Enzymatic activity of CaMKII is not required for its interaction with the glutamate receptor subunit GluN2B

Molecular Pharmacology

Volumn 84, Issue 6, 2013, Pages 834-843

  Barcomb, Kelsey ^a   Coultrap, Steven J ^a   Bayer, K Ulrich ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; ADENOSINE TRIPHOSPHATE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN BINDING PROTEIN; GLUTAMATE RECEPTOR 2; N METHYL DEXTRO ASPARTIC ACID; NUCLEOTIDE BINDING PROTEIN; PHOSPHOTRANSFERASE INHIBITOR; STAUROSPORINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELL STRAIN HEK293; COMPETITIVE INHIBITION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME INHIBITOR INTERACTION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE COMPLEX; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELLS, CULTURED; FEMALE; GLUTAMIC ACID; HEK293 CELLS; HUMANS; MALE; NEURONS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; STAUROSPORINE; SYNAPSES;

EID: 84888881335     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.089045     Document Type: Article

References (60)

1. Barria A and Malinow R (2005) NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48:289-301.
2. Bayer KU, De Koninck P, Leonard AS, Hell JW, and Schulman H (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411: 801-805.
3. Bayer KU, LeBel E, McDonald GL, O'Leary H, Schulman H, and De Koninck P (2006) Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. J Neurosci 26:1164-1174.
4. Buard I, Coultrap SJ, Freund RK, Lee Y-S, Dell'Acqua ML, Silva AJ, and Bayer KU (2010) CaMKII "autonomy" is required for initiating but not for maintaining neuronal long-term information storage. J Neurosci 30:8214-8220.
5. Chen HX, Otmakhov N, Strack S, Colbran RJ, and Lisman JE (2001) Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP? J Neurophysiol 85:1368-1376.
6. Colbran RJ and Brown AM (2004) Calcium/calmodulin-dependent protein kinase II and synaptic plasticity. Curr Opin Neurobiol 14:318-327.
7. Colley PA, Sheu FS, and Routtenberg A (1990) Inhibition of protein kinase C blocks two components of LTP persistence, leaving initial potentiation intact. J Neurosci 10:3353-3360.
8. Copeland RA (2000) Enzymes: A Practical Introduction to Structure, Mechanism, and Data Analysis, 2nd ed., pp 305-317, Wiley-Interscience, NY
9. Coultrap SJ and Bayer KU (2011) Improving a natural CaMKII inhibitor by random and rational design. PLoS ONE 6:e25245.
10. Coultrap SJ and Bayer KU (2012a) CaMKII regulation in information processing and storage. Trends Neurosci 35:607-618.
11. 2+/Calmodulin-Dependent Protein Kinase II (CaMKII), in Protein Kinase Technologies (Neuromethods) (Mukai H ed) pp 49-57, Humana Press, Totowa, NJ.
12. Denny JB, Polan-Curtain J, Rodriguez S, Wayner MJ, and Armstrong DL (1990) Evidence that protein kinase M does not maintain long-term potentiation. Brain Res 534:201-208.
13. 2+/calmodulin- kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci USA 96:3269-3274.
14. Engh RA, Girod A, Kinzel V, Huber R, and Bossemeyer D (1996) Crystal structures of catalytic subunit of cAMP-dependent protein kinase in complex with isoquinolinesulfonyl protein kinase inhibitors H7, H8, and H89. Structural implications for selectivity. J Biol Chem 271:26157-26164.
15. 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.
16. Giese KP, Fedorov NB, Filipkowski RK, and Silva AJ (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279:870-873.
17. Gouet C, Aburto B, Vergara C, and SanhuezaM (2012) On the mechanism of synaptic depression induced by CaMKIIN, an endogenous inhibitor of CaMKII. PLoS ONE 7:e49293.
18. Halt AR, Dallapiazza RF, Zhou Y, Stein IS, Qian H, Juntti S, Wojcik S, Brose N, Silva AJ, and Hell JW (2012) CaMKII binding to GluN2B is critical during memory consolidation. EMBO J 31:1203-1216.
19. Hanks SK, Quinn AM, and Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
20. Hanse E and Gustafsson B (1994) Staurosporine impairs both short-term and long-term potentiation in the dentate gyrus in vitro. Neuroscience 58:263-274.
21. Hanson PI, Meyer T, Stryer L, and Schulman H (1994) Dual role of calmodulin in autophosphorylation of multifunctional CaM kinase may underlie decoding of calcium signals. Neuron 12:943-956.
22. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, and Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
23. Hidaka H, Inagaki M, Kawamoto S, and Sasaki Y (1984) Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 23:5036-5041.
24. 2+/calmodulin-dependent protein kinase II clustering at synaptic and nonsynaptic sites based on self-association. J Neurosci 25: 6971-6983.
25. Hyman SE, Malenka RC, and Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565-598.
26. Jalan-Sakrikar N, Bartlett RK, Baucum AJ, 2nd, and Colbran RJ (2012) Substrateselective and calcium-independent activation of CaMKII by α-actinin. J Biol Chem 287:15275-15283.
27. 2+/calmodulin- dependent kinase II regulation of AMPA receptor gating. Nat Neurosci 14:727-735.
28. Ling DSF, Benardo LS, Serrano PA, Blace N, Kelly MT, Crary JF, and Sacktor TC (2002) Protein kinase Mzeta is necessary and sufficient for LTP maintenance. Nat Neurosci 5:295-296.
29. 2+/calmodulin-dependent protein kinase by autophosphorylation: ATP modulates production of an autonomous enzyme. Proc Natl Acad Sci USA 83:9497-9501.
30. Loweth JA, Li D, Cortright JJ, Wilke G, Jeyifous O, Neve RL, Bayer KU, and Vezina P (2013) Persistent reversal of enhanced amphetamine intake by transient CaMKII inhibition. J Neurosci 33:1411-1416.
31. Malinow R, Schulman H, and Tsien RW (1989) Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245:862-866.
32. 2+/calmodulin protein kinase IIalpha (CaMKIIalpha) to inhibitory synapses. Proc Natl Acad Sci USA 107:20559-20564.
33. Matthies H, Jr, Behnisch T, Kase H, Matthies H, and Reymann KG (1991) Differential effects of protein kinase inhibitors on pre-established long-term potentiation in rat hippocampal neurons in vitro. Neurosci Lett 121:259-262.
34. Meggio F, Donella Deana A, Ruzzene M, Brunati AM, Cesaro L, Guerra B, Meyer T, Mett H, Fabbro D, and Furet P et al. (1995) Different susceptibility of protein kinases to staurosporine inhibition. Kinetic studies and molecular bases for the resistance of protein kinase CK2. Eur J Biochem 234:317-322.
35. Merrill MA, Chen Y, Strack S, and Hell JW (2005) Activity-driven postsynaptic translocation of CaMKII. Trends Pharmacol Sci 26:645-653.
36. 2+-triggered molecular switch. Cell 44:861-870.
37. Morrison JF (1969) Kinetics of the reversible inhibition of enzyme-catalysed reactions by tight-binding inhibitors. Biochim Biophys Acta 185:269-286.
38. Nakano H, Kobayashi E, Takahashi I, Tamaoki T, Kuzuu Y, and Iba H (1987) Staurosporine inhibits tyrosine-specific protein kinase activity of Rous sarcoma virus transforming protein p60. J Antibiot (Tokyo) 40:706-708.
39. Nathan PJ, Cobb SR, Lu B, Bullmore ET, and Davies CH (2011) Studying synaptic plasticity in the human brain and opportunities for drug discovery. Curr Opin Pharmacol 11:540-548.
40. 2+/ calmodulin-dependent protein kinase II (CaMKII) binding to the N-methyl-D-aspartate (NMDA) receptor subunit GluN2B. J Biol Chem 286:31272-31281.
41. Omura S, Sasaki Y, Iwai Y, and Takeshima H (1995) Staurosporine, a potentially important gift from a microorganism. J Antibiot (Tokyo) 48:535-548.
42. Opazo P, Labrecque S, Tigaret CM, Frouin A, Wiseman PW, De Koninck P, and Choquet D (2010) CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 67:239-252.
43. Otmakhov N, Griffith LC, and Lisman JE (1997) Postsynaptic inhibitors of calcium/calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation. J Neurosci 17:5357-5365.
44. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, and Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141-1144.
45. Prade L, Engh RA, Girod A, Kinzel V, Huber R, and Bossemeyer D (1997) Staurosporine-induced conformational changes of cAMP-dependent protein kinase catalytic subunit explain inhibitory potential. Structure 5:1627-1637.
46. 2+/calmodulin-dependent protein kinase II. J Biol Chem 273: 28424-28429.
47. Sanhueza M, Fernandez-Villalobos G, Stein IS, Kasumova G, Zhang P, Bayer KU, Otmakhov N, Hell JW, and Lisman J (2011) Role of the CaMKII/NMDA receptor complex in the maintenance of synaptic strength. J Neurosci 31:9170-9178.
48. Sanhueza M and Lisman J (2013) The CaMKII/NMDAR complex as a molecular memory. Mol Brain 6:10.
49. 2+/calmodulindependent protein kinase II. Identification of a regulatory autophosphorylation site adjacent to the inhibitory and calmodulin-binding domains. J Biol Chem 263: 13486-13489.
50. She K, Rose JK, Craig AM (2012) Differential stimulus-dependent synaptic recruitment of CaMKIIa by intracellular determinants of GluN2B. Mol Cell Neurosci 51:68-78.
51. Shen K and Meyer T (1999) Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284:162-166.
52. Soderling TR and Derkach VA (2000) Postsynaptic protein phosphorylation and LTP. Trends Neurosci 23:75-80.
53. Strack S and Colbran RJ (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.
54. Strack S, McNeill RB, and Colbran RJ (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.
55. 2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem Biophys Res Commun 181:968-975.
56. ++-dependent protein kinase. Biochem Biophys Res Commun 135:397-402.
57. 2+-independent activity. Proc Natl Acad Sci USA 85:6337-6341.
58. Vest RS, Davies KD, O'Leary H, Port JD, and Bayer KU (2007) Dual mechanism of a natural CaMKII inhibitor. Mol Biol Cell 18:5024-5033.
59. 2+)/ calmodulin-dependent protein kinase II (CaMKII) inhibitor. J Biol Chem 285:20675-20682.
60. 2+/calmodulin- dependent protein kinase II. J Neurochem 56:294-298.