Ca 2+ sensor proteins in dendritic spines: A race for Ca 2+

Frontiers in Molecular Neuroscience

Volumn , Issue MAY 2012, 2012, Pages

  Raghuram, Vijeta ^a,b   Sharma, Yogendra ^a   Kreutz, Michael R ^b  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

Binding affinity; Ca 2+; Calcium dynamics; Calcium binding protein; Dendritic spine; Neuronal calcium sensor; Neuronal calcium signaling; Protein protein interaction

Indexed keywords

AMPA RECEPTOR; CALCIUM BINDING PROTEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CHANNEL; CALCIUM ION; CALDENDRIN; CALMODULIN; CALSENILIN; GUANYLATE CYCLASE ACTIVATOR; HIPPOCALCIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEURONAL CALCIUM SENSOR; NEURONAL CALCIUM SENSOR 1; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

BINDING AFFINITY; BIOSENSOR; CALCIUM BINDING; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL HETEROGENEITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; DENDRITIC SPINE; HUMAN; LONG TERM POTENTIATION; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; NONHUMAN; POSTSYNAPTIC DENSITY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SMOOTH ENDOPLASMIC RETICULUM;

EID: 84864023954     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2012.00061     Document Type: Review

References (135)

1. An, W. F., Bowlby, M. R., Betty, M., Cao, J., Ling, H. P., Mendoza, G., Hinson, J. W., Mattsson, K. I., Strassle, B. W., Trimmer, J. S., and Rhodes, K. J. (2000). Modulation of A-type potassium channels by a family of calcium sensors. Nature 403, 553-556.
2. Anderson, D., Mehaffey, W. H., Iftinca, M., Rehak, R., Engbers, J. D., Hameed, S., Zamponi, G. W., and Turner, R. W. (2010). Regulation of neuronal activity by Cav3-Kv4 channel signaling complexes. Nat. Neurosci. 13, 333-337.
3. 2+-induced conformational changes, and equilibrium unfolding transitions. J. Mol. Biol. 376, 1100-1115.
4. Araya, R., Jiang, J., Eisenthal, K. B., and Yuste, R. (2006). The spine neck filters membrane potentials. Proc. Natl. Acad. Sci. U.S.A. 103, 17961-17966.
5. Arellano, J. I., Benavides-Piccione, R., Defelipe, J., and Yuste, R. (2007). Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front. Neurosci. 1:10. doi: 10.3389/neuro.01.1.1.010.2007
6. Bahi, N., Friocourt, G., Carrié, A., Graham, M. E., Weiss, J. L., Chafey, P., Fauchereau, F., Burgoyne, R. D., and Chelly, J. (2003). IL1 receptor accessory protein like, a protein involved in X-linked mental retardation, interacts with Neuronal Calcium Sensor-1 and regulates exocytosis. Hum. Mol. Genet. 12, 1415-1425.
7. Baimbridge, K. G., Celio, M. R., and Rogers, J. H. (1992). Calcium-binding proteins in the nervous system. Trends Neurosci. 15, 303-308.
8. Berridge, M. J., Lipp, P., and Bootman, M. D. (2000). The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell. Biol. 1, 11-21.
9. Biber, A., Schmid, G., and Hempel, K. (1984). Calmodulin content in specific brain areas. Exp. Brain Res. 56, 323-326.
10. Biess, A., Korkotian, E., and Holcman, D. (2007). Diffusion in a dendritic spine: the role of geometry. Phys. Rev. EStat. Nonlin. SoftMatterPhys. 76, 021922.
11. Bloodgood, B. L., Giessel, A. J., and Sabatini, B. L. (2009). Biphasic synaptic Ca influx arising from compartmentalized electrical signals in dendritic spines. PLoS Biol. 7:e1000190. doi: 10.1371/journal.pbio.1000190
12. Bloodgood, B. L., and Sabatini, B. L. (2005). Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310, 866-869.
13. Bloodgood, B. L., and Sabatini, B. L. (2007). Nonlinear regulation ofuni-tary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron 53, 249-260.
14. Bofill-Cardona, E., Kudlacek, O., Yang, Q., Ahorn, H., Freissmuth, M., and Nanoff, C. (2000). Binding of calmodulin to the D2-dopamine receptor reduces receptor signaling by arresting the G protein activation switch. J. Biol. Chem. 275, 32672-32680.
15. 2+ signalling. Nat. Rev. Neurosci. 8, 182-193.
16. 2+-binding proteins. Biochem. J. 353, 1-12.
17. Buxbaum, J. D., Choi, E. K., Luo, Y., Lilliehook, C., Crowley, A. C., Merriam, D. E., and Wasco, W. (1998). Calsenilin: a calcium-binding protein that interacts with the presenilins and regulates the levels of a presenilin fragment. Nat. Med. 4, 1177-1181.
18. Byrne, M. J., Putkey, J. A., Waxham, M. N., and Kubota, Y. (2009). Dissecting cooperative calmodulin binding to CaM kinase II: a detailed stochastic model. J. Comput. Neurosci. 27, 621-638.
19. Byrne, M. J., Waxham, M. N., and Kubota, Y. (2011). The impacts of geometry and binding on CaMKII diffusion and retention in dendritic spines. J. Comput. Neurosci. 31, 1-12.
20. Clapham, D. E. (2007). Calcium signaling. Cell 131, 1047-1058.
21. Cline, M. S., Smoot, M., Cerami, E., Kuchinsky, A., Landys, N., Workman, C., Christmas, R., Avila-Campilo, I., Creech, M., Gross, B., Hanspers, K., Isserlin, R., Kelley, R., Killcoyne, S., Lotia, S., Maere, S., Morris, J., Ono, K., Pavlovic, V., Pico, A. R., Vailaya, A., Wang, P. L., Adler, A., Conklin, B. R., Hood, L., Kuiper, M., Sander, C., Schmulevich, I., Schwikowski, B., Warner, G. J., Ideker, T., and Bader, G. D. (2007). Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2, 2366-2382.
22. Cornelisse, L. N., van Elburg, R. A., Meredith, R. M., Yuste, R., and Mansvelder, H. D. (2007). High speed two-photon imaging of calcium dynamics in dendritic spines: consequences for spine calcium kinetics and buffer capacity. PLoS One 2:e1073. doi: 10.1371/jour-nal.pone.0001073
23. Czarnecki, K. Haas, C. A. Bas Orth, C. Deller, T., and Frotscher, M. (2005). Postnatal development of synap-topodin expression in the rodent hippocampus. J. Comp. Neurol. 490, 133-144.
24. De Castro, E., Nef, S., Fiumelli, H., Lenz, S. E., Kawamura, S., and Nef, P. (1995). Regulation of rhodopsin phosphorylation by a family of neuronal calcium sensors. Biochem. Biophys. Res. Commun. 216, 133-140.
25. 2+ selectivity in the calmodulin regulation of CaV channels. Nature 451, 830-834.
26. Dieterich, D. C., Karpova, A., Mikhaylova, M., Zdobnova, I., König, I., Landwehr, M., Kreutz, M., Smalla, K. H., Richter, K., Landgraf, P., Reissner, C., Boeckers, T. M., Zuschratter, W., Spilker, C., Seidenbecher, C. I., Garner, C. C., Gundelfinger, E. D., and Kreutz, M. R. (2008). Caldendrin-Jacob: a protein liaison that couples NMDA receptor signalling to the nucleus. PLoS Biol. 6:e34. doi: 10.1371/journal.pbio.0060034
27. 2+ sensor protein hippocalcin in rat hippocampal neurons. Eur. J. Neurosci. 32, 347-358.
28. Dukhanina, E. A., Dukhanin, A. S., Lomonosov, M. Y., Lukanidin, E. M., and Georgiev, G. P. (1997). Spectral studies on the calcium-binding properties of Mtsl protein and its interaction with target protein. FEBS Lett. 410, 403-406.
29. Emptage, N., Bliss, T. V., and Fine, A. (1999). Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22, 115-124.
30. 2+ signals. Nat. Neurosci. 14, 301-304.
31. 2+ buffering by calretinin. PLoSBiol. 5:e311. doi: 10.1371/jour-nal.pbio.0050311
32. Few, A. P., Lautermilch, N. J., Westenbroek, R. E., Scheuer, T., and Catterall, W. A. (2005). Differential regulation of CaV2.1 channels by calcium-binding protein 1 and visinin-like protein-2 requires N-terminal myristoylation. J. Neurosci. 25, 7071-7080.
33. Furuta, Y., Kobayashi, M., Masaki, T., and Takamatsu, K. (1999). Age-related changes in expression of hip-pocalcin and NVP2 in rat brain. Neurochem. Res. 24, 651-658.
34. Gaertner, T. R., Putkey, J. A., and Waxham, M. N. (2004). RC3/ Neurogranin and Ca2+/calmodulin dependent protein kinase II produce opposing effects on the affinity of calmodulin for calcium. J. Biol. Chem. 279, 39374-39382.
35. Gerendasy, D. D., Herron, S. R., Watson, J. B., and Sutcliffe, J. G. (1994). Mutational and biophysical studies suggest C3/neurogranin regulates calmodulin availability. J. Biol. Chem. 269, 22420-22426.
36. Gierke, P., Zhao, C., Brackmann, M., Linke, B., Heinemann, U., and Braunewell, K. H. (2004). Expression analysis of members of the neuronal calcium sensor protein family: combining bioinformatics and Western Blot analysis. Biochem. Biophys. Res. Commun. 323, 38-43.
37. 2+-binding helix-loop-helix EF-hand motifs. Biochem. J. 405, 199-221.
38. Grabarek, Z. (2006). Structural basis for diversity of the EF-hand calcium-binding proteins. J. Mol. Biol. 359, 509-525.
39. Grunditz, A., Holbro, N., Tian, L., Zuo, Y., and Oertner, T. G. (2008). Spine neck plasticity controls postsynap-tic calcium signals through electrical compartmentalization. J. Neurosci. 28, 13457-13466.
40. 2+-binding protein (CABP) subfamily with similarity to calmodulin. J. Biol. Chem. 275, 1247-1260.
41. Hao, J., and Oertner, T. G. (2011). Depolarization gates spine calcium transients and spike-timing-dependent potentiation. Curr. Opin. Neurobiol. doi: 10.1016/j.conb.2011. 10.004. [Epub ahead of print].
42. Harris, K. M., and Stevens, J. K. (1989). Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982-2997.
43. Hayashi, Y., and Majewska, A. K. (2005). Dendritic spine geometry: functional implication and regulation. Neuron 46, 529-532.
44. Haynes, L. P., Fitzgerald, D. J., Wareing, B., O'Callaghan, D. W., Morgan, A., and Burgoyne, R. D. (2006). Analysis of the interacting partners of the neuronal calcium-binding proteins L-CaBP1, hippocalcin, NCS-1 and neurocalcin delta. Proteomics 6, 1822-1832.
45. Helias, M., Rotter, S., Gewaltig, M. O., and Diesmann, M. (2008). Structural plasticity controlled by calcium based correlation detection. Front. Comput. Neurosci. 2:7. doi: 10.3389/neuro.10.007.2008
46. 2+-free rat beta-parvalbumin (oncomodulin). ProteinSci. 16, 1914-1926.
47. Hirota, J., Michikawa, T., Natsume, M., Furuichi, T., and Mikoshiba, K. (1999). Calmodulin inhibits inositol 1, 4, 5-trisphosphate-induced calcium release through the purified and reconstituted inositol 1, 4, 5-trisphosphate receptor type 1. FEBS Lett. 456, 322-326.
48. Holbro, N., Grunditz, A., and Oertner, T. G. (2009). Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses. Proc. Natl. Acad. Sci. U.S.A. 106, 15055-15060.
49. Holbro, N., Grunditz, A., Wiegert, J. S., and Oertner, T. G. (2010). AMPA receptors gate spine Ca(2+) transients and spike-timing-dependent potentiation. Proc. Natl. Acad. Sci. U.S.A. 107, 15975-15980.
50. 2+ sensor calneurons requires the TRC40/Asna1 protein chaperone. J. Biol. Chem. 286, 36762-36776.
51. Huang, K. P., Huang, F. L., Jäger, T., Li, J., Reymann, K. G., and Balschun, D. (2004). Neurogranin/RC3 enhances long-term potentiation and learning by promoting calcium-mediated signaling. J. Neurosci. 24, 10660-10669.
52. Hui, H., McHugh, D., Hannan, M., Zeng, F., Xu, S. Z., Khan, S. H., Levenson, R., Beech, D. J., and Weiss, J. L. (2006). Calcium-sensing mechanism in TRPC5 channels contributing to retardation of neurite outgrowth. J. Physiol. 572, 165-172.
53. Jinno, S., and Kosaka, T. (2010). Stereological estimation of numerical densities of glutamatergic principal neurons in the mouse hippocampus. Hippocampus 20, 829-840.
54. 2+ sensors, NCS-1 and PICK1. Neuron 60, 1095-1111.
55. Jo, J., Son, G. H., Winters, B. L., Kim, M. J., Whitcomb, D. J., Dickinson, B. A., Lee, Y. B., Futai, K., Amici, M., Sheng, M., Collingridge, G. L., and Cho, K. (2010). Muscarinic receptors induce LTD of NMDAR EPSCs via a mechanism involving hippocalcin, AP2 and PSD-95. Nat. Neurosci. 13, 1216-1224.
56. Kabbani, N., Negyessy, L., Lin, R., Goldman-Rakic, P., and Levenson, R. (2002). Interaction with neuronal calcium sensor NCS-1 mediates desensitization of the D2 dopamine receptor. J. Neurosci. 22, 8476-8486.
57. Kakiuchi, S., Yasuda, S., Yamazaki, R., Teshima, Y., Kanda, K., Kakiuchi, R., and Sobue, K. (1982). Quantitative determinations of calmodulin in the supernatant and particulate fractions of mammalian tissues. J. Biochem. 92, 1041-1048.
58. Kapp-Barnea, Y., Melnikov, S., Shefler, I., Jeromin, A., and Sagi-Eisenberg, R. (2003). Neuronal calcium sensor-1 and phosphatidylinositol 4-kinase ß regulate IgE receptor-triggered exocytosis in cultured mast cells. J. Immunol. 171, 5320-5327.
59. Kasri, N. N., Holmes, A. M., Bultynck, G., Parys, J. B., Bootman, M. D., Rietdorf, K., Missiaen, L., McDonald, F., De Smedt, H., Conway, S. J., Holmes, A. B., Berridge, M. J., and Roderick, H. L. (2004). Regulation of InsP3 receptor activity by neuronal Ca2+-binding proteins. EMBO J. 23, 312-321.
60. Keller, D. X., Franks, K. M., Bartol, T. M. Jr., and Sejnowski, T. J. (2008). Calmodulin activation by calcium transients in the postsynap-tic density of dendritic spines. PLoS One 3:e2045. doi: 10.1371/jour-nal.pone.0002045
61. 2+-binding protein 1 in Xenopus oocytes. Pflugers Arch. 450, 345-354.
62. Kitajima, S., Seto-Ohshima, A., Sano, M., and Kato, K. (1983). Production of antibodies to calmodulin in rabbits and enzyme immunoassays for calmodulin and anti-calmodulin. J. Biochem. 94, 559-564.
63. Klee, C. B., and Vanaman, T. C. (1982). Calmodulin. Adv. Protein Chem. 35, 213-321.
64. Kubota, Y., Putkey, J. A., Shouval, H. Z., and Waxham, M. N. (2008). IQ-motif proteins influence intracellular free Ca2+ in hippocampal neurons through their interactions with calmodulin. J. Neurophysiol. 99, 264-276.
65. 2+/CaM signaling. Biophys. J. 93, 3848-3859.
66. 2+-calmodulin nano-domain in neuronal spines: a single molecule level analysis. PLoS Comput. Biol. 6:e1000987. doi: 10.1371/journal.pcbi.1000987
67. Kuo, H. C., Cheng, C. F., Clark, R. B., Lin, J. J., Lin, J. L., Hoshijima, M., Nguyêñ-Trân, V. T., Gu, Y., Ikeda, Y., Chu, P. H., Ross, J., Giles, W. R., and Chien, K. R. (2001). A defect in the Kv channel-interacting protein 2 (KChIP2) gene leads to a complete loss of I(to) and confers susceptibility to ventricular tachycardia. Cell 107, 801-813.
68. 2+-binding protein caldendrin: gene structure, splice isoforms and expression in the rat central nervous system. Mol. Cell. Neurosci. 19, 459-475.
69. 2+ channels. J. Neurosci. 20, 6830-6838.
70. 2+-binding protein 1. Nat. Neurosci. 5, 210-217.
71. Lindholm, D., Mercer, E. A., Yu, L. Y., Chen, Y., Kukkonen, J., Korhonen, L., and Arumäe, U. (2002). Neuronal apoptosis inhibitory protein: structural requirements for hippocalcin binding and effects on survival of NGF-dependent sympathetic neurons. Biochim. Biophys. Acta 1600, 138-147.
72. Lisman, J. E., and Zhabotinsky, A. M. (2001). A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 31, 191-201.
73. Lüscher, C., and Huber, K. M. (2010). Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron 65, 445-459.
74. Markram, H., Roth, A., and Helmchen, F. (1998). Competitive calcium binding: implications for dendritic calcium signaling. J. Comput. Neurosci. 5, 331-348.
75. McCue, H. V., Burgoyne, R. D., and Haynes, L. P. (2009). Membrane targeting of the EF-hand containing calcium-sensing proteins CaBP7 and CaBP8. Biochem. Biophys. Res. Commun. 380, 825-831.
76. 2+-sensing proteins CaBP7 and CaBP8. PLoS One 6:e17853. doi: 10.1371/jour-nal.pone.0017853
77. 2+-binding proteins. BMC Res. Notes 3, 118.
78. McCue, H. V., Haynes, L. P., and Burgoyne, R. D. (2010b). The diversity of calcium sensor proteins in the regulation of neuronal function. Cold Spring Harb. Perspect. Biol. 2, a004085.
79. 2+ sensor 1, the mammalian homologue of frequenin, is expressed in chromaffin and PC12 cells and regulates neurosecretion from dense-core granules. J. Biol. Chem. 273, 22768-22772.
80. Mercer, E. A., Korhonen, L., Skoglösa, Y., Olsson, P. A., Kukkonen, J. P., and Lindholm, D. (2000). NAIP interacts with hippocalcin and protects neurons against calcium-induced cell death through caspase-3-dependent and-independent pathways. EMBO J. 19, 3597-3607.
81. Meyer, T., Hanson, P. I., Stryer, L., and Schulman, H. (1992). Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science 256, 1199-1202.
82. 2+ signalling. J. Neurochem. 118, 695-713.
83. Mikhaylova, M., Reddy, P. P., Munsch, T., Landgraf, P., Suman, S. K., Smalla, K. H., Gundelfinger, E. D., Sharma, Y., and Kreutz, M. R. (2009). Calneurons provide a calcium threshold for trans-Golgi network to plasma membrane trafficking. Proc. Natl. Acad. Sci. U.S.A. 106, 9093-9098.
84. 2+ signaling via caldendrin and calneurons. Biochim. Biophys. Acta 1763, 1229-1237.
85. Nagata, K., Puls, A., Futter, C. I., Aspenstrom, P., Schaefer, E., Nakata, T., Hirokawa, N., and Hall, A. (1998). The MAP kinase kinase kinase MLK2 co-localizes with activated JNK along microtubules and associates with kinesin superfamily motor KIF3. EMBO J. 17, 149-158.
86. 2+-binding protein, as a regulator of Kv4 K-currents. Proc. Natl. Acad. Sci. U.S.A. 98, 12808-12813.
87. Neher, E., and Augustine, G. J. (1992). Calcium gradients and buffers in bovine chromaffin cells. J. Physiol. 450, 273-301.
88. 2+-mediated feedback loop in dendritic spines. Nat. Neurosci. 8, 642-649.
89. Nimchinsky, E. A., Yasuda, R., Oertner, T. G., and Svoboda, K. (2004). The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J. Neurosci. 24, 2054-2064.
90. 2+ signaling in dendrites. Neuron 46, 609-622.
91. O'Callaghan, D. W., Haynes, L. P., and Burgoyne, R. D. (2005). High-affinity interaction of the N-terminal myristoylation motif of the neuronal calcium sensor protein hippocalcin with phosphatidylinos-itol 4, 5-bisphosphate. Biochem. J. 391, 231-238.
92. 2+/myristoyl switch protein hippocalcin in living cells. J. Cell. Biol. 163, 715-721.
93. Ordaz, B., Tang, J., Xiao, R., Salgado, A., Sampieri, A., Zhu, M. X., and Vaca, L. (2005). Calmodulin and calcium interplay in the modulation of TRPC5 channel activity. J. Biol. Chem. 280, 30788-30796.
94. 2+ differentially regulate DNA binding and dimerization of DREAM. J. Biol. Chem. 280, 18008-18014.
95. Palmer, C. L., Lim, W., Hastie, P. G., Toward, M., Korolchuk, V. I., Burbidge, S. A., Banting, G., Collingridge, G. L., Isaac, J. T., and Henley, J. M. (2005). Hippocalcin functions as a calcium sensor in hippocampal LTD. Neuron 47, 487-494.
96. 2+ binding and implications for kinase activation. Protein Sci. 6, 794-807.
97. Redecker, P., Kreutz, M. R., Bockmann, J., Gundelfinger, E. D., and Boeckers, T. M. (2003). Brain synaptic junctional proteins at the acrosome of rat testicular germ cells. J. Histochem. Cytochem. 51, 809-819.
98. Résibois, A., and Rogers, J. H. (1992). Calretinin in rat brain: an immuno-histochemical study. Neuroscience 46, 101-134.
99. Rose, C. R., and Konnerth, A. (2001). Stores not just for storage: intracellular calcium release and synaptic plasticity. Neuron 31, 519-522.
100. Ruiz-Gomez, A., Mellström, B., Tornero, D., Morato, E., Savignac, M., Holguín, H., Aurrekoetxea, K., González, P., González-García, C., Ceña, V., Mayor, F. Jr., and Naranjo, J. R. (2007). G protein-coupled receptor kinase 2-mediated phosphorylation of downstream regulatory element antagonist modulator regulates membrane trafficking of Kv4.2 potassium channel. J. Biol. Chem. 282, 1205-1215.
101. 2+ signaling in dendritic spines. Curr. Opin. Neurobiol. 11, 349-356.
102. 2+ ions in dendritic spines. Neuron 33, 439-452.
103. Sano, M., and Kitajima, S. (1983). Ontogeny of calmodulin and calmodulin-dependent adenylate cyclase in rat brain. Brain Res. 283, 215-220.
104. Schaad, N. C., De Castro, E., Nef, S., Hegi, S., Hinrichsen, R., Martone, M. E., Ellisman, M. H., Sikkink, R., Rusnak, F., Sygush, J., and Nef, P. (1996). Direct modulation of calmodulin targets by the neuronal calcium sensor NCS-1. Proc. Natl. Acad. Sci. U.S.A. 93, 9253-9258.
105. Schlecker, C., Boehmerle, W., Jeromin, A., DeGray, B., Varshney, A., Sharma, Y., Szigeti-Buck, K., and Ehrlich, B. E. (2006). Neuronal calcium sensor-1 enhancement of InsP3 receptor activity is inhibited by therapeutic levels of lithium. J. Clin. Invest. 116, 1668-1674.
106. Schmidt, H., and Eilers, J. (2009). Spine neck geometry determines spino-dendritic cross-talk in the presence of mobile endogenous calcium binding proteins. J. Comput. Neurosci. 27, 229-243.
107. Schmidt, H., Schwaller, B., and Eilers, J. (2005). Calbindin D28k targets myo-inositol monophosphatase in spines and dendrites of cerebellar Purkinje neurons. Proc. Natl. Acad. Sci. U.S.A. 102, 5850-5855.
108. 2+ buffers. Cold Spring Harb. Perspect. Biol. 2, a004051.
109. Schwaller, B. (2011). The use of transgenic mouse models to reveal the functions of Ca(2+) buffer proteins in excitable cells. Biochim. Biophys. Acta doi: 10.1016/j.bbagen.2011.11.008. [Epub ahead of print].
110. Segal, M. (2001). Rapid plasticity of dendritic spine: hints to possible functions? Prog. Neurobiol. 63, 61-70.
111. 2+-sensor proteins. J. Mol. Biol. 336, 957-970.
112. Seidenbecher, C. I., Langnaese, K., Sanmartí-Vila, L., Boeckers, T. M., Smalla, K. H., Sabel, B. A., Garner, C. C., Gundelfinger, E. D., and Kreutz, M. R. (1998). Caldendrin, a novel neuronal calcium-binding protein confined to the somato-dendritic compartment. J. Biol. Chem. 273, 21324-21331.
113. Simon, S. M., and Llinás, R. R. (1985). Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys. J. 48, 485-498.
114. Sloviter, R. S. (1989). Calcium-binding protein (calbindin-D28k) and par-valbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J. Comp. Neurol. 280, 183-196.
115. Smalla, K. H., Seidenbecher, C. I., Tischmeyer, W., Schicknick, H., Wyneken, U., Böckers, T. M., Gundelfinger, E. D., and Kreutz, M. R. (2003). Kainate-induced epileptic seizures induce a recruitment of caldendrin to the postsynaptic density in rat brain. Mol. Brain Res. 116, 159-162.
116. Spacek, J., and Harris, K. M. (1997). Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci. 17, 190-203.
117. Stuart, R. O., Bush, K. T., and Nigam, S. K. (2003). Changes in gene expression patterns in the ureteric bud and metanephric mesenchyme in models of kidney development. Kidney Int. 64, 1997-2008.
118. 2+ channel. Cell 133, 1228-1240.
119. Takashima, N., Odaka, Y. S., Sakoori, K., Akagi, T., Hashikawa, T., Morimura, N., Yamada, K., and Aruga, J. (2011). Impaired cognitive function and altered hippocampal synapse morphology in mice lacking Lrrtm1, a gene associated with schizophrenia. PLoS One 6:e22716. doi: 10.1371/jour-nal.pone.0022716
120. Teolato, S., Calderini, G., Bonetti, A. C., and Toffano, G. (1983). Calmodulin content in different brain areas of aging rats. Neurosci. Lett. 38, 57-60.
121. 2+ channels. J. Biol. Chem. 282, 8464-8473.
122. Toresson, H., and Grant, S. G. (2005). Dynamic distribution of endoplasmic reticulum in hippocampal neuron dendritic spines. Eur. J. Neurosci. 22, 1793-1798.
123. Vargas, F., and Guidotti, A. (1980). Calmodulin in brain of schizophrenics. Neurochem. Res. 5, 673-681.
124. Wang, Q., Liang, K. C., Czader, A., Waxham, M. N., and Cheung, M. S. (2011). The effect of macromolecular crowding, ionic strength and calcium binding on calmodulin dynamics. PLoS Comput. Biol. 7:e1002114. doi: 10.1371/journal.pcbi.1002114
125. 2+ binding to CaBP1, a neuron-specific regulator of calcium channels. J. Biol. Chem. 280, 37461-37470.
126. Woll, M. P., De Cotiis, D. A., Bewley, M. C., Tacelosky, D. M., Levenson, R., and Flanagan, J. M. (2011). Interaction between the D2 dopamine receptor and neuronal calcium sensor-1 analyzed by fluorescence anisotropy. Biochemistry 50, 8780-8791.
127. Wu, L. J., Mellström, B., Wang, H., Ren, M., Domingo, S., Kim, S. 5., Li, X. Y., Chen, T., Naranjo, J. R., and Zhuo, M. (2010). DREAM (Downstream Regulatory Element Antagonist Modulator) contributes to synaptic depression and contextual fear memory. Mol. Brain 3, 3.
128. Wu, Y. Q., Lin, X., Liu, C. M., Jamrich, M., and Shaffer, L. G. (2001). Identification of a human brain-specific gene, calneuron 1, a new member of the calmodulin superfamily. Mol. Genet. Metab. 72, 343-350.
129. Xia, Z., and Storm, D. R. (2005). The role of calmodulin as a signal integrator for synaptic plasticity. Nat. Rev. Neurosci. 6, 267-276.
130. 2+ release channels. Proc. Natl. Acad. Sci. U.S.A. 99, 7711-7716.
131. Yuste, R., Majewska, A., and Holthoff, K. (2000). From form to function: calcium compartmentalization in dendritic spines. Nat. Neurosci. 3, 653-659.
132. Yuste, R., and Denk, W. (1995). Dendritic spines as basic functional units of neuronal integration. Nature 375, 682-684.
133. Zhang, Y., Su, P., Liang, P., Liu, T., Liu, X., Liu, X. Y., Zhang, B., Han, T., Zhu, Y. B., Yin, D. M., Li, J., Zhou, Z., Wang, K. W., and Wang, Y. (2010). The DREAM protein negatively regulates the NMDA receptor through interaction with the NR1 subunit. J. Neurosci. 30, 7575-7586.
134. 2+ channels. J. Neurosci. 24, 4698-4708.
135. 2+-binding protein-1. J. Biol. Chem. 280, 29612-29619.