Regulation of CaMKII in vivo: The importance of targeting and the intracellular microenvironment

Neurochemical Research

Volumn 34, Issue 10, 2009, Pages 1792-1804

  Skelding, Kathryn A ^a   Rostas, John A P ^a,b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

Calcium calmodulin; CaMKII; Cell signalling; Molecular targeting; Protein phosphorylation

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; PHOSPHATASE; THREONINE;

AUTOPHOSPHORYLATION; BINDING SITE; CELL INTERACTION; CELL TYPE; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME STRUCTURE; HUMAN; IN VIVO STUDY; MICROENVIRONMENT; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; SIGNAL TRANSDUCTION; STIMULUS;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; HUMANS; INTRACELLULAR FLUID; MEMBRANE PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; THREONINE;

EID: 69049101050     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-009-9985-9     Document Type: Review

References (113)

1. 2+/calmodulin-dependent protein kinase associate differently with the postsynaptic density fraction J Biol Chem 260 9039 9046
2. KP Giese NB Fedorov RK Filipkowski AJ Silva 1998 Autophosphorylation of Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning Science 279 870 873 10.1126/science.279.5352.870
3. S Miller M Yasuda SK Coats Y Jones ME Martine M Mayford 2002 Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation Neuron 36 507 519 10.1016/S0896-6273(02) 00978-9
4. TR Soderling VA Derkach 2000 Postsynaptic protein phosphorylation and LTP Trends Neurosci 23 75 80 10.1016/S0166-2236(99)01490-3
5. S Taha SL Hanover AJ Silva MP Stryker 2002 Autophosphorylation of alphaCaMKII is required for ocular dominance plasticity Neuron 36 483 491 10.1016/S0896-6273(02)00966-2
6. X Cao H Wang B Mei S An L Yin LP Wang JZ Tsien 2008 Inducible and selective erasure of memories in the mouse brain via chemical-genetic manipulation Neuron 60 353 366 10.1016/j.neuron.2008.08.027
7. 2+/ calmodulin-dependent kinase II autophosphorylation is required for memory consolidation-specific transcription NeuroReport 16 1411 1414 10.1097/01.wnr.0000175244.51084.bb
8. KT Jones 2007 Intracellular calcium in the fertilization and development of mammalian eggs Clin Exp Pharmacol Physiol 34 1084 1089 10.1111/j.1440-1681. 2007.04726.x
9. 2+/calmodulin-dependent protein kinase II/ERK/AP-1 signaling pathway in human bone marrow-derived mesenchymal stem cells Cell Signal 20 613 624 10.1016/j.cellsig.2007.11.012
10. S Munevar SS Gangopadhyay C Gallant B Colombo FW Sellke KG Morgan 2008 CaMKIIT287 and T305 regulate history-dependent increases in alpha agonist-induced vascular tone J Cell Mol Med 12 219 226 10.1111/j.1582-4934. 2007.00202.x
11. 2+/calmodulin-dependent protein kinase II Biochem J 364 593 611 10.1042/BJ20020228
12. 2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function Annu Rev Biochem 71 473 510 10.1146/annurev.biochem.71.110601.135410
13. Y Elgersma JD Sweatt KP Giese 2004 Mouse genetic approaches to investigating calcium/calmodulin-dependent protein kinase II function in plasticity and cognition J Neurosci 24 8410 8415 10.1523/JNEUROSCI.3622-04.2004
14. 2+/calmodulin- dependent protein kinase II and its messenger RNA in the rat hippocampus following normo- and hypothermic ischemia Neuroscience 68 1003 1016 10.1016/0306-4522(95)00213-3
15. T Mengesdorf S Althausen G Mies L Olah W Paschen 2002 Phosphorylation state, solubility, and activity of calcium/calmodulin-dependent protein kinase II alpha in transient focal ischemia in mouse brain Neurochem Res 27 471 484 10.1023/A:1019844518704
16. JW Gurd S Rawof JZ Huo C Dykstra N Bissoon L Teves MC Wallace JAP Rostas 2008 Ischemia and status epilepticus result in enhanced phosphorylation of calcium and calmodulin stimulated protein kinase II on threonine 253 Brain Res 1218 158 165 10.1016/j.brainres.2008.04.040
17. 2+/calmodulin-dependent protein kinase II levels in Alzheimer's disease NeuroReport 16 1809 1813 10.1097/01.wnr.0000185015.44563.5d
18. JZ Wang I Grundke-Iqbal K Iqbal 2007 Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration Eur J NeuroSci 25 59 68
19. J Xiao G Perry J Troncoso MJ Monteiro 1996 Alpha-calcium-calmodulin- dependent kinase II is associated with paired helical filaments of Alzheimer's disease J Neuropathol Exp Neurol 55 954 963 10.1097/00005072-199609000-00002
20. JO McNamara YZ Huang AS Leonard 2006 Molecular signaling mechanisms underlying epileptogenesis Sci STKE 2006 356 re12 10.1126/stke.3562006re12
21. KP Zeitz KP Giese AJ Silva AI Basbaum 2004 The contribution of autophosphorylated alpha-calcium-calmodulin kinase II to injury-induced persistent pain Neuroscience 128 889 898 10.1016/j.neuroscience.2004.07.029
22. 2+-calmodulin-dependent protein kinase II function mediates synaptic and motor deficits in experimental Parkinsonism J Neurosci 24 5283 5291 10.1523/JNEUROSCI.1224-04.2004
23. RJ Colbran MK Smith CM Schworer Y-L Fong TR Soderling 1989 Regulatory domain of calcium/calmodulin-dependent protein kinase II. Mechanism of inhibition and regulation by phosphorylation J Biol Chem 264 4800 4804
24. MK Smith RJ Colbran DA Brickey TR Soderling 1992 Functional determinants in the autoinhibitory domain of calcium-calmodulin dependent protein kinase II J Biol Chem 267 1761 1768
25. ME Payne Y-L Fong T Ono RJ Colbran BE Kemp TR Soderling AR Means 1988 Calcium/calmodulin-dependent protein kinase II. Characterization of distinct calmodulin binding and inhibitory domains J Biol Chem 263 7190 7195
26. AP Braun H Schulman 1995 The multifunctional calcium/calmodulin-dependent protein kinase: from form to function Annu Rev Physiol 57 417 445 10.1146/annurev.ph.57.030195.002221
27. T Tobimatsu H Fujisawa 1989 Tissue-specific expression of four types of rat calmodulin-dependent protein kinase II mRNAs J Biol Chem 264 17907 17912
28. SJ Kolb A Hudmon TR Ginsberg MN Waxham 1998 Identification of domains essential for the assembly of calcium/calmodulin-dependent protein kinase II holoenzymes J Biol Chem 273 31555 31564 10.1074/jbc.273.47.31555
29. MK Bennett NE Erondu MB Kennedy 1983 Purification and characterization of a calmodulin-dependent protein kinase that is highly concentrated in brain J Biol Chem 258 12735 12744
30. L Brocke LW Chiang PD Wagner H Schulman 1999 Functional implications of the subunit composition of neuronal CaM kinase II J Biol Chem 274 22713 22722 10.1074/jbc.274.32.22713
31. 2+/calmodulin-dependent protein kinase II revealed by electron microscopy J Cell Biol 115 1049 1060 10.1083/jcb.115.4.1049
32. M Srinivasan CF Edman H Schulman 1994 Alternative splicing introduces a nuclear localization signal that targets multifunctional CaM kinase to the nucleus J Cell Biol 126 839 852 10.1083/jcb.126.4.839
33. 2+/ calmodulin-dependent protein kinase II J Biol Chem 279 12484 12494 10.1074/jbc.M313597200
34. JR Woodgett MT Davison P Cohen 1983 The calmodulin-dependent glycogen synthase kinase from rabbit skeletal muscle. Purification, subunit structure, and substrate specificity Eur J Biochem 136 481 487 10.1111/j.1432-1033.1983. tb07766.x
35. EP Morris K Torok 2001 Oligomeric structure of alpha-calmodulin-dependent protein kinase II J Mol Biol 308 1 8 10.1006/jmbi.2001.4584
36. OS Rosenberg S Deindl RJ Sung AC Nairn J Kuriyan 2005 Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme Cell 123 849 860 10.1016/j.cell.2005.10.029
37. T Meyer PI Hanson L Stryer H Schulman 1992 Calmodulin trapping by calcium-calmodulin-dependent protein kinase Science 256 1199 1202 10.1126/science.256.5060.1199
38. D Newton C Klee J Woodgett P Cohen 1985 Selective effects of CAPP1-calmodulin on its target proteins Biochim Biophys Acta 845 533 539 10.1016/0167-4889(85)90222-8
39. JA Putkey GF Draetta GR Slaughter CB Klee P Cohen JT Stull AR Means 1986 Genetically engineered calmodulins differentially activate target enzymes J Biol Chem 261 9896 9903
40. RJ Colbran CM Schworer Y Hashimoto Y-L Fong DP Rich MK Smith TR Soderling 1989 Calcium/calmodulin-dependent protein kinase II Biochem J 258 313 325
41. 2+ oscillations Science 279 227 230 10.1126/science.279.5348.227
42. S Strack RJ Colbran 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 10.1074/jbc.273.33. 20689
43. 2+/calmodulin- dependent protein kinase II by protein phosphatases 1 and 2A J Neurochem 68 2119 2128
44. 2+/calmodulin-dependent protein kinase analyzed by site-directed mutagenesis J Biol Chem 267 17216 17224
45. 2+/calmodulin is inhibited by autophosphorylation of threonine within the calmodulin-binding domain J Biol Chem 265 11204 11212
46. WE Meador AR Means FA Quicho 1993 Modulation of calmodulin plasticity in molecular recognition of CaMKII by scaffold-dependent autophosphorylation Science 262 1718 1721 10.1126/science.8259515
47. RJ Colbran TR Soderling 1990 Calcium/calmodulin-independent autophosphorylation sites of calcium/calmodulin-dependent protein kinase II. Studies on the effect of phosphorylation of threonine 305/306 and serine 314 on calmodulin binding using synthetic peptides J Biol Chem 265 11213 11219
48. PV Migues IT Lehmann L Fluechter M Cammarota JW Gurd AT Sim PW Dickson JA Rostas 2006 Phosphorylation of CaMKII at Thr253 occurs in vivo and enhances binding to isolated postsynaptic densities J Neurochem 98 289 299 10.1111/j.1471-4159.2006.03876.x
49. 2+/calmodulin-dependent protein kinase and mutational analysis of its autoregulation Neuron 3 59 70 10.1016/0896-6273(89) 90115-3
50. I Lengyel S Fieuw-Makaroff AL Hall AT Sim JA Rostas PR Dunkley 2000 Modulation of the phosphorylation and activity of calcium/calmodulin-dependent by protein kinase II by zinc J Neurochem 75 594 605 10.1046/j.1471-4159.2000. 0750594.x
51. H Jaffe L Vinade A Dosemeci 2004 Identification of novel phosphorylation sites on postsynaptic density proteins Biochem Biophys Res Commun 321 210 218 10.1016/j.bbrc.2004.06.122
52. 2+/calmodulin-dependent protein kinase in cultures of postnatal rat hippocampal slices Proc Natl Acad Sci USA 88 4756 4760 10.1073/pnas.88.11.4756
53. MO Collins L Yu MP Coba H Hsui I Campuzano WP Blackstock JS Choudhary SG Grant 2005 Proteomic analysis of in vivo phosphorylated synaptic proteins J Biol Chem 280 5972 5982 10.1074/jbc.M411220200
54. Y Ouyang D Kantor KM Harris EM Schuman MB Kennedy 1997 Visualization of the distribution of autophosphorylated calcium/calmodulin-dependent protein kinase II after tetanic stimulation in the CA1 area of the hippocampus J Neurosci 17 5416 5427
55. HX Chen N Otmakhov S Strack RJ Colbran JE Lisman 2001 Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP? J Neurophysiol 85 1368 1376
56. I Lengyel K Voss M Cammarota K Bradshaw V Brent KP Murphy KP Giese JA Rostas TV Bliss 2004 Autonomous activity of CaMKII is only transiently increased following the induction of long-term potentiation in the rat hippocampus Eur J NeuroSci 20 3063 3072 10.1111/j.1460-9568.2004.03748.x
57. SJ Lee Y Escobedo-Lozoya EM Szatmari R Yasuda 2009 Activation of CaMKII in single dendritic spines during long-term potentiation Nature 458 299 304 10.1038/nature07842
58. EM Lepicard K Mizuno A Antunes-Martins LSJ von Hertzen KP Giese 2006 An endogenous inhibitor of calcium/calmodulin-dependent kinase II is up-regulated during consolidation of fear memory Eur J NeuroSci 23 3063 3070 10.1111/j.1460-9568.2006.04830.x
59. ML Errington KD Bradshaw M Peters TVP Bliss KP Giese 2002 LTP is abolished in area CA1 but survives in the dentate gyrus of alphaCaMKII-T286A mutant mice: an in vivo and in vitro study Abstr Fed Eur Soc Neurosci 3 262
60. SF Cooke J Wu F Plattner M Errington M Rowan M Peters A Hirano KD Bradshaw R Anwyl TVP Bliss KP Giese 2006 Autophosphorylation of alphaCaMKII is not a general requirement for NMDA receptor-dependent LTP in the adult mouse J Physiol 574 805 818 10.1113/jphysiol.2006.111559
61. 2+/calmodulin-dependent kinase II disrupts memory consolidation Proc Natl Acad Sci USA 104 16317 16322 10.1073/pnas.0703344104
62. R Sugai M Takeuchi S Okuno H Fujisawa 1996 Molecular cloning of a novel protein containing the association domain of calmodulin-dependent protein kinase II J Biochem 120 773 779
63. KU Bayer K Harbers H Schulman 1998 AlphaKAP is an anchoring protein for a novel CaM kinase II isoform in skeletal muscle EMBO J 17 5598 5605 10.1093/emboj/17.19.5598
64. H O'Leary E Lasada KU Bayer 2006 CaMKIIbeta association with the actin cytoskeleton is regulated by alternative splicing Mol Biol Cell 17 4656 4665 10.1091/mbc.E06-03-0252
65. SJ House RG Ginnan SE Armstrong HA Singer 2007 Calcium/calmodulin- dependent protein kinase II-delta isoform regulation of vascular smooth muscle cell proliferation Am J Physiol Cell Physiol 292 C2276 C2287 10.1152/ajpcell.00606.2006
66. P An JY Zhu Y Yang P Lv YH Tian MK Chen HS Luo 2007 KN-93, a specific inhibitor of CaMKII inhibits human hepatic stellate cell proliferation in vitro World J Gastroenterol 13 1445 1448
67. TA Morris RJ DeLorenzo RM Tombes 1998 CaMK-II inhibition reduces cyclin D1 levels and enhances the association of p27kip1 with Cdk2 to cause G1 arrest in NIH 3T3 cells Exp Cell Res 240 218 227 10.1006/excr.1997.3925
68. MD Planas-Silva AR Means 1992 Expression of a constitutive form of calcium/calmodulin dependent protein kinase II leads to arrest of the cell cycle in G2 EMBO J 11 507 517
69. H Schulman 2004 Activity-dependent regulation of calcium/calmodulin- dependent protein kinase II localization J Neurosci 24 8399 8403 10.1523/JNEUROSCI.3606-04.2004
70. RJ Colbran 2004 Targeting of calcium/calmodulin-dependent protein kinase II Biochem J 378 1 16 10.1042/BJ20031547
71. 2+/calmodulin kinase II translocates in a hippocampal slice model of ischemia J Neurochem 64 2147 2156
72. S Strack S Choi DM Lovinger RJ Colbran 1997 Translocation of autophosphorylated calcium/calmodulin-dependent protein kinase II to the postsynaptic density J Biol Chem 272 13467 13470 10.1074/jbc.272.21.13467
73. 2+/calmodulin-dependent protein kinase II into postsynaptic density after decapitation J Neurochem 63 1529 1537
74. 2+/calmodulin-stimulated protein kinase II in chicken brain during post hatch development J Neurochem 66 1625 1632
75. Y Elgersma NB Fedorov S Ikonen ES Choi M Elgersma OM Carvalho KP Giese AJ Silva 2002 Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning Neuron 36 493 505 10.1016/S0896-6273(02)01007-3
76. KU Bayer P De Koninck AS Leonard JW Hell H Schulman 2001 Interaction with the NMDA receptor locks CaMKII in an active formation Nature 411 801 805 10.1038/35081080
77. F Gardoni A Caputi M Cimino L Pastorino F Cattabeni M Di Luca 1998 Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities J Neurochem 71 1733 1741
78. F Gardoni LH Schrama JJW van Dalen WH Gispen F Cattabeni M Di Luca 1999 AlphaCaMKII binding to the C-terminal tail of NMDA receptor subunit NR2A and its modulation by autophosphorylation FEBS Lett 456 394 398 10.1016/S0014-5793(99) 00985-0
79. YC Lin L Redmond 2008 CaMKIIbeta binding to stable F-actin in vivo regulates F-actin filament stability Proc Natl Acad Sci USA 105 15791 15796 10.1073/pnas.0804399105
80. K Shen MN Teruel K Subramanian T Meyer 1998 CaMKIIbeta functions as an F-actin targeting module that localizes CaMKIIalpha/beta hetero oligomers to dendritic spines Neuron 21 593 606 10.1016/S0896-6273(00)80569-3
81. AB Jefferson H Schulman 1991 Phosphorylation of microtubule-associated protein-2 in GH3 cells. Regulation by cAMP and by calcium J Biol Chem 266 346 354
82. 2+, calmodulin-dependent regulation of microtubule formation via phosphorylation of microtubule-associated protein 2, tau factor, and tubulin, and comparison with the cyclic AMP-dependent phosphorylation J Neurochem 44 759 768 10.1111/j.1471-4159.1985.tb12880.x
83. KU Bayer E LeBel GL McDonald H O'Leary H Schulman P De Koninck 2006 Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B J Neurosci 26 1164 1174 10.1523/JNEUROSCI.3116-05.2006
84. 2+/CaM-responsive pool of CaMKII by scaffold-dependent autophosphorylation Neuron 40 1185 1197 10.1016/S0896-6273(03)00786-4
85. 2+/calmodulin-dependent protein kinase II translocated to the postsynaptic density Brain Res Mol Brain Res 81 118 128 10.1016/S0169-328X(00) 00170-4
86. 2+/calmodulin-dependent protein kinase II in the postsynaptic density by protein sequencing and mass spectrometry Biochem Biophys Res Commun 290 948 954 10.1006/bbrc.2001.6320
87. 2+/calmodulin-dependent protein kinase II blocks its nuclear targeting J Biol Chem 273 19763 19771 10.1074/jbc.273.31. 19763
88. V Urquidi SJ Ashcroft 1995 A novel pancreatic beta-cell isoform of calcium/calmodulin-dependent protein kinase II (beta 3 isoform) contains a proline-rich tandem repeat in the association domain FEBS Lett 358 23 26 10.1016/0014-5793(94)01381-A
89. AJ Robison MA Bass Y Jiao LB MacMillan LC Carmody RK Bartlett RJ Colbran 2005 Multivalent interactions of calcium/calmodulin-dependent protein kinase II with the postsynaptic density proteins NR2B, densin-180, and alpha-actinin-2 J Biol Chem 280 35329 35336 10.1074/jbc.M502191200
90. X Wang QB Tian A Okano H Sakagami IS Moon H Kondo S Endo T Suzuki 2005 BAALC 1-6-8 protein is targeted to postsynaptic lipid rafts by its N-terminal myristoylation and palmitoylation, and interacts with alpha, but not beta, subunit of Ca/calmodulin-dependent protein kinase II J Neurochem 92 647 659 10.1111/j.1471-4159.2004.02902.x
91. K Okamoto R Narayanan SH Lee K Murata Y Hayashi 2007 The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure Proc Natl Acad Sci USA 104 6418 6423 10.1073/pnas.0701656104
92. 2+/calmodulin kinase II by a small C-terminal domain phosphatase Biochem J 412 507 516 10.1042/BJ20071582
93. SM Shields TS Ingebritsen PT Kelly 1985 Identification of protein phosphatase 1 in synaptic junctions: dephosphorylation of endogenous calmodulin-dependent kinase II and synapse-enriched phosphoproteins J Neurosci 5 3414 3422
94. 2+/calmodulin-dependent protein kinase II by protein phosphatase 2C J Biol Chem 268 133 137
95. EJ Weeber YH Jiang Y Elgersma AW Varga Y Carrasquillo SE Brown JM Christian B Mirnikjoo A Silva AL Beaudet JD Sweatt 2003 Derangements of hippocampal calcium/calmodulin-dependent protein kinase II in a mouse model for Angelman mental retardation syndrome J Neurosci 23 2634 2644
96. A Dosemeci TS Reese 1993 Inhibition of endogenous phosphatase in a postsynaptic density fraction allows extensive phosphorylation of the major postsynaptic density protein J Neurochem 61 550 555
97. P Mullasseril A Dosemeci JE Lisman LC Griffith 2007 A structural mechanism for maintaining the 'on-state' of the CaMKII memory switch in the post-synaptic density J Neurochem 103 357 364
98. 2+/calmodulin-dependent protein kinase J Biol Chem 269 31330 31333
99. 2+/calmodulin-dependent protein kinase II in Escherichia coli J Biochem 138 605 611 10.1093/jb/mvi161
100. 2+/calmodulin-dependent protein kinase II and alpha-actinin-1 in a calcium-dependent manner J Neurosci 22 7879 7891
101. CE Grueter SA Abiria Y Wu ME Anderson RJ Colbran 2008 Differential regulated interactions of calcium/calmodulin-dependent protein kinase II with isoforms of voltage-gated calcium channel beta subunits Biochemistry 47 1760 1767 10.1021/bi701755q
102. JW Hell SM Appleyard CT Yokoyama C Warner WA Catterall 1994 Differential phosphorylation of two size forms of the N-type calcium channel alpha1 subunit which have different COOH termini J Biol Chem 269 7390 7396
103. 2+/calmodulin-dependent protein kinase II is a modulator of CARMA1-mediated NF-kappaB activation Mol Cell Biol 26 5497 5508 10.1128/MCB.02469-05
104. CM Atkins N Nozaki Y Shigeri TR Soderling 2004 Cytoplasmic polyadenylation element binding protein-dependent protein synthesis is regulated by calcium/calmodulin-dependent protein kinase II J Neurosci 24 5193 5201 10.1523/JNEUROSCI.0854-04.2004
105. 2+/calmodulin-dependent protein kinase II with neuronal cytoskeletal proteins J Biol Chem 270 10043 10049 10.1074/jbc.270.17.10043
106. T Yamashita S Inui K Maeda DR Hua K Takagi K Fukunaga N Sakaguchi 2006 Regulation of CaMKII by alpha4/PP2Ac contributes to learning and memory Brain Res 1082 1 10 10.1016/j.brainres.2006.01.101
107. M Fahrmaan M Erfmann G Beinbrech 2002 Binding of CaMKII to the giant muscle protein projectin: stimulation of CaMKII activity by projectin Biochim Biophys Acta 1569 127 134
108. JS Moyers PJ Bilans J Zhu CR Kahn 1997 Rad and Rad-related GTPases interact with calmodulin and calmodulin-dependent protein kinase II J Biol Chem 272 11832 11839 10.1074/jbc.272.18.11832
109. J Baratier L Peris J Brocard S Gory-Faure F Dufour C Bosc A Fourest-Lieuvin L Blanchoin P Salin D Job A Andrieux 2006 Phosphorylation of microtubule-associated protein STOP by calmodulin kinase II J Biol Chem 281 19561 19569 10.1074/jbc.M509602200
110. 2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I Nature 359 417 420 10.1038/359417a0
111. 2+/calmodulin-activated protein kinase II to syntaxin 1A J Neurosci 22 3342 3351
112. M Bennecib CX Gong I Grundke-Iqbal K Iqbal 2001 Inhibition of PP-2A upregulates CaMKII in rat forebrain and induces hyperphosphorylation of tau at Ser 262/356 FEBS Lett 490 15 22 10.1016/S0014-5793(01)02127-5
113. IT Lehmann L Bobrovskaya SL Gordon PR Dunkley PW Dickson 2006 Differential regulation of the human tyrosine hydroxylase isoforms via hierarchical phosphorylation J Biol Chem 281 17644 17651 10.1074/jbc.M512194200