Decoding glutamate receptor activation by the Ca2+ sensor protein hippocalcin in rat hippocampal neurons

European Journal of Neuroscience

Volumn 32, Issue 3, 2010, Pages 347-358

  Dovgan, A V ^a   Cherkas, V P ^a   Stepanyuk, A R ^a   Fitzgerald, D J ^b   Haynes, L P ^b   Tepikin, A V ^b   Burgoyne, R D ^b   Belan, P V ^a  

^a BOGOMOLETZ INSTITUTE OF PHYSIOLOGY   (Ukraine)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

NCS proteins; NMDA receptors; signal transduction; synapse; translocation

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; HIPPOCALCIN; MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEURONAL CALCIUM SENSOR; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DENDRITIC SPINE; DEPOLARIZATION; HIPPOCAMPUS; LEARNING; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPSE VESICLE;

ANIMALS; CALCIUM; CALCIUM CHANNELS; DENDRITIC SPINES; GLUTAMIC ACID; HIPPOCALCIN; HIPPOCAMPUS; MEMBRANE POTENTIALS; NEURONS; RATS; RECEPTORS, GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 77955140533     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07303.x     Document Type: Article

References (40)

1. Ames, J.B., Ishima, R., Tanaka, T., Gordon, J.I., Stryer, L. Ikura, M. (1997) Molecular mechanics of calcium-myristoyl switches. Nature, 389, 198 202.
2. 2+store in the plasticity of central neurons. Trends Pharmacol. Sci., 27, 78 84.
3. Bayley, P., Ahlstrom, P., Martin, S.R. Forsen, S. (1984) The kinetics of calcium binding to calmodulin: Quin 2 and ANS stopped-flow fluorescence studies. Biochem.Biophys.Res.Commun., 120, 185 191.
4. Ben Ari, Y. (2001) Developing networks play a similar melody. Trends Neurosci., 24, 353 360.
5. Bezprozvanny, I. (2005) The inositol 1,4,5-trisphosphate receptors. Cell Calcium, 38, 261 272.
6. Bloodgood, B.L. Sabatini, B.L. (2007) Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron, 53, 249 260.
7. 2+-sensor proteins: from Alzheimer's disease to cancer. Trends Pharmacol.Sci., 26, 345 351.
8. 2+-sensor proteins: multitalented regulators of neuronal function. Trends Neurosci., 27, 203 209.
9. Dickinson, B., Jo, J., Seok, H., Son, G., Whitcomb, D., Davies, C., Sheng, M., Collingridge, G. Cho, K. (2009) A novel mechanism of hippocampal LTD involving muscarinic receptor-triggered interactions between AMPARs, GRIP and liprin-alpha. Molecular Brain, 2, 18.
10. Furuta, Y., Kobayashi, M., Masaki, T. Takamatsu, K. (1999) Age-related changes in expression of hippocalcin and NVP2 in rat brain. Neurochem.Res., 24, 651 658.
11. Haynes, L.P., Fitzgerald, D.J., Wareing, B., O'Callaghan, D.W., Morgan, A. 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.
12. Holmes, W.R. (2000) Models of calmodulin trapping and CaM kinase II activation in a dendritic spine. J Comput.Neurosci, 8, 65 85.
13. Jinno, S., Jeromin, A. Kosaka, T. (2004) Expression and possible role of neuronal calcium sensor-1 in the cerebellum. Cerebellum., 3, 83 88.
14. Jo, J., Heon, S., Kim, M.J., Son, G.H., Park, Y., Henley, J.M., Weiss, J.L., Sheng, M., Collingridge, G.L. Cho, K. (2008) Metabotropic glutamate receptor-mediated LTD involves two interacting Ca(2+) sensors, NCS-1 and PICK1. Neuron, 60, 1095 1111.
15. Kakiuchi, S., Yasuda, S., Yamazaki, R., Teshima, Y., Kanda, K., Kakiuchi, R. Sobue, K. (1982) Quantitative determinations of calmodulin in the supernatant and particulate fractions of mammalian tissues. J. Biochem., 92, 1041 1048.
16. Kobayashi, M., Takamatsu, K., Saitoh, S. Noguchi, T. (1993) Myristoylation of hippocalcin is linked to its calcium-dependent membrane association properties. J Biol.Chem., 268, 18898 18904.
17. Kobayashi, M., Masaki, T., Hori, K., Masuo, Y., Miyamoto, M., Tsubokawa, H., Noguchi, H., Nomura, M. Takamatsu, K. (2005) Hippocalcin-deficient mice display a defect in cAMP response element-binding protein activation associated with impaired spatial and associative memory. Neuroscience, 133, 471 484.
18. Korhonen, L., Hansson, I., Kukkonen, J.P., Brannvall, K., Kobayashi, M., Takamatsu, K. Lindholm, D. (2005) Hippocalcin protects against caspase-12-induced and age-dependent neuronal degeneration. Mol.Cell Neurosci., 28, 85 95.
19. Lindholm, D., Mercer, E.A., Yu, L.Y., Chen, Y., Kukkonen, J., Korhonen, L. Arumae, 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.
20. Majewska, A., Tashiro, A. Yuste, R. (2000) Regulation of spine calcium dynamics by rapid spine motility. J. Neurosci., 20, 8262 8268.
21. Mangan, P.S. Kapur, J. (2004) Factors underlying bursting behavior in a network of cultured hippocampal neurons exposed to zero magnesium. J. Neurophysiol., 91, 946 957.
22. Markova, O., Fitzgerald, D., Stepanyuk, A., Dovgan, A., Cherkas, V., Tepikin, A., Burgoyne, R.D. Belan, P. (2008) Hippocalcin signaling via site-specific translocation in hippocampal neurons. Neurosci.Lett., 442, 152 157.
23. 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.
24. Melnick, I.V., Chvanov, M.A. Belan, P.V. (1999) Rat hippocampal neurons maintain their own GABAergic synaptic transmission in culture. Neurosci. Lett., 262, 151 154.
25. Micheva, K.D., Holz, R.W. Smith, S.J. (2001) Regulation of presynaptic phosphatidylinositol 4,5-biphosphate by neuronal activity. J. Cell Biol., 154, 355 368.
26. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B. Seeburg, P.H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron, 12, 529 540.
27. 2+signal transduction. J Biol.Chem., 277, 14227 14237.
28. 2+/myristoyl switch protein hippocalcin in living cells. J. Cell Biol., 163, 715 721.
29. O'Callaghan, D.W., Haynes, L.P. Burgoyne, R.D. (2005) High-affinity interaction of the N-terminal myristoylation motif of the neuronal calcium sensor protein hippocalcin with phosphatidylinositol 4,5-bisphosphate. Biochem.J, 391, 231 238.
30. Palmer, C.L., Lim, W., Hastie, P.G., Toward, M., Korolchuk, V.I., Burbidge, S.A., Banting, G., Collingridge, G.L., Isaac, J.T. Henley, J.M. (2005) Hippocalcin functions as a calcium sensor in hippocampal LTD. Neuron, 47, 487 494.
31. 2+binding studied with a microfluidic mixer. Proc. Natl Acad. Sci. USA, 105, 542 547.
32. Sabatini, B.L., Oertner, T.G. Svoboda, K. (2002) The life cycle of Ca(2+) ions in dendritic spines. Neuron, 33, 439 452.
33. Sharma, K., Fong, D.K. Craig, A.M. (2006) Postsynaptic protein mobility in dendritic spines: long-term regulation by synaptic NMDA receptor activation. Mol.Cell Neurosci, 31, 702 712.
34. Teruel, M.N. Meyer, T. (2000) Translocation and reversible localization of signaling proteins: a dynamic future for signal transduction. Cell, 103, 181 184.
35. Tzingounis, A.V. Nicoll, R.A. (2008) Contribution of KCNQ2 and KCNQ3 to the medium and slow afterhyperpolarization currents. Proc.Natl.Acad.Sci.USA, 105, 19974 19979.
36. Tzingounis, A.V., Kobayashi, M., Takamatsu, K. Nicoll, R.A. (2007) Hippocalcin gates the calcium activation of the slow afterhyperpolarization in hippocampal pyramidal cells. Neuron, 53, 487 493.
37. van der Wal, J., Habets, R., Varnai, P., Balla, T. Jalink, K. (2001) Monitoring agonist-induced phospholipase C activation in live cells by fluorescence resonance energy transfer. J Biol.Chem., 276, 15337 15344.
38. Walther, H., Lambert, J.D., Jones, R.S., Heinemann, U. Hamon, B. (1986) Epileptiform activity in combined slices of the hippocampus, subiculum and entorhinal cortex during perfusion with low magnesium medium. Neurosci. Lett., 69, 156 161.
39. Yasuda, R., Harvey, C.D., Zhong, H., Sobczyk, A., van Aelst, L. Svoboda, K. (2006) Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging. Nat.Neurosci., 9, 283 291.
40. Zheng, Q., Bobich, J.A., Vidugiriene, J., McFadden, S.C., Thomas, F., Roder, J. Jeromin, A. (2005) Neuronal calcium sensor-1 facilitates neuronal exocytosis through phosphatidylinositol 4-kinase. J. Neurochem., 92, 442 451.