Cdk-mediated phosphorylation of the Kvβ2 auxiliary subunit regulates Kv1 channel axonal targeting

Journal of Cell Biology

Volumn 192, Issue 5, 2011, Pages 813-824

  Vacher, Hélène ^a,c,d   Yang, Jae Won ^a,e   Cerda, Oscar ^a   Autillo Touati, Amapola ^c,d   Dargent, Bénédicte ^c,d   Trimmer, James S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSERM   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; SERINE; SHAKER POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MICROTUBULE; MOUSE; NERVE FIBER; NEUROACANTHOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; AXONS; CHROMATOGRAPHY, LIQUID; CYCLIN-DEPENDENT KINASES; HIPPOCAMPUS; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOLECULAR SEQUENCE DATA; NEURONS; PHOSPHORYLATION; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RATS; SCIATIC NERVE; SERINE; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; TANDEM MASS SPECTROMETRY;

EID: 79952368304     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201007113     Document Type: Article

References (66)

1. Adelman, J.P., C.T. Bond, M. Pessia, and J. Maylie. 1995. Episodic ataxia results from voltage-dependent potassium channels with altered functions. Neuron. 15:1449-1454. doi:10.1016/0896-6273(95)90022-5 (Pubitemid 26005381)
2. Bach, S., M. Knockaert, J. Reinhardt, O. Lozach, S. Schmitt, B. Baratte, M. Koken, S.P. Coburn, L. Tang, T. Jiang, et al. 2005. Roscovitine targets, protein kinases and pyridoxal kinase. J. Biol. Chem. 280:31208-31219. doi:10.1074/jbc.M500806200
3. Baek, J.H., O. Cerda, and J.S. Trimmer. 2011. Mass spectrometry-based phosphoproteomics reveals multisite phosphorylation on mammalian brain voltage-gated sodium and potassium channels. Semin. Cell Dev. Biol. In press.
4. Bean, B.P. 2007. The action potential in mammalian central neurons. Nat. Rev. Neurosci. 8:451-465. doi:10.1038/nrn2148
5. Bekele-Arcuri, Z., M.F. Matos, L. Manganas, B.W. Strassle, M.M. Monaghan, K.J. Rhodes, and J.S. Trimmer. 1996. Generation and characterization of subtype-specific monoclonal antibodies to K+ channel alpha- and beta-subunit polypeptides. Neuropharmacology. 35:851-865. doi:10.1016/0028-3908(96)00128-1 (Pubitemid 26377672)
6. Bieling, P., L. Laan, H. Schek, E.L. Munteanu, L. Sandblad, M. Dogterom, D. Brunner, and T. Surrey. 2007. Reconstitution of a microtubule plus-end tracking system in vitro. Nature. 450:1100-1105. doi:10.1038/nature06386 (Pubitemid 350273611)
7. Bréchet, A., M.P. Fache, A. Brachet, G. Ferracci, A. Baude, M. Irondelle, S. Pereira, C. Leterrier, and B. Dargent. 2008. Protein kinase CK2 contributes to the organization of sodium channels in axonal membranes by regulating their interactions with ankyrin G. J. Cell Biol. 183:1101-1114. doi:10.1083/jcb.200805169
8. Campomanes, C.R., K.I. Carroll, L.N. Manganas, M.E. Hershberger, B. Gong, D.E. Antonucci, K.J. Rhodes, and J.S. Trimmer. 2002. Kv beta subunit oxidoreductase activity and Kv1 potassium channel trafficking. J. Biol. Chem. 277:8298-8305. doi:10.1074/jbc.M110276200
9. Chung, Y.H., C.M. Shin, M.J. Kim, and C.I. Cha. 2000. Immunohistochemical study on the distribution of six members of the Kv1 channel subunits in the rat basal ganglia. Brain Res. 875:164-170. doi:10.1016/S0006-8993(00)02586-5
10. Clark, B.D., E.M. Goldberg, and B. Rudy. 2009. Electrogenic tuning of the axon initial segment. Neuroscientist. 15:651-668. doi:10.1177/1073858409341973
11. Cohen, N.A., J.E. Brenman, S.H. Snyder, and D.S. Bredt. 1996. Binding of the inward rectifier K+ channel Kir 2.3 to PSD-95 is regulated by protein kinase A phosphorylation. Neuron. 17:759-767. doi:10.1016/S0896-6273(00)80207-X (Pubitemid 26365354)
12. Dixit, R., B. Barnett, J.E. Lazarus, M. Tokito, Y.E. Goldman, and E.L. Holzbaur. 2009. Microtubule plus-end tracking by CLIP-170 requires EB1. Proc. Natl. Acad. Sci. USA. 106:492-497. doi:10.1073/pnas.0807614106
13. Goldberg, E.M., B.D. Clark, E. Zagha, M. Nahmani, A. Erisir, and B. Rudy. 2008. K+ channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron. 58:387-400. doi:10.1016/j.neuron.2008.03.003 (Pubitemid 351615188)
14. Goslin, K., and G. Banker. 1989. Experimental observations on the development of polarity by hippocampal neurons in culture. J. Cell Biol. 108:1507-1516. doi:10.1083/jcb.108.4.1507 (Pubitemid 19097054)
15. Gu, C., Y.N. Jan, and L.Y. Jan. 2003. A conserved domain in axonal targeting of Kv1 (Shaker) voltage-gated potassium channels. Science. 301:646-649. doi:10.1126/science.1086998
16. Gu, C., W. Zhou, M.A. Puthenveedu, M. Xu, Y.N. Jan, and L.Y. Jan. 2006. The microtubule plus-end tracking protein EB1 is required for Kv1 voltage-gated K+ channel axonal targeting. Neuron. 52:803-816. doi:10.1016/j.neuron.2006.10. 022
17. Guillaud, L., R. Wong, and N. Hirokawa. 2008. Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: a molecular model of kinesin-cargo release. Nat. Cell Biol. 10:19-29. doi:10.1038/ncb1665
18. Gulbis, J.M., S. Mann, and R. MacKinnon. 1999. Structure of a voltage-dependent K+ channel beta subunit. Cell. 97:943-952. doi:10.1016/S0092-8674(00)80805-3 (Pubitemid 29375052)
19. Gulbis, J.M., M. Zhou, S. Mann, and R. MacKinnon. 2000. Structure of the cytoplasmic beta subunit-T1 assembly of voltage-dependent K+ channels. Science. 289:123-127. doi:10.1126/science.289.5476.123 (Pubitemid 30463306)
20. Honnappa, S., C.M. John, D. Kostrewa, F.K. Winkler, and M.O. Steinmetz. 2005. Structural insights into the EB1-APC interaction. EMBO J. 24:261-269. doi:10.1038/sj.emboj.7600529 (Pubitemid 40216131)
21. Honnappa, S., S.M. Gouveia, A. Weisbrich, F.F. Damberger, N.S. Bhavesh, H. Jawhari, I. Grigoriev, F.J. van Rijssel, R.M. Buey, A. Lawera, et al. 2009. An EB1-binding motif acts as a microtubule tip localization signal. Cell. 138:366-376. doi:10.1016/j.cell.2009.04.065
22. Inda, M.C., J. DeFelipe, and A. Muñoz. 2006. Voltage-gated ion channels in the axon initial segment of human cortical pyramidal cells and their relationship with chandelier cells. Proc. Natl. Acad. Sci. USA. 103:2920-2925. doi:10.1073/pnas.0511197103
23. Jen, J.C., T.D. Graves, E.J. Hess, M.G. Hanna, R.C. Griggs, and R.W. Baloh; CINCH investigators. 2007. Primary episodic ataxias: diagnosis, pathogenesis and treatment. Brain. 130:2484-2493. doi:10.1093/brain/awm126
24. Johnston, J., I.D. Forsythe, and C. Kopp-Scheinpflug. 2010. Going native: voltage-gated potassium channels controlling neuronal excitability. J. Physiol. 588:3187-3200. doi:10.1113/jphysiol.2010.191973
25. Judge, S.I., J.M. Lee, C.T. Bever Jr., and P.M. Hoffman. 2006. Voltage-gated potassium channels in multiple sclerosis: Overview and new implications for treatment of central nervous system inflammation and degeneration. J. Rehabil. Res. Dev. 43:111-122. doi:10.1682/JRRD.2004.09.0116
26. Kullmann, D.M., and M.G. Hanna. 2002. Neurological disorders caused by inherited ion-channel mutations. Lancet Neurol. 1:157-166. doi:10.1016/S1474- 4422(02)00071-6 (Pubitemid 37163484)
27. Kumar, P., K.S. Lyle, S. Gierke, A. Matov, G. Danuser, and T. Wittmann. 2009. GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J. Cell Biol. 184:895-908. doi:10.1083/jcb. 200901042
28. Long, S.B., E.B. Campbell, and R. Mackinnon. 2005. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 309:897-903. doi:10.1126/science.1116269 (Pubitemid 41099919)
29. Lorincz, A., and Z. Nusser. 2008. Cell-type-dependent molecular composition of the axon initial segment. J. Neurosci. 28:14329-14340. doi:10.1523/JNEUROSCI.4833-08.2008
30. Matsuda, S., S. Mikawa, and H. Hirai. 1999. Phosphorylation of serine-880 in GluR2 by protein kinase C prevents its C terminus from binding with glutamate receptor-interacting protein. J. Neurochem. 73:1765-1768. doi:10.1046/j.1471-4159.1999.731765.x (Pubitemid 29440182)
31. Meijer, L., A. Borgne, O. Mulner, J.P. Chong, J.J. Blow, N. Inagaki, M. Inagaki, J.G. Delcros, and J.P. Moulinoux. 1997. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur. J. Biochem. 243:527-536. doi:10.1111/j.1432- 1033.1997.t01-2-00527.x
32. Mi, H., T.J. Deerinck, M.H. Ellisman, and T.L. Schwarz. 1995. Differential distribution of closely related potassium channels in rat Schwann cells. J. Neurosci. 15:3761-3774.
33. Morfini, G., G. Szebenyi, R. Elluru, N. Ratner, and S.T. Brady. 2002. Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J. 21:281-293. doi:10.1093/emboj/21.3.281 (Pubitemid 34137290)
34. Murakoshi, H., G. Shi, R.H. Scannevin, and J.S. Trimmer. 1997. Phosphorylation of the Kv2.1 K+ channel alters voltage-dependent activation. Mol. Pharmacol. 52:821-828.
35. Nagaya, N., and D.M. Papazian. 1997. Potassium channel alpha and beta subunits assemble in the endoplasmic reticulum. J. Biol. Chem. 272:3022-3027. doi:10.1074/jbc.272.5.3022
36. Nakahira, K., G. Shi, K.J. Rhodes, and J.S. Trimmer. 1996. Selective interaction of voltage-gated K+ channel beta-subunits with alpha-subunits. J. Biol. Chem. 271:7084-7089. doi:10.1074/jbc.271.12.7084
37. Nakahira, K., M.F. Matos, and J.S. Trimmer. 1998. Differential interaction of voltage-gated K+ channel beta-subunits with cytoskeleton is mediated by unique amino terminal domains. J. Mol. Neurosci. 11:199-208. doi:10.1385/JMN:11:3:199
38. Ogawa, Y., I. Horresh, J.S. Trimmer, D.S. Bredt, E. Peles, and M.N. Rasband. 2008. Postsynaptic density-93 clusters Kv1 channels at axon initial segments independently of Caspr2. J. Neurosci. 28:5731-5739. doi:10.1523/JNEUROSCI.4431-07.2008
39. Orlova, E.V., M. Papakosta, F.P. Booy, M. van Heel, and J.O. Dolly. 2003. Voltage-gated K+ channel from mammalian brain: 3D structure at 18A of the complete (alpha)4(beta)4 complex. J. Mol. Biol. 326:1005-1012. doi:10.1016/S0022-2836(02)00708-8
40. Osten, P., L. Khatri, J.L. Perez, G. Köhr, G. Giese, C. Daly, T.W. Schulz, A. Wensky, L.M. Lee, and E.B. Ziff. 2000. Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron. 27:313-325. doi:10.1016/S0896-6273(00)00039-8
41. Park, K.S., D.P. Mohapatra, H. Misonou, and J.S. Trimmer. 2006. Graded regulation of the Kv2.1 potassium channel by variable phosphorylation. Science. 313:976-979. doi:10.1126/science.1124254 (Pubitemid 44267390)
42. Pongs, O., T. Leicher, M. Berger, J. Roeper, R. Bähring, D. Wray, K.P. Giese, A.J. Silva, and J.F. Storm. 1999. Functional and molecular aspects of voltage-gated K+ channel beta subunits. Ann. N. Y. Acad. Sci. 868:344-355. doi:10.1111/j.1749-6632.1999.tb11296.x
43. Rasband, M.N. 2004. It's "juxta" potassium channel! J. Neurosci. Res. 76:749-757. doi:10.1002/jnr.20073
44. Rasband, M.N., J.S. Trimmer, T.L. Schwarz, S.R. Levinson, M.H. Ellisman, M. Schachner, and P. Shrager. 1998. Potassium channel distribution, clustering, and function in remyelinating rat axons. J. Neurosci. 18:36-47. (Pubitemid 28046765)
45. Rettig, J., S.H. Heinemann, F. Wunder, C. Lorra, D.N. Parcej, J.O. Dolly, and O. Pongs. 1994. Inactivation properties of voltage-gated K+ channels altered by presence of beta-subunit. Nature. 369:289-294. doi:10.1038/369289a0
46. Rhodes, K.J., S.A. Keilbaugh, N.X. Barrezueta, K.L. Lopez, and J.S. Trimmer. 1995. Association and colocalization of K+ channel alpha- and beta-subunit polypeptides in rat brain. J. Neurosci. 15:5360-5371.
47. Rhodes, K.J., M.M. Monaghan, N.X. Barrezueta, S. Nawoschik, Z. Bekele- Arcuri, M.F. Matos, K. Nakahira, L.E. Schechter, and J.S. Trimmer. 1996. Voltage-gated K+ channel beta subunits: expression and distribution of Kv beta 1 and Kv beta 2 in adult rat brain. J. Neurosci. 16:4846-4860. (Pubitemid 26269647)
48. Rhodes, K.J., B.W. Strassle, M.M. Monaghan, Z. Bekele-Arcuri, M.F. Matos, and J.S. Trimmer. 1997. Association and colocalization of the Kvbeta1 and Kvbeta2 beta-subunits with Kv1 alpha-subunits in mammalian brain K+ channel complexes. J. Neurosci. 17:8246-8258. (Pubitemid 27461049)
49. Rivera, J., P.J. Chu, T.L. Lewis Jr., and D.B. Arnold. 2007. The role of Kif5B in axonal localization of Kv1 K(+) channels. Eur. J. Neurosci. 25:136-146. doi:10.1111/j.1460-9568.2006.05277.x
50. Ruppersberg, J.P., K.H. Schröter, B. Sakmann, M. Stocker, S. Sewing, and O. Pongs. 1990. Heteromultimeric channels formed by rat brain potassium-channel proteins. Nature. 345:535-537. doi:10.1038/345535a0
51. Sato-Yoshitake, R., H. Yorifuji, M. Inagaki, and N. Hirokawa. 1992. The phosphorylation of kinesin regulates its binding to synaptic vesicles. J. Biol. Chem. 267:23930-23936.
52. Sewing, S., J. Roeper, and O. Pongs. 1996. Kv beta 1 subunit binding specific for shaker-related potassium channel alpha subunits. Neuron. 16:455-463. doi:10.1016/S0896-6273(00)80063-X
53. Shi, G., K. Nakahira, S. Hammond, K.J. Rhodes, L.E. Schechter, and J.S. Trimmer. 1996. Beta subunits promote K+ channel surface expression through effects early in biosynthesis. Neuron. 16:843-852. doi:10.1016/S0896-6273(00) 80104-X (Pubitemid 26124061)
54. Skube, S.B., J.M. Chaverri, and H.V. Goodson. 2010. Effect of GFP tags on the localization of EB1 and EB1 fragments in vivo. Cytoskeleton (Hoboken). 67:1-12.
55. Sokolova, O., A. Accardi, D. Gutierrez, A. Lau, M. Rigney, and N. Grigorieff. 2003. Conformational changes in the C terminus of Shaker K+ channel bound to the rat Kvbeta2-subunit. Proc. Natl. Acad. Sci. USA. 100:12607-12612. doi:10.1073/pnas.2235650100
56. Tiffany, A.M., L.N. Manganas, E. Kim, Y.P. Hsueh, M. Sheng, and J.S. Trimmer. 2000. PSD-95 and SAP97 exhibit distinct mechanisms for regulating K(+) channel surface expression and clustering. J. Cell Biol. 148:147-158. doi:10.1083/jcb.148.1.147
57. Trimmer, J.S. 1991. Immunological identification and characterization of a delayed rectifier K+ channel polypeptide in rat brain. Proc. Natl. Acad. Sci. USA. 88:10764-10768. doi:10.1073/pnas.88.23.10764
58. Trimmer, J.S. 1998. Regulation of ion channel expression by cytoplasmic subunits. Curr. Opin. Neurobiol. 8:370-374. doi:10.1016/S0959-4388(98)80063-9
59. Vabnick, I., J.S. Trimmer, T.L. Schwarz, S.R. Levinson, D. Risal, and P. Shrager. 1999. Dynamic potassium channel distributions during axonal development prevent aberrant firing patterns. J. Neurosci. 19:747-758. (Pubitemid 29036026)
60. Vacher, H., D.P. Mohapatra, H. Misonou, and J.S. Trimmer. 2007. Regulation of Kv1 channel trafficking by the mamba snake neurotoxin dendrotoxin K. FASEB J. 21:906-914. doi:10.1096/fj.06-7229com (Pubitemid 46348263)
61. van den Heuvel, S., and E. Harlow. 1993. Distinct roles for cyclin-dependent kinases in cell cycle control. Science. 262:2050-2054. doi:10.1126/science.8266103 (Pubitemid 24041887)
62. Van Wart, A., J.S. Trimmer, and G. Matthews. 2007. Polarized distribution of ion channels within microdomains of the axon initial segment. J. Comp. Neurol. 500:339-352. doi:10.1002/cne.21173
63. Vitre, B., F.M. Coquelle, C. Heichette, C. Garnier, D. Chrétien, and I. Arnal. 2008. EB1 regulates microtubule dynamics and tubulin sheet closure in vitro. Nat. Cell Biol. 10:415-421. doi:10.1038/ncb1703
64. Wang, H., D.D. Kunkel, T.M. Martin, P.A. Schwartzkroin, and B.L. Tempel. 1993. Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons. Nature. 365:75-79. doi:10.1038/365075a0 (Pubitemid 23305573)
65. Watanabe, T., J. Noritake, M. Kakeno, T. Matsui, T. Harada, S. Wang, N. Itoh, K. Sato, K. Matsuzawa, A. Iwamatsu, et al. 2009. Phosphorylation of CLASP2 by GSK-3beta regulates its interaction with IQGAP1, EB1 and microtubules. J. Cell Sci. 122:2969-2979. doi:10.1242/jcs.046649
66. Xu, J., W. Yu, J.M. Wright, R.W. Raab, and M. Li. 1998. Distinct functional stoichiometry of potassium channel beta subunits. Proc. Natl. Acad. Sci. USA. 95:1846-1851. doi:10.1073/pnas.95.4.1846