The Microtubule Plus-End Tracking Protein EB1 Is Required for Kv1 Voltage-Gated K+ Channel Axonal Targeting

Neuron

Volumn 52, Issue 5, 2006, Pages 803-816

  Gu, Chen ^a,b   Zhou, Wei ^a   Puthenveedu, Manojkumar A ^a   Xu, Mingxuan ^b   Jan, Yuh Nung ^a   Jan, Lily Yeh ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

CELLBIO; MOLNEURO

Indexed keywords

BREFELDIN A; POTASSIUM CHANNEL; PROTEIN; PROTEIN EB1; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL KV1; VOLTAGE GATED POTASSIUM CHANNEL KV2 BETA;

ALPHA CHAIN; ANIMAL CELL; ARTICLE; BETA CHAIN; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MICROTUBULE; NERVE FIBER; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; AXONS; BLOTTING, WESTERN; CELL MOVEMENT; CELLS, CULTURED; DNA, COMPLEMENTARY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIPPOCAMPUS; HUMANS; IMMUNOPRECIPITATION; KINESIN; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MUTAGENESIS; NEURONS; RATS; RNA, SMALL INTERFERING; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS;

EID: 36248997297     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.10.022     Document Type: Article

References (53)

1. Akhmanova A., and Hoogenraad C.C. Microtubule plus-end-tracking proteins: mechanisms and functions. Curr. Opin. Cell Biol. 17 (2005) 47-54
2. Baccus S.A., Burrell B.D., Sahley C.L., and Muller K.J. Action potential reflection and failure at axon branch points cause stepwise changes in EPSPs in a neuron essential for learning. J. Neurophysiol. 83 (2000) 1693-1700
3. Berezuk M.A., and Schroer T.A. Fractionation and characterization of kinesin II species in vertebrate brain. Traffic 5 (2004) 503-513
4. Browne D.L., Gancher S.T., Nutt J.G., Brunt E.R., Smith E.A., Kramer P., and Litt M. Episodic ataxia/myokymia syndrome is associated with point mutations in the human potassium channel gene, KCNA1. Nat. Genet. 8 (1994) 136-140
5. Browning H., and Hackney D.D. The EB1 homolog Mal3 stimulates the ATPase of the kinesin Tea2 by recruiting it to the microtubule. J. Biol. Chem. 280 (2005) 12299-12304
6. Browning H., Hackney D.D., and Nurse P. Targeted movement of cell end factors in fission yeast. Nat. Cell Biol. 5 (2003) 812-818
7. Busch K.E., and Brunner D. The microtubule plus end-tracking proteins mal3p and tip1p cooperate for cell-end targeting of interphase microtubules. Curr. Biol. 14 (2004) 548-559
8. Busch K.E., Hayles J., Nurse P., and Brunner D. Tea2p kinesin is involved in spatial microtubule organization by transporting tip1p on microtubules. Dev. Cell 6 (2004) 831-843
9. Campomanes C.R., Carroll K.I., Manganas L.N., Hershberger M.E., Gong B., Antonucci D.E., Rhodes K.J., and Trimmer J.S. Kv beta subunit oxidoreductase activity and Kv1 potassium channel trafficking. J. Biol. Chem. 277 (2002) 8298-8305
10. Chiu S.Y., Zhou L., Zhang C.L., and Messing A. Analysis of potassium channel functions in mammalian axons by gene knockouts. J. Neurocytol. 28 (1999) 349-364
11. Cirelli C., Bushey D., Hill S., Huber R., Kreber R., Ganetzky B., and Tononi G. Reduced sleep in Drosophila Shaker mutants. Nature 434 (2005) 1087-1092
12. Debanne D. Information processing in the axon. Nat. Rev. Neurosci. 5 (2004) 304-316
13. Elliott S.L., Cullen C.F., Wrobel N., Kernan M.J., and Ohkura H. EB1 is essential during Drosophila development and plays a crucial role in the integrity of chordotonal mechanosensory organs. Mol. Biol. Cell 16 (2005) 891-901
14. Galjart N. CLIPs and CLASPs and cellular dynamics. Nat. Rev. Mol. Cell Biol. 6 (2005) 487-498
15. Grosse G., Draguhn A., Hohne L., Tapp R., Veh R.W., and Ahnert-Hilger G. Expression of Kv1 potassium channels in mouse hippocampal primary cultures: development and activity-dependent regulation. J. Neurosci. 20 (2000) 1869-1882
16. Gu C., Sorkin A., and Cooper D.M. Persistent interactions between the two transmembrane clusters dictate the targeting and functional assembly of adenylyl cyclase. Curr. Biol. 11 (2001) 185-190
17. Gu C., Jan Y.N., and Jan L.Y. A conserved domain in axonal targeting of Kv1 (Shaker) voltage-gated potassium channels. Science 301 (2003) 646-649
18. + channel beta subunit. Cell 97 (1999) 943-952
19. Hayashi I., and Ikura M. Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1). J. Biol. Chem. 278 (2003) 36430-36434
20. Hayashi I., Wilde A., Mal T.K., and Ikura M. Structural basis for the activation of microtubule assembly by the EB1 and p150Glued complex. Mol. Cell 19 (2005) 449-460
21. Heidemann S.R., Landers J.M., and Hamborg M.A. Polarity orientation of axonal microtubules. J. Cell Biol. 91 (1981) 661-665
22. Heinemann S.H., and Hoshi T. Multifunctional potassium channels: electrical switches and redox enzymes, all in one. Sci. STKE 2006 (2006) pe33
23. Herson P.S., Virk M., Rustay N.R., Bond C.T., Crabbe J.C., Adelman J.P., and Maylie J. A mouse model of episodic ataxia type-1. Nat. Neurosci. 6 (2003) 378-383
24. Hirokawa N., and Takemura R. Molecular motors and mechanisms of directional transport in neurons. Nat. Rev. Neurosci. 6 (2005) 201-214
25. Hodgkin A.L., and Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117 (1952) 500-544
26. Honnappa S., John C.M., Kostrewa D., Winkler F.K., and Steinmetz M.O. Structural insights into the EB1-APC interaction. EMBO J. 24 (2005) 261-269
27. Jan Y.N., Jan L.Y., and Dennis M.J. Two mutations of synaptic transmission in Drosophila. Proc. R. Soc. Lond. B. Biol. Sci. 198 (1977) 87-108
28. Komarova Y., Lansbergen G., Galjart N., Grosveld F., Borisy G.G., and Akhmanova A. EB1 and EB3 control CLIP dissociation from the ends of growing microtubules. Mol. Biol. Cell 16 (2005) 5334-5345
29. Lang B., and Vincent A. Autoantibodies to ion channels at the neuromuscular junction. Autoimmun. Rev. 2 (2003) 94-100
30. Ma Y., Shakiryanova D., Vardya I., and Popov S.V. Quantitative analysis of microtubule transport in growing nerve processes. Curr. Biol. 14 (2004) 725-730
31. Mimori-Kiyosue Y., Shiina N., and Tsukita S. The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr. Biol. 10 (2000) 865-868
32. Misonou H., and Trimmer J.S. Determinants of voltage-gated potassium channel surface expression and localization in Mammalian neurons. Crit. Rev. Biochem. Mol. Biol. 39 (2004) 125-145
33. + channel alpha and beta subunits in rat hippocampal formation. J. Neurosci. 21 (2001) 5973-5983
34. Morrison E.E., Wardleworth B.N., Askham J.M., Markham A.F., and Meredith D.M. EB1, a protein which interacts with the APC tumour suppressor, is associated with the microtubule cytoskeleton throughout the cell cycle. Oncogene 17 (1998) 3471-3477
35. Nakata T., and Hirokawa N. Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J. Cell Biol. 162 (2003) 1045-1055
36. + channels altered by presence of beta-subunit. Nature 369 (1994) 289-294
37. Rhodes K.J., Strassle B.W., Monaghan M.M., Bekele-Arcuri Z., Matos M.F., and Trimmer J.S. Association and colocalization of the Kv beta 1 and Kv beta 2 beta-subunits with Kv1 alpha-subunits in mammalian brain K+ channel complexes. J. Neurosci. 17 (1997) 8246-8258
38. Rouzier R., Rajan R., Wagner P., Hess K.R., Gold D.L., Stec J., Ayers M., Ross J.S., Zhang P., Buchholz T.A., et al. Microtubule-associated protein tau: a marker of paclitaxel sensitivity in breast cancer. Proc. Natl. Acad. Sci. USA 102 (2005) 8315-8320
39. + channel surface expression through effects early in biosynthesis. Neuron 16 (1996) 843-852
40. Slep K.C., Rogers S.L., Elliott S.L., Ohkura H., Kolodziej P.A., and Vale R.D. Structural determinants for EB1-mediated recruitment of APC and spectraplakins to the microtubule plus end. J. Cell Biol. 168 (2005) 587-598
41. Smart S.L., Lopantsev V., Zhang C.L., Robbins C.A., Wang H., Chiu S.Y., Schwartzkroin P.A., Messing A., and Tempel B.L. Deletion of the K(v)1.1 potassium channel causes epilepsy in mice. Neuron 20 (1998) 809-819
42. Sorkin A., McClure M., Huang F., and Carter R. Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr. Biol. 10 (2000) 1395-1398
43. Southan A.P., and Robertson B. Electrophysiological characterization of voltage-gated K(+) currents in cerebellar basket and purkinje cells: Kv1 and Kv3 channel subfamilies are present in basket cell nerve terminals. J. Neurosci. 20 (2000) 114-122
44. Stepanova T., Slemmer J., Hoogenraad C.C., Lansbergen G., Dortland B., De Zeeuw C.I., Grosveld F., van Cappellen G., Akhmanova A., and Galjart N. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23 (2003) 2655-2664
45. Su L.K., Burrell M., Hill D.E., Gyuris J., Brent R., Wiltshire R., Trent J., Vogelstein B., and Kinzler K.W. APC binds to the novel protein EB1. Cancer Res. 55 (1995) 2972-2977
46. Takeda S., Yamazaki H., Seog D.H., Kanai Y., Terada S., and Hirokawa N. Kinesin superfamily protein 3 (KIF3) motor transports fodrin-associating vesicles important for neurite building. J. Cell Biol. 148 (2000) 1255-1265
47. Tirnauer J.S., and Bierer B.E. EB1 proteins regulate microtubule dynamics, cell polarity, and chromosome stability. J. Cell Biol. 149 (2000) 761-766
48. Tirnauer J.S., Grego S., Salmon E.D., and Mitchison T.J. EB1-microtubule interactions in Xenopus egg extracts: role of EB1 in microtubule stabilization and mechanisms of targeting to microtubules. Mol. Biol. Cell 13 (2002) 3614-3626
49. Vasquez R.J., Howell B., Yvon A.M., Wadsworth P., and Cassimeris L. Nanomolar concentrations of nocodazole alter microtubule dynamic instability in vivo and in vitro. Mol. Biol. Cell 8 (1997) 973-985
50. Vaughan K.T. Microtubule plus ends, motors, and traffic of Golgi membranes. Biochim. Biophys. Acta 1744 (2005) 316-324
51. Yamazaki H., Nakata T., Okada Y., and Hirokawa N. KIF3A/B: a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport. J. Cell Biol. 130 (1995) 1387-1399
52. Zhou L., Zhang C.L., Messing A., and Chiu S.Y. Temperature-sensitive neuromuscular transmission in Kv1.1 null mice: role of potassium channels under the myelin sheath in young nerves. J. Neurosci. 18 (1998) 7200-7215
53. Zhou F.Q., Zhou J., Dedhar S., Wu Y.H., and Snider W.D. NGF-induced axon growth is mediated by localized inactivation of GSK-3β and functions of the microtubule plus end binding protein APC. Neuron 42 (2004) 897-912