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. 1991 Jun 15;88(12):5374–5378. doi: 10.1073/pnas.88.12.5374

Possible role for calmodulin and the Ca2+/calmodulin-dependent protein kinase II in postsynaptic neurotransmission.

P Siekevitz 1
PMCID: PMC51875  PMID: 1647030

Abstract

The theory presented here is based on results from in vitro experiments and deals with three proteins in the postsynaptic density/membrane-namely, calmodulin, the Ca2+/calmodulin-dependent protein kinase, and the voltage-dependent Ca2+ channel. It is visualized that, in vivo in the polarized state of the membrane, calmodulin is bound to the kinase; upon depolarization of the membrane and the intrusion of Ca2+, Ca2(+)-bound calmodulin activates the autophosphorylation of the kinase. Calmodulin is visualized as having less affinity for the phosphorylated form of the kinase and is translocated to the voltage-dependent Ca2+ channel. There, with its bound Ca2+, it acts as a Ca2+ sensor, to close off the Ca2+ channel of the depolarized membrane. At the same time, it is thought that the configuration of the kinase is altered by its phosphorylated states; by interacting with Na+ and K+ channels, it alters the electrical properties of the membrane to regain the polarized state. Calmodulin is moved to the unphosphorylated kinase to complete the cycle, allowing the voltage-dependent Ca2+ channel to be receptive to Ca2+ flux upon the next cycle of depolarization. Thus, the theory tries to explain (i) why calmodulin and the kinase reside at the postsynaptic density/membrane site, and (ii) what function autophosphorylation of the kinase may play.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anthony F. A., Winkler M. A., Edwards H. H., Cheung W. Y. Quantitative subcellular localization of calmodulin-dependent phosphatase in chick forebrain. J Neurosci. 1988 Apr;8(4):1245–1253. doi: 10.1523/JNEUROSCI.08-04-01245.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Apel E. D., Byford M. F., Au D., Walsh K. A., Storm D. R. Identification of the protein kinase C phosphorylation site in neuromodulin. Biochemistry. 1990 Mar 6;29(9):2330–2335. doi: 10.1021/bi00461a017. [DOI] [PubMed] [Google Scholar]
  3. Berman R. F., Hullihan J. P., Kinnier W. J., Wilson J. E. In vivo phosphorylation of postsynaptic density proteins. Neuroscience. 1984 Nov;13(3):965–971. doi: 10.1016/0306-4522(84)90111-8. [DOI] [PubMed] [Google Scholar]
  4. Blaustein M. P. Calcium transport and buffering in neurons. Trends Neurosci. 1988 Oct;11(10):438–443. doi: 10.1016/0166-2236(88)90195-6. [DOI] [PubMed] [Google Scholar]
  5. Carafoli E. Intracellular calcium homeostasis. Annu Rev Biochem. 1987;56:395–433. doi: 10.1146/annurev.bi.56.070187.002143. [DOI] [PubMed] [Google Scholar]
  6. Carlin R. K., Grab D. J., Cohen R. S., Siekevitz P. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol. 1980 Sep;86(3):831–845. doi: 10.1083/jcb.86.3.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carlin R. K., Grab D. J., Siekevitz P. Function of a calmodulin in postsynaptic densities. III. Calmodulin-binding proteins of the postsynaptic density. J Cell Biol. 1981 Jun;89(3):449–455. doi: 10.1083/jcb.89.3.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carlin R. K., Siekevitz P. Characterization of Na+-independent GABA and flunitrazepam binding sites in preparations of synaptic membranes and postsynaptic densities isolated from canine cerebral cortex and cerebellum. J Neurochem. 1984 Oct;43(4):1011–1017. doi: 10.1111/j.1471-4159.1984.tb12837.x. [DOI] [PubMed] [Google Scholar]
  9. Cheung W. Y. Biological functions of calmodulin. Harvey Lect. 1983 1984;79:173–216. [PubMed] [Google Scholar]
  10. Colbran R. J., Schworer C. M., Hashimoto Y., Fong Y. L., Rich D. P., Smith M. K., Soderling T. R. Calcium/calmodulin-dependent protein kinase II. Biochem J. 1989 Mar 1;258(2):313–325. doi: 10.1042/bj2580313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cotman C., Monaghan D. Multiple excitatory amino acid receptor regulation of intracellular Ca2+. Implications for aging and Alzheimer's disease. Ann N Y Acad Sci. 1989;568:138–148. doi: 10.1111/j.1749-6632.1989.tb12501.x. [DOI] [PubMed] [Google Scholar]
  12. Cox J. A. Sequential events in calmodulin on binding with calcium and interaction with target enzymes. Fed Proc. 1984 Dec;43(15):3000–3004. [PubMed] [Google Scholar]
  13. Crouch T. H., Klee C. B. Positive cooperative binding of calcium to bovine brain calmodulin. Biochemistry. 1980 Aug 5;19(16):3692–3698. doi: 10.1021/bi00557a009. [DOI] [PubMed] [Google Scholar]
  14. Dunkley P. R., Baker C. M., Robinson P. J. Depolarization-dependent protein phosphorylation in rat cortical synaptosomes: characterization of active protein kinases by phosphopeptide analysis of substrates. J Neurochem. 1986 Jun;46(6):1692–1703. doi: 10.1111/j.1471-4159.1986.tb08486.x. [DOI] [PubMed] [Google Scholar]
  15. Fagg G. E., Matus A. Selective association of N-methyl aspartate and quisqualate types of L-glutamate receptor with brain postsynaptic densities. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6876–6880. doi: 10.1073/pnas.81.21.6876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fukunaga K., Rich D. P., Soderling T. R. Generation of the Ca2(+)-independent form of Ca2+/calmodulin-dependent protein kinase II in cerebellar granule cells. J Biol Chem. 1989 Dec 25;264(36):21830–21836. [PubMed] [Google Scholar]
  17. Goldenring J. R., McGuire J. S., Jr, DeLorenzo R. J. Identification of the major postsynaptic density protein as homologous with the major calmodulin-binding subunit of a calmodulin-dependent protein kinase. J Neurochem. 1984 Apr;42(4):1077–1084. doi: 10.1111/j.1471-4159.1984.tb12713.x. [DOI] [PubMed] [Google Scholar]
  18. Gorelick F. S., Wang J. K., Lai Y., Nairn A. C., Greengard P. Autophosphorylation and activation of Ca2+/calmodulin-dependent protein kinase II in intact nerve terminals. J Biol Chem. 1988 Nov 25;263(33):17209–17212. [PubMed] [Google Scholar]
  19. Grab D. J., Berzins K., Cohen R. S., Siekevitz P. Presence of calmodulin in postsynaptic densities isolated from canine cerebral cortex. J Biol Chem. 1979 Sep 10;254(17):8690–8696. [PubMed] [Google Scholar]
  20. Grab D. J., Carlin R. K., Siekevitz P. Function of a calmodulin in postsynaptic densities. II. Presence of a calmodulin-activatable protein kinase activity. J Cell Biol. 1981 Jun;89(3):440–448. doi: 10.1083/jcb.89.3.440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Grab D. J., Carlin R. K., Siekevitz P. Function of calmodulin in postsynaptic densities. I. Presence of a calmodulin-activatable cyclic nucleotide phosphodiesterase activity. J Cell Biol. 1981 Jun;89(3):433–439. doi: 10.1083/jcb.89.3.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Graff J. M., Young T. N., Johnson J. D., Blackshear P. J. Phosphorylation-regulated calmodulin binding to a prominent cellular substrate for protein kinase C. J Biol Chem. 1989 Dec 25;264(36):21818–21823. [PubMed] [Google Scholar]
  23. Grover L. M., Teyler T. J. Two components of long-term potentiation induced by different patterns of afferent activation. Nature. 1990 Oct 4;347(6292):477–479. doi: 10.1038/347477a0. [DOI] [PubMed] [Google Scholar]
  24. Hashimoto Y., Schworer C. M., Colbran R. J., Soderling T. R. Autophosphorylation of Ca2+/calmodulin-dependent protein kinase II. Effects on total and Ca2+-independent activities and kinetic parameters. J Biol Chem. 1987 Jun 15;262(17):8051–8055. [PubMed] [Google Scholar]
  25. Hashimoto Y., Sharma R. K., Soderling T. R. Regulation of Ca2+/calmodulin-dependent cyclic nucleotide phosphodiesterase by the autophosphorylated form of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem. 1989 Jun 25;264(18):10884–10887. [PubMed] [Google Scholar]
  26. Holmes W. R. Is the function of dendritic spines to concentrate calcium? Brain Res. 1990 Jun 11;519(1-2):338–342. doi: 10.1016/0006-8993(90)90098-v. [DOI] [PubMed] [Google Scholar]
  27. Ingebritsen T. S., Cohen P. Protein phosphatases: properties and role in cellular regulation. Science. 1983 Jul 22;221(4608):331–338. doi: 10.1126/science.6306765. [DOI] [PubMed] [Google Scholar]
  28. Jones R. S., Heinemann U. H. Differential effects of calcium entry blockers on pre- and postsynaptic influx of calcium in the rat hippocampus in vitro. Brain Res. 1987 Jul 28;416(2):257–266. doi: 10.1016/0006-8993(87)90905-x. [DOI] [PubMed] [Google Scholar]
  29. Kelly P. T., McGuinness T. L., Greengard P. Evidence that the major postsynaptic density protein is a component of a Ca2+/calmodulin-dependent protein kinase. Proc Natl Acad Sci U S A. 1984 Feb;81(3):945–949. doi: 10.1073/pnas.81.3.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kelly P. T., Yip R. K., Shields S. M., Hay M. Calmodulin-dependent protein phosphorylation in synaptic junctions. J Neurochem. 1985 Nov;45(5):1620–1634. doi: 10.1111/j.1471-4159.1985.tb07235.x. [DOI] [PubMed] [Google Scholar]
  31. Kennedy M. B., Bennett M. K., Erondu N. E. Biochemical and immunochemical evidence that the "major postsynaptic density protein" is a subunit of a calmodulin-dependent protein kinase. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7357–7361. doi: 10.1073/pnas.80.23.7357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kennedy M. B. Regulation of synaptic transmission in the central nervous system: long-term potentiation. Cell. 1989 Dec 1;59(5):777–787. doi: 10.1016/0092-8674(89)90601-6. [DOI] [PubMed] [Google Scholar]
  33. Kilhoffer M. C., Roberts D. M., Adibi A. O., Watterson D. M., Haiech J. Investigation of the mechanism of calcium binding to calmodulin. Use of an isofunctional mutant with a tryptophan introduced by site-directed mutagenesis. J Biol Chem. 1988 Nov 15;263(32):17023–17029. [PubMed] [Google Scholar]
  34. Kwiatkowski A. P., King M. M. Autophosphorylation of the type II calmodulin-dependent protein kinase is essential for formation of a proteolytic fragment with catalytic activity. Implications for long-term synaptic potentiation. Biochemistry. 1989 Jun 27;28(13):5380–5385. doi: 10.1021/bi00439a010. [DOI] [PubMed] [Google Scholar]
  35. LaPorte D. C., Wierman B. M., Storm D. R. Calcium-induced exposure of a hydrophobic surface on calmodulin. Biochemistry. 1980 Aug 5;19(16):3814–3819. doi: 10.1021/bi00557a025. [DOI] [PubMed] [Google Scholar]
  36. Lai Y., Nairn A. C., Greengard P. Autophosphorylation reversibly regulates the Ca2+/calmodulin-dependence of Ca2+/calmodulin-dependent protein kinase II. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4253–4257. doi: 10.1073/pnas.83.12.4253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Le Vine H., 3rd, Sahyoun N. E., Cuatrecasas P. Binding of calmodulin to the neuronal cytoskeletal protein kinase type II cooperatively stimulates autophosphorylation. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2253–2257. doi: 10.1073/pnas.83.7.2253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. LeVine H., 3rd, Sahyoun N. E., Cuatrecasas P. Calmodulin binding to the cytoskeletal neuronal calmodulin-dependent protein kinase is regulated by autophosphorylation. Proc Natl Acad Sci U S A. 1985 Jan;82(2):287–291. doi: 10.1073/pnas.82.2.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lester B. R., Miller A. L., Peck E. J., Jr Differential solubilization of gamma-aminobutyric acid receptive sites from membranes of mammalian brain. J Neurochem. 1981 Jan;36(1):154–164. doi: 10.1111/j.1471-4159.1981.tb02390.x. [DOI] [PubMed] [Google Scholar]
  40. Lickteig R., Shenolikar S., Denner L., Kelly P. T. Regulation of Ca2+/calmodulin-dependent protein kinase II by Ca2+/calmodulin-independent autophosphorylation. J Biol Chem. 1988 Dec 15;263(35):19232–19239. [PubMed] [Google Scholar]
  41. Lisman J. E., Goldring M. A. Feasibility of long-term storage of graded information by the Ca2+/calmodulin-dependent protein kinase molecules of the postsynaptic density. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5320–5324. doi: 10.1073/pnas.85.14.5320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lisman J. A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9574–9578. doi: 10.1073/pnas.86.23.9574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lisman J., Goldring M. Evaluation of a model of long-term memory based on the properties of the Ca2+/calmodulin-dependent protein kinase. J Physiol (Paris) 1988;83(3):187–197. [PubMed] [Google Scholar]
  44. Malenka R. C., Kauer J. A., Perkel D. J., Mauk M. D., Kelly P. T., Nicoll R. A., Waxham M. N. An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature. 1989 Aug 17;340(6234):554–557. doi: 10.1038/340554a0. [DOI] [PubMed] [Google Scholar]
  45. Malinow R., Madison D. V., Tsien R. W. Persistent protein kinase activity underlying long-term potentiation. Nature. 1988 Oct 27;335(6193):820–824. doi: 10.1038/335820a0. [DOI] [PubMed] [Google Scholar]
  46. Matus A., Pehling G., Wilkinson D. gamma-Aminobutyric acid receptors in brain postsynaptic densities. J Neurobiol. 1981 Jan;12(1):67–73. doi: 10.1002/neu.480120106. [DOI] [PubMed] [Google Scholar]
  47. McIntyre D. C., Racine R. J. Kindling mechanisms: current progress on an experimental epilepsy model. Prog Neurobiol. 1986;27(1):1–12. doi: 10.1016/0301-0082(86)90010-9. [DOI] [PubMed] [Google Scholar]
  48. Miller R. J., Murphy S. N., Glaum S. R. Neuronal Ca2+ channels and their regulation by excitatory amino acids. Ann N Y Acad Sci. 1989;568:149–158. doi: 10.1111/j.1749-6632.1989.tb12502.x. [DOI] [PubMed] [Google Scholar]
  49. Miller S. G., Kennedy M. B. Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch. Cell. 1986 Mar 28;44(6):861–870. doi: 10.1016/0092-8674(86)90008-5. [DOI] [PubMed] [Google Scholar]
  50. Nunoki K., Florio V., Catterall W. A. Activation of purified calcium channels by stoichiometric protein phosphorylation. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6816–6820. doi: 10.1073/pnas.86.17.6816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Olwin B. B., Storm D. R. Calcium binding to complexes of calmodulin and calmodulin binding proteins. Biochemistry. 1985 Dec 31;24(27):8081–8086. doi: 10.1021/bi00348a037. [DOI] [PubMed] [Google Scholar]
  52. Popov N. S., Reymann K. G., Schulzeck K., Schulzeck S., Matthies H. Alterations in calmodulin content in fractions of rat hippocampal slices during tetanic- and calcium-induced long-term potentiation. Brain Res Bull. 1988 Aug;21(2):201–206. doi: 10.1016/0361-9230(88)90232-8. [DOI] [PubMed] [Google Scholar]
  53. Regehr W. G., Connor J. A., Tank D. W. Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation. Nature. 1989 Oct 12;341(6242):533–536. doi: 10.1038/341533a0. [DOI] [PubMed] [Google Scholar]
  54. Rich D. P., Colbran R. J., Schworer C. M., Soderling T. R. Regulatory properties of calcium/calmodulin-dependent protein kinase II in rat brain postsynaptic densities. J Neurochem. 1989 Sep;53(3):807–816. doi: 10.1111/j.1471-4159.1989.tb11777.x. [DOI] [PubMed] [Google Scholar]
  55. Saitoh T., Schwartz J. H. Phosphorylation-dependent subcellular translocation of a Ca2+/calmodulin-dependent protein kinase produces an autonomous enzyme in Aplysia neurons. J Cell Biol. 1985 Mar;100(3):835–842. doi: 10.1083/jcb.100.3.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Schulman H., Greengard P. Ca2+-dependent protein phosphorylation system in membranes from various tissues, and its activation by "calcium-dependent regulator". Proc Natl Acad Sci U S A. 1978 Nov;75(11):5432–5436. doi: 10.1073/pnas.75.11.5432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Schulman H., Greengard P. Stimulation of brain membrane protein phosphorylation by calcium and an endogenous heat-stable protein. Nature. 1978 Feb 2;271(5644):478–479. doi: 10.1038/271478a0. [DOI] [PubMed] [Google Scholar]
  58. Schulman H., Lou L. L. Multifunctional Ca2+/calmodulin-dependent protein kinase: domain structure and regulation. Trends Biochem Sci. 1989 Feb;14(2):62–66. doi: 10.1016/0968-0004(89)90045-5. [DOI] [PubMed] [Google Scholar]
  59. Schworer C. M., Colbran R. J., Soderling T. R. Reversible generation of a Ca2+-independent form of Ca2+(calmodulin)-dependent protein kinase II by an autophosphorylation mechanism. J Biol Chem. 1986 Jul 5;261(19):8581–8584. [PubMed] [Google Scholar]
  60. Shields S. M., Ingebritsen T. S., Kelly P. T. Identification of protein phosphatase 1 in synaptic junctions: dephosphorylation of endogenous calmodulin-dependent kinase II and synapse-enriched phosphoproteins. J Neurosci. 1985 Dec;5(12):3414–3422. doi: 10.1523/JNEUROSCI.05-12-03414.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Shields S. M., Vernon P. J., Kelly P. T. Autophosphorylation of calmodulin-kinase II in synaptic junctions modulates endogenous kinase activity. J Neurochem. 1984 Dec;43(6):1599–1609. doi: 10.1111/j.1471-4159.1984.tb06084.x. [DOI] [PubMed] [Google Scholar]
  62. Siekevitz P. The postsynaptic density: a possible role in long-lasting effects in the central nervous system. Proc Natl Acad Sci U S A. 1985 May;82(10):3494–3498. doi: 10.1073/pnas.82.10.3494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Sobue K., Kanda K., Adachi J., Kakiuchi S. Calmodulin-binding proteins that interact with actin filaments in a Ca2+-dependent flip-flop manner: survey in brain and secretory tissues. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6868–6871. doi: 10.1073/pnas.80.22.6868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Sulakhe P. V., St Louis P. J. Passive and active calcium fluxes across plasma membranes. Prog Biophys Mol Biol. 1980;35(3):135–195. doi: 10.1016/0079-6107(80)90005-x. [DOI] [PubMed] [Google Scholar]
  65. Suzuki T., Tanaka R. Characterization of Ca2+/calmodulin-dependent protein kinase associated with rat cerebral synaptic junction: substrate specificity and effect of autophosphorylation. J Neurochem. 1986 Aug;47(2):642–651. doi: 10.1111/j.1471-4159.1986.tb04548.x. [DOI] [PubMed] [Google Scholar]
  66. Tanabe T., Takeshima H., Mikami A., Flockerzi V., Takahashi H., Kangawa K., Kojima M., Matsuo H., Hirose T., Numa S. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 1987 Jul 23;328(6128):313–318. doi: 10.1038/328313a0. [DOI] [PubMed] [Google Scholar]
  67. Ueda T., Greengard P., Berzins K., Cohen R. S., Blomberg F., Grab D. J., Siekevitz P. Subcellular distribution in cerebral cortex of two proteins phosphorylated by a cAMP-dependent protein kinase. J Cell Biol. 1979 Nov;83(2 Pt 1):308–319. doi: 10.1083/jcb.83.2.308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Willmund R., Mitschulat H., Schneider K. Long-term modulation of Ca2+-stimulated autophosphorylation and subcellular distribution of the Ca2+/calmodulin-dependent protein kinase in the brain of Drosophila. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9789–9793. doi: 10.1073/pnas.83.24.9789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Wong D. T., Horng J. S. Na+-independent binding of GABA to the triton X-100 treated synaptic membranes from cerebellum of rat brain. Life Sci. 1977 Feb 1;20(3):445–451. doi: 10.1016/0024-3205(77)90386-1. [DOI] [PubMed] [Google Scholar]
  70. Wood J. G., Wallace R. W., Whitaker J. N., Cheung W. Y. Immunocytochemical localization of calmodulin and a heat-labile calmodulin-binding protein (CaM-BP80) in basal ganglia of mouse brain. J Cell Biol. 1980 Jan;84(1):66–76. doi: 10.1083/jcb.84.1.66. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Wu K., Carlin R., Sachs L., Siekevitz P. Existence of a Ca2+-dependent K+ channel in synaptic membrane and postsynaptic density fractions isolated from canine cerebral cortex and cerebellum, as determined by apamin binding. Brain Res. 1985 Dec 23;360(1-2):183–194. doi: 10.1016/0006-8993(85)91234-x. [DOI] [PubMed] [Google Scholar]
  72. Wu K., Carlin R., Siekevitz P. Binding of L-[3H]glutamate to fresh or frozen synaptic membrane and postsynaptic density fractions isolated from cerebral cortex and cerebellum of fresh or frozen canine brain. J Neurochem. 1986 Mar;46(3):831–841. doi: 10.1111/j.1471-4159.1986.tb13047.x. [DOI] [PubMed] [Google Scholar]
  73. Wu K., Sachs L., Carlin R. K., Siekevitz P. Characteristics of a Ca2+/calmodulin-dependent binding of the Ca2+ channel antagonist, nitrendipine, to a postsynaptic density fraction isolated from canine cerebral cortex. Brain Res. 1986 Nov;387(2):167–184. doi: 10.1016/0169-328x(86)90008-2. [DOI] [PubMed] [Google Scholar]
  74. Wu K., Siekevitz P. Neurochemical characteristics of a postsynaptic density fraction isolated from adult canine hippocampus. Brain Res. 1988 Aug 2;457(1):98–112. doi: 10.1016/0006-8993(88)90061-3. [DOI] [PubMed] [Google Scholar]
  75. Wu K., Wasterlain C., Sachs L., Siekevitz P. Effect of septal kindling on glutamate binding and calcium/calmodulin-dependent phosphorylation in a postsynaptic density fraction isolated from rat cerebral cortex. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5298–5302. doi: 10.1073/pnas.87.14.5298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Yip R. K., Kelly P. T. In situ protein phosphorylation in hippocampal tissue slices. J Neurosci. 1989 Oct;9(10):3618–3630. doi: 10.1523/JNEUROSCI.09-10-03618.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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