Displacement of α-actinin from the NMDA receptor NR1 C0 domain by Ca2+/calmodulin promotes CaMKII binding

Biochemistry

Volumn 46, Issue 29, 2007, Pages 8485-8497

  Merrill, Michelle A ^a   Malik, Zulfiqar ^a   Akyol, Zeynep ^a   Bartos, Jason A ^a   Leonard, A Soren ^a   Hudmon, Andy ^b   Shea, Madeline A ^a   Hell, Johannes W ^a  

^a UNIVERSITY OF IOWA   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CALCIUM COMPOUNDS; COMPLEXATION; ENZYME ACTIVITY; PLASTICITY; SIGNAL TRANSDUCTION;

CALMODULIN; N-METHYL-D-ASPARTATE (NMDA); POSTSYNAPTIC ACCUMULATION;

PROTEINS;

ALPHA ACTININ; CALCIUM ION; CALMODULIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PROTEIN KINASE (CALCIUM,CALMODULIN) II;

AMINO TERMINAL SEQUENCE; ARTICLE; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVATION; ENZYME ACTIVITY; NEGATIVE FEEDBACK; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ACTININ; ANIMALS; BINDING SITES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CALMODULIN; HUMANS; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 34547135936     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0623025     Document Type: Article

References (64)

1. Soderling, T. R., Chang, B., and Brickey, D. (2001) Cellular signaling through multifunctional Ca2+/calmodulin-dependent protein kinase II, J. Biol. Chem. 276, 3719-3722.
2. Malenka, R. C., and Nicoll, R. A. (1999) Long-term potentiation-a decade of progress? Science 285, 1870-1874.
3. Martin, S. J., Grimwood, P. D., and Morris, R. G. (2000) Synaptic plasticity and memory: an evaluation of the hypothesis, Annu. Rev. Neurosci. 23, 649-711.
4. Malenka, R. C., and Bear, M. F. (2004) LTP and LTD: an embarrassment of riches, Neuron 44, 5-21.
5. Collingridge, G. L., Isaac, J. T., and Wang, Y. T. (2004) Receptor trafficking and synaptic plasticity, Nat. Rev. Neurosci. 5, 952-962.
6. Leonard, A. S., Lim, I. A., Hemsworth, D. E., Horne, M. C., and Hell, J. W. (1999) Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor, Proc. Natl. Acad. Sci. U.S.A. 96, 3239-3244.
7. Leonard, A. S., Bayer, K.-U., Merrill, M. A., Lim, I. A., Shea, M. A., Schulman, H., and Hell, J. W. (2002) Regulation of calcium/calmodulin-dependent protein kinase II docking to N-methyl-D-aspartate receptors by calcium/calmodulin and α-actinin, J. Biol. Chem. 277, 48441-48448.
8. Gardoni, F., Schrama, L. H., van Dalen, J. J., Gispen, W. H., Cattabeni, F., and Di Luca, M. (1999) AlphaCaMKII binding to the C-terminal tail of NMDA receptor subunit NR2A and its modulation by autophosphorylation, FEBS Lett. 456, 394-398.
9. Gardoni, F., Caputi, A., Cimino, M., Pastorino, L., Cattabeni, F., and Di, Luca, M. (1998) Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities, J. Neurochem. 71, 1733-1741.
10. Strack, S., and Colbran, R. J. (1998) Autophosphorylation-dependent targeting of calcium/calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-D-aspartate receptor, J. Biol. Chem. 273, 20689-20692.
11. Strack, S., McNeill, R. B., and Colbran, R. J. (2000) Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B subunit of the N-methyl-D-aspartate receptor, J. Biol. Chem. 275, 23798-23806.
12. Bayer, K. U., De, Koninck, P., Leonard, A. S., Hell, J. W., and Schulman, H. (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation, Nature 411, 801-805.
13. Robison, A. J., Bartlett, R. K., Bass, M. A., and Colbran, R. J. (2005) Differential modulation of Ca2+/calmodulin-dependent protein kinase II activity by regulated interactions with N-methyl-D-aspartate receptor NR2B subunits and α-actinin, J. Biol. Chem. 280, 39316-39323.
14. Robison, A. J., Bass, M. A., Jiao, Y., Macmillan, L. B., Carmody, L. C., Bartlett, R. K., and Colbran, R. J. (2005) Multivalent interactions of calcium/calmodulin-dependent protein kinase II with the postsynaptic density proteins NR2B, densin-180, and α-actinin-2, J. Biol. Chem. 280, 35329-35336.
15. Colbran, R. J. (2004) Targeting of calcium/calmodulin-dependent protein kinase II, Biochem. J. 378, 1-16.
16. Merrill, M. A., Chen, Y., Strack, S., and Hell, J. W. (2005) Activity-driven postsynaptic translocation of CaMKII, Trends Pharmacol. Sci. 26, 645-653.
17. Barria, A., Muller, D., Derkach, V., Griffith, L. C., and Soderling, T. R. (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation, Science 276, 2042-2045.
18. Lee, H. K., Barbarosie, M., Kameyama, K., Bear, M. F., and Huganir, R. L. (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity, Nature 405, 955-959.
19. Lee, H. K., Takamiya, K., Han, J. S., Man, H., Kim, C. H., Rumbaugh, G., Yu, S., Ding, L., He, C., Petralia, R. S., Wenthold, R. J., Gallagher, M., and Huganir, R. L. (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory, Cell 112, 631-643.
20. Seeburg, P. H. (1993) The molecular biology of mammalian glutamate receptor channels, Trends Pharmacol. Sci. 14, 297-303.
21. Hollmann, M., and Heinemann, S. (1994) Cloned glutamate receptors, Annu. Rev. Neurosci. 17, 31-108.
22. Sheng, M., Cummings, J., Roldan, L. A., Jan, Y. N., and Jan, L. Y. (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex, Nature 368, 144-147.
23. Blahos, J., II, and Wenthold, R. J. (1996) Relationship between N-methyl-D-aspartate receptor NR1 splice variants and NR2 subunits, J. Biol. Chem. 271, 15669-15674.
24. Ehlers, M. D., Zhang, S., Bernhardt, J. P., and Huganir, R. L. (1996) Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit, Cell 84, 745-755.
25. Wyszynski, M., Lin, J., Rao, A., Nigh, E., Beggs, A. H., Craig, A. M., and Sheng, M. (1997) Competitive binding of α-actinin and calmodulin to the NMDA receptor, Nature 385, 439-442.
26. Akyol, Z., Bartos, J. A., Merrill, M. A., Faga, L. A., Jaren, O. R., Shea, M. A., and Hell, J. W. (2004) Apo-calmodulin binds with its C-terminal domain to the N-methyl-D-aspartate receptor NR1 C0 region, J. Biol. Chem. 279, 2166-2175.
27. Rosenmund, C., and Westbrook, G. L. (1993) Calcium-induced actin depolymerization reduces NMDA channel activity, Neuron 10, 805-814.
28. Zhang, S., Ehlers, M. D., Bernhardt, J. P., Su, C. T., and Huganir, R. L. (1998) Calmodulin mediates calcium-dependent inactivation of N-methyl-D-aspartate receptors, Neuron 21, 443-453.
29. Krupp, J. J., Vissel, B., Thomas, C. G., Heinemann, S. F., and Westbrook, G. L. (1999) Interactions of calmodulin and alpha-actinin with the NR1 subunit modulate Ca2+-dependent inactivation of NMDA receptors, J. Neurosci. 19, 1165-1178.
30. Elgersma, Y., Fedorov, N. B., Ikonen, S., Choi, E. S., Elgersma, M., Carvalho, O. M., Giese, K. P., and Silva, A. J. (2002) Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning, Neuron 36, 493-505.
31. Sorensen, B. R., and Shea, M. A. (1998) Interactions between domains of apo calmodulin alter calcium binding and stability, Biochemistry 37, 4244-4253.
32. Bradshaw, J. M., Hudmon, A., and Schulman, H. (2002) Chemical quenched flow kinetic studies indicate an intraholoenzyme autophosphorylation mechanism for Ca2+/calmodulin-dependent protein kinase II, J. Biol. Chem. 277, 20991-20998.
33. Bhatt, A., Kaverina, I., Otey, C., and Huttenlocher, A. (2002) Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain, J. Cell Sci. 115, 3415-3425.
34. Edlund, M., Lotano, M. A., and Otey, C. A. (2001) Dynamics of alpha-actinin in focal adhesions and stress fibers visualized with alpha-actinin-green fluorescent protein, Cell Motil. Cytoskeleton 48, 190-200.
35. Klee, C. B., Crouch, T. H., and Krinks, M. H. (1979) Calcineurin: a calcium- and calmodulin-binding protein of the nervous system, Proc. Natl. Acad. Sci. U.S.A. 76, 6270-6273.
36. Grab, D. J., Berzins, K., Cohen, R. S., and Siekevitz, P. (1979) Presence of calmodulin in postsynaptic densities isolated from canine cerebral cortex, J. Biol. Chem. 254, 8690-8696.
37. Fabiato, A., and Fabiato, F. (1979) Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells, J. Physiol. (Paris) 75, 463-505.
38. Martell, A., and Sillen, L., (Eds.) (1971) Stability Constants of Metal Ion Comples. Supplement No. 1, The Chemical Society, London.
39. Hashimoto, Y., Schworer, C. M., Colbran, R. J., and Soderling, T. R. (1987) Autophosphorylation of Ca2+/calmodulin-dependent protein kinase II. Effects on total and Ca2+-independent activities and kinetic parameters, J. Biol. Chem. 262, 8051-8055.
40. Lou, L. L., and Schulman, H. (1989) Distinct autophosphorylation sites sequentially produce autonomy and inhibition of the multifunctional Ca2+/calmodulin-dependent protein kinase, J. Neurosci. 9, 2020-2032.
41. Davare, M. A., and Hell, J. W. (2003) Increased phosphorylation of the neuronal L-type Ca(2+) channel Ca(v)1.2 during aging, Proc. Natl. Acad. Sci. U.S.A. 100, 16018-16023.
42. Hall, D. D., Feekes, J. A., Arachchige, Don, A. S., Shi, M., Hamid, J., Chen, L., Strack, S., Zamponi, G. W., Home, M. C., and Hell, J. W. (2006) Binding of protein phosphatase 2A to the L-type calcium channel Cav1.2 next to Ser1928, its main PKA site, is critical for Ser1928 dephosphorylation, Biochemistry 45, 3448-3459.
43. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, 2d ed., Kluwer Academic, New York.
44. Beggs, A. H., Byers, T. J., Knoll, J. H., Boyce, F. M., Bruns, G. A., and Kunkel, L. M. (1992) Cloning and characterization of two human skeletal muscle alpha-actinin genes located on chromosomes 1 and 11, J. Biol. Chem. 267, 9281-9288.
45. Tang, J., Taylor, D. W., and Taylor, K. A. (2001) The three-dimensional structure of alpha-actinin obtained by cryoelectron microscopy suggests a model for Ca(2+)-dependent actin binding, J. Mol. Biol. 310, 845-858.
46. Walikonis, R. S., Jensen, O. N., Mann, M., Provance, D. W., Jr., Mercer, J. A., and Kennedy, M. B. (2000) Identification of proteins in the postsynaptic density fraction by mass spectrometry, J. Neurosci. 20, 4069-4080.
47. Peng, J., Kim, M. J., Cheng, D., Duong, D. M., Gygi, S. P., and Sheng, M. (2004) Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry, J. Biol. Chem. 279, 21003-21011.
48. Meador, W. E., Means, A. R., and Quiocho, F. A. (1993) Modulation of calmodulin plasticity in molecular recognition on the basis of x-ray structures, Science 262, 1718-1721.
49. Strack, S., Choi, S., Lovinger, D. M., and Colbran, R. J. (1997) Translocation of autophosphorylated calcium/calmodulin-dependent protein kinase II to the postsynaptic density, J. Biol. Chem. 272, 13467-13470.
50. Shen, K., and Meyer, T. (1999) Dynamic control of CaMKII Translocation in hippocampal neurons by NMDA receptor stimulation, Science 284, 162-166.
51. Shen, K., Teruel, M. N., Connor, J. H., Shenolikar, S., and Meyer, T. (2000) Molecular memory by reversible translocation of calcium/calmodulin- dependent protein kinase II, Nat. Neurosci. 3, 881-886.
52. Gleason, M. R., Higashijima, S., Dallman, J., Liu, K., Mandel, G., and Fetcho, J. R. (2003) Translocation of CaM kinase II to synaptic sites in vivo, Nat. Neurosci. 6, 217-218.
53. Otmakhov, N., Tao-Cheng, J. H., Carpenter, S., Asrican, B., Dosemeci, A., Reese, T. S., and Lisman, J. (2004) Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation, J. Neurosci. 24, 9324-9331.
54. Gu, Z., Jiang, Q., Yuen, E. Y., and Yan, Z. (2006) Activation of dopamine D4 receptors induces synaptic translocation of Ca2+/ calmodulin-dependent protein kinase II in cultured prefrontal cortical neurons, Mol. Pharmacol. 69, 813-822.
55. Strack, S., Robison, A. J., Bass, M. A., and Colbran, R. J. (2000) Association of calcium/calmodulin-dependent kinase II with developmentally regulated splice variants of the postsynaptic density protein densin-180, J. Biol. Chem. 275, 25061-25064.
56. Walikonis, R. S., Oguni, A., Khorosheva, E. M., Jeng, C. J., Asuncion, F. J., and Kennedy, M. B. (2001) Densin-180 forms a ternary complex with the (alpha)-subunit of Ca2+/calmodulin-dependent protein kinase II and (alpha)-actinin, J. Neurosci. 21, 423-433.
57. Dhavan, R., Greer, P. L., Morabito, M. A., Orlando, L. R., and Tsai, L. H. (2002) The cyclin-dependent kinase 5 activators p35 and p39 interact with the alpha-subunit of Ca2+/calmodulin-dependent protein kinase II and alpha-actinin-1 in a calcium-dependent manner, J. Neurosci. 22, 7879-7891.
58. Hudmon, A., and Schulman, H. (2002) Neuronal CA2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function, Annu. Rev. Biochem. 71, 473-510.
59. Sessoms-Sikes, S., Honse, Y., Lovinger, D. M., and Colbran, R. J. (2005) CaMKIIalpha enhances the desensitization of NR2B-containing NMDA receptors by an autophosphorylation-dependent mechanism, Mol. Cell. Neurosci. 29, 139-147.
60. Hudmon, A., and Schulman, H. (2002) Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II, Biochem. J. 364, 593-611.
61. Hudmon, A., Lebel, E., Roy, H., Sik, A., Schulman, H., Waxham, M. N., and De Koninck, P. (2005) A mechanism for Ca2+/ calmodulin-dependent protein kinase II clustering at synaptic and nonsynaptic sites based on self-association, J. Neurosci. 25, 6971-6983.
62. 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.
63. Lisman, J., Schulman, H., and Cline, H. (2002) The molecular basis of CaMKII function in synaptic and behavioral memory, Nat. Neurosci. 3, 175-190.
64. Matsuzaki, M., Honkura, N., Ellis-Davies, G. C., and Kasai, H. (2004) Structural basis of long-term potentiation in single dendritic spines, Nature 429, 761-766.