Calcium-Calmodulin-Dependent Kinase II Modulates Kv4.2 Channel Expression and Upregulates Neuronal A-Type Potassium Currents

Journal of Neuroscience

Volumn 24, Issue 14, 2004, Pages 3643-3654

  Varga, Andrew W ^a   Yuan, Li Lian ^a   Anderson, Anne E ^a   Schrader, Laura A ^a   Wu, Gang Yi ^a   Gatchel, Jennifer R ^a   Johnston, Daniel ^a   Sweatt, J David ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Division of Neuroscience   (United States)

Author keywords

Hippocampus; Kinase; Memory; Phosphorylation; Potassium channel; Synaptic plasticity

Indexed keywords

POTASSIUM CHANNEL; PROTEIN KINASE (CALCIUM,CALMODULIN) II;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CELL STRAIN COS7; CELL SURFACE; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; HIPPOCAMPUS; IN VITRO STUDY; MEMBRANE DEPOLARIZATION; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; OOCYTE; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; REPOLARIZATION; UPREGULATION; WILD TYPE; XENOPUS;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CRICETINAE; GENE EXPRESSION REGULATION; GENE TRANSFER TECHNIQUES; HIPPOCAMPUS; KV CHANNEL-INTERACTING PROTEINS; MUTAGENESIS, SITE-DIRECTED; NEURONS; OOCYTES; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; POTASSIUM; POTASSIUM CHANNELS; POTASSIUM CHANNELS, VOLTAGE-GATED; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; SHAL POTASSIUM CHANNELS; UP-REGULATION; XENOPUS;

EID: 1842681997     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0154-04.2004     Document Type: Article

References (56)

1. Adams JP, Anderson AE, Varga AW, Dineley KT, Cook RG, Pfaffinger PJ, Sweatt JD (2000) The A-type potassium channel Kv4.2 is a substrate for the mitogen-activated protein kinase ERK. J Neurochem 75:2277-2287.
2. An WF, Bowlby MR, Betty M, Cao J, Ling HP, Mendoza G, Hinson JW, Mattsson KI, Strassle BW, Trimmer JS, Rhodes KJ (2000) Modulation of A-type potassium channels by a family of calcium sensors. Nature 403:553-556.
3. Anderson AE, Adams JP, Qian Y, Cook RG, Pfaffinger PJ, Sweatt JD (2000) Kv4.2 phosphorylation by cyclic AMP-dependent protein kinase. J Biol Chem 275:5337-5346.
4. Barria A, Muller D, Derkach V, Griffith LC, Soderling TR (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276:2042-2045.
5. 2+/calmodulin-dependent kinase II alpha-subunit mutation. Proc Natl Acad Sci USA 92:6852-6855.
6. Choe S, Kreusch A, Pfaffinger PJ (1999) Towards the three-dimensional structure of voltage-gated potassium channels. Trends Biochem Sci 24:345-349.
7. Churn SB, Sombati S, Jakoi ER, Sievert L, DeLorenzo RJ (2000) Inhibition of calcium/calmodulin kinase II alpha subunit expression results in epileptiform activity in cultured hippocampal neurons. Proc Natl Acad Sci USA 97:5604-5609.
8. 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.
9. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525.
10. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6:231-242.
11. Frangioni JV, Neel BG (1993) Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal Biochem 210:179-187.
12. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279:870-873.
13. Golowasch J, Abbott LF, Marder E (1999) Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis. J Neurosci 19:RC33(1-5).
14. Grosse G, Draguhn A, Hohne L, Tapp R, Veh RW, Ahnert-Hilger G (2000) Expression of Kv1 potassium channels in mouse hippocampal primary cultures: development and activity-dependent regulation. J Neurosci 20:1869-1882.
15. Hakes DJ, Dixon JE (1992) New vectors for high level expression of recombinant proteins in bacteria. Anal Biochem 202:293-298.
16. 2+/calmodulin-dependent protein kinase and mutational analysis of its autoregulation. Neuron 3:59-70.
17. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
18. Hinds HL, Tonegawa S, Malinow R (1998) CA1 long-term potentiation is diminished but present in hippocampal slices from alpha-CaMKII mutant mice. Learn Mem 5:344-354.
19. + channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci 18:3521-3528.
20. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869-875.
21. Holmqvist MH, Cao J, Hernandez-Pineda R, Jacobson MD, Carroll KI, Sung MA, Betty M, Ge P, Gilbride KJ, Brown ME, Jurman ME, Lawson D, Silos-Santiago I, Xie Y, Covarrubias M, Rhodes KJ, Distefano PS, An WF (2002) Elimination of fast inactivation in Kv4 A-type potassium channels by an auxiliary subunit domain. Proc Natl Acad Sci USA 99:1035-1040.
22. + current in murine proximal colon by calcium-calmodulin-dependent protein kinase II. J Physiol (Lond) 517:75-84.
23. Lledo PM, Hjelmstad GO, Mukherji S, Soderling TR, Malenka RC, Nicoll RA (1995) Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci USA 92:11175-11179.
24. Malenka RC, Kauer JA, Perkel DJ, Mauk MD, Kelly PT, Nicoll RA, Waxham MN (1989) An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature 340:554-557.
25. + channel polypeptides in rat hippocampal neurons developing in situ and in vitro. J Neurosci 15:3840-3851.
26. Malinow R, Schulman H, Tsien RW (1989) Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245:862-866.
27. Marder E, Prinz AA (2002) Modeling stability in neuron and network function: the role of activity in homeostasis. BioEssays 24:1145-1154.
28. + channels. Neuron 37:449-461.
29. + channel beta-subunits with alpha-subunits. J Biol Chem 271:7084-7089.
30. + current, by PKC. Am J Physiol 273:H1775-H1786.
31. Perez-Garcia MT, Lopez-Lopez JR, Gonzalez C (1999) Kvbeta1.2 subunit coexpression in HEK293 cells confers O2 sensitivity to kv4.2 but not to Shaker channels. J Gen Physiol 113:897-907.
32. Pettit DL, Perlman S, Malinow R (1994) Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons. Science 266:1881-1885.
33. 2+/calmodulin-dependent protein kinase II. J Neurosci 22:4406-4411.
34. Ramakers GM, Storm JF (2002) A postsynaptic transient K(+) current modulated by arachidonic acid regulates synaptic integration and threshold for LTP induction in hippocampal pyramidal cells. Proc Natl Acad Sci USA 99:10144-10149.
35. 2+/calmodulin-dependent protein kinase. J Neurosci 17:3379-3391.
36. Sanguinetti MC, Johnson JH, Hammerland LG, Kelbaugh PR, Volkmann RA, Saccomano NA, Mueller AL (1997) Heteropodatoxins: peptides isolated from spider venom that block Kv4.2 potassium channels. Mol Pharmacol 51:491-498.
37. Schrader LA, Anderson AE, Mayne A, Pfaffinger PJ, Sweatt JD (2002) PKA modulation of Kv4.2-encoded A-type potassium channels requires formation of a supramolecular complex. J Neurosci 22:10123-10133.
38. + (A-type) currents in rat brain. J Neurophysiol 79:1081-1091.
39. + channel proteins in rat central neurons. Neuron 9:271-284.
40. + current mediated by the Kv4 channel regulates the generation of action potential in developing cerebellar granule cells. J Neurosci 20:4145-4155.
41. Shibata R, Misonou H, Campomanes CR, Anderson AE, Schrader LA, Doliveira LC, Carroll KI, Sweatt JD, Rhodes KJ, Trimmer JS (2003) A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J Biol Chem 278:36445-36454.
42. Silva AJ, Stevens CF, Tonegawa S, Wang Y (1992a) Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257:201-206.
43. Silva AJ, Paylor R, Welmer JM, Tonegawa S (1992b) Impaired spatial learning in α-calcium-calmodulin kinase II mutant mice. Science 257:206-211.
44. Song WJ, Tkatch T, Baranauskas G, Ichinohe N, Kitai ST, Surmeier DJ (1998) Somatodendritic depolarization-activated potassium currents in rat neostriatal cholinergic interneurons are predominantly of the A type and attributable to coexpression of Kv4.2 and Kv4.1 subunits. J Neurosci 18:3124-3137.
45. 2+/calmodulin-dependent protein kinases II in human atrial myocytes. Circ Res 85:810-819.
46. + current amplitude are linearly related in basal ganglia and basal forebrain neurons. J Neurosci 20:579-588.
47. Varga AW, Anderson AE, Adams JP, Vogel H, Sweatt JD (2000) Input-specific immunolocalization of differentially phosphorylated Kv4.2 in the mouse brain. Learn Mem 7:321-332.
48. Veh RW, Lichtinghagen R, Sewing S, Wunder F, Grumbach IM, Pongs O (1995) Immunohistochemical localization of five members of the Kv1 channel subunits: contrasting subcellular locations and neuron-specific co-localizations in rat brain. Eur J Neurosci 7:2189-2205.
49. 2+/CaM induces synaptic potentiation requiring CaMKII and PKC activity. Neuron 15:443-452.
50. + channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 99:8366-8371.
51. Wu GY, Deisseroth K, Tsien RW (2001) Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat Neurosci 4:151-158.
52. Wu RL, Butler DM, Barish ME (1998) Potassium current development and its linkage to membrane expansion during growth of cultured embryonic mouse hippocampal neurons: sensitivity to inhibitors of phosphatidyl-inositol 3-kinase and other protein kinases. J Neurosci 18:6261-6278.
53. Xia Z, Dudek H, Miranti CK, Greenberg ME (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 16:5425-5436.
54. + channels in mid-brain dopaminergic neurons. Nat Neurosci 4:1071-1078.
55. + currents in Drosophila neurons. J Neurophysiol 85:1384-1394.
56. + channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22:4860-4868.