Schwaller, A. Mihaly, T. Henzi, E. Losonczic, and E. Knyihar-Csillik Upregulated expression of oncomodulin, the beta isoform of parvalbumin, in perikarya and axons in the diencephalon of parvalbumin knockout mice Neuroscience 165 2010 749 757
101. 2 +-binding protein J. Biol. Chem. 275 2000 24740 24751 (Pubitemid 30626577)
102. 2 +-binding protein Cereb. Cortex 11 2001 1161 1169 (Pubitemid 33108243)
103. J. Attems, A. Ittner, K. Jellinger, R.M. Nitsch, M. Maj, L. Wagner, J. Gotz, and M. Heikenwalder Reduced secretagogin expression in the hippocampus of P301L tau transgenic mice J. Neural Transm. 118 2011 737 745
104. K.C. Choi, and E.B. Jeung Molecular mechanism of regulation of the calcium-binding protein calbindin-D(9k), and its physiological role(s) in mammals: a review of current research J. Cell. Mol. Med. 12 2008 409 420
105. 2 + absorption in small intestine Arch. Biochem. Biophys. 460 2007 227 232 (Pubitemid 46589396)
106. G.S. Lee, K.Y. Lee, K.C. Choi, Y.H. Ryu, S.G. Paik, G.T. Oh, and E.B. Jeung Phenotype of a calbindin-D9k gene knockout is compensated for by the induction of other calcium transporter genes in a mouse model J. Bone Miner. Res. 22 2007 1968 1978