The fibroblast growth factor 14·voltage-gated sodium channel complex is a new target of glycogen synthase kinase 3 (GSK3)

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 19370-19385

  Shavkunov, Alexander S ^a   Wildburger, Norelle C ^a,b,c   Nenov, Miroslav N ^a   James, Thomas F ^a,b   Buzhdygan, Tetyana P ^b   Panova Elektronova, Neli I ^a   Green, Thomas A ^a,d   Veselenak, Ronald L ^e   Bourne, Nigel ^e,f   Laezza, Fernanda ^a,d,g  

^a University of Texas Medical Branch School of Medicine   (United States)

^b Neuroscience Graduate Program   (United States)

^c The Sealy Center for Structural Biology   (United States)

^d Center for Addiction Research   (United States)

^e Department of Pediatric Vaccinology ^*  (United States)

^f Galveston National Laboratory Assay Development Service Division   (United States)

^g Center for Biomedical Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICAL PROPERTIES; CO-IMMUNOPRECIPITATIONS; CONFOCAL IMMUNOFLUORESCENCE; FIBROBLAST GROWTH FACTOR; GLYCOGEN SYNTHASE KINASE-3; MACROMOLECULAR COMPLEXES; SMALL-MOLECULE LIBRARY; SUBCELLULAR DISTRIBUTION;

NEURONS; SODIUM;

ELECTROPHYSIOLOGY;

FIBROBLAST GROWTH FACTOR 14; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; SODIUM CHANNEL NAV1.6; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; CELL VIABILITY; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; DISSOCIATION; ELECTROPHYSIOLOGY; ENZYME INHIBITION; FEMALE; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MOUSE; NERVE CELL; NERVE EXCITABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; RAT; SODIUM CURRENT;

EXCITABILITY; FGF14; GSK3; ION CHANNELS; NEURONS; PHOSPHORYLATION; PROTEIN/PROTEIN INTERACTIONS; SODIUM CHANNELS;

ANIMALS; ENZYME INHIBITORS; FIBROBLAST GROWTH FACTORS; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MICE; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; NAV1.6 VOLTAGE-GATED SODIUM CHANNEL; NEURONS; RATS; SIGNAL TRANSDUCTION;

EID: 84880055131     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.445924     Document Type: Article

References (45)

1. Dover, K., Solinas, S., D'Angelo, E., and Goldfarb, M. (2010) Long-term inactivation particle for voltage-gated sodium channels. J. Physiol. 588, 3695-3711
2. Wang, C., Chung, B. C., Yan, H., Lee, S. Y., and Pitt, G. S. (2012) Crystal structure of the ternary complex of a NaV C-terminal domain, a fibroblast growth factor homologous factor, and calmodulin. Structure 20, 1167-1176
3. Wei, E. Q., Barnett, A. S., Pitt, G. S., and Hennessey, J. A. (2011) Fibroblast growth factor homologous factors in the heart: a potential locus for cardiac arrhythmias. Trends Cardiovasc. Med. 21, 199-203
4. Lou, J. Y., Laezza, F., Gerber, B. R., Xiao, M., Yamada, K. A., Hartmann, H., Craig, A. M., Nerbonne, J. M., and Ornitz, D. M. (2005) Fibroblast growth factor 14 is an intracellular modulator of voltage-gated sodium channels. J. Physiol. 569, 179-193
5. Laezza, F., Gerber, B. R., Lou, J. Y., Kozel, M. A., Hartman, H., Craig, A. M., Ornitz, D. M., and Nerbonne, J. M. (2007) The FGF14(F145S) mutation disrupts the interaction of FGF14 with voltage-gated Na+ channels and impairs neuronal excitability. J. Neurosci. 27, 12033-12044
6. Laezza, F., Lampert, A., Kozel, M. A., Gerber, B. R., Rush, A. M., Nerbonne, J. M., Waxman, S. G., Dib-Hajj, S. D., and Ornitz, D. M. (2009) FGF14 N-terminal splice variants differentially modulate Nav1.2- and Nav1.6- encoded sodium channels. Mol. Cell. Neurosci. 42, 90-101
7. Goetz, R., Dover, K., Laezza, F., Shtraizent, N., Huang, X., Tchetchik, D., Eliseenkova, A. V., Xu, C. F., Neubert, T. A., Ornitz, D. M., Goldfarb, M., and Mohammadi, M. (2009) Crystal structure of a fibroblast growth factor homologous factor (FHF) defines a conserved surface on FHFs for binding and modulation of voltage-gated sodium channels. J. Biol. Chem. 284, 17883-17896
8. Wang, C., Wang, C., Hoch, E. G., and Pitt, G. S. (2011) Identification of novel interaction sites that determine specificity between fibroblast growth factor homologous factors and voltage-gated sodium channels. J. Biol. Chem. 286, 24253-24263
9. Wittmack, E. K., Rush, A. M., Craner, M. J., Goldfarb, M., Waxman, S. G., and Dib-Hajj, S. D. (2004) Fibroblast growth factor homologous factor 2B: association with Nav1.6 and selective colocalization at nodes of Ranvier of dorsal root axons. J. Neurosci. 24, 6765-6775
10. Liu, Cj, Dib-Hajj, S. D., and Waxman, S. G. (2001) Fibroblast growth factor homologous factor 1B binds to the C terminus of the tetrodotoxin- resistant sodium channel rNav1.9a (NaN). J. Biol. Chem. 276, 18925-18933
11. Liu, C. J., Dib-Hajj, S. D., Renganathan, M., Cummins, T. R., and Waxman, S. G. (2003) Modulation of the cardiac sodium channel Nav1.5 by fibroblast growth factor homologous factor 1B. J. Biol. Chem. 278, 1029-1036
12. Goldfarb, M., Schoorlemmer, J., Williams, A., Diwakar, S., Wang, Q., Huang, X., Giza, J., Tchetchik, D., Kelley, K., Vega, A., Matthews, G., Rossi, P., Ornitz, D. M., and D'Angelo, E. (2007) Fibroblast growth factor homologous factors control neuronal excitability through modulation of voltage-gated sodium channels. Neuron 55, 449-463
13. Shakkottai, V. G., Xiao, M., Xu, L., Wong, M., Nerbonne, J. M., Ornitz, D. M., and Yamada, K. A. (2009) FGF14 regulates the intrinsic excitability of cerebellar Purkinje neurons. Neurobiol. Dis. 33, 81-88
14. Shavkunov, A., Panova, N., Prasai, A., Veselenak, R., Bourne, N., Stoilova-McPhie, S., and Laezza, F. (2012) Bioluminescence methodology for the detection of protein/protein interactions within the voltage-gated sodium channel macromolecular complex. Assay Drug Dev. Technol. 10, 148-160
15. Xiao, M., Xu, L., Laezza, F., Yamada, K., Feng, S., Ornitz, D.M. (2007) Impaired hippocampal synaptic transmission and plasticity in mice lacking fibroblast growth factor. Mol. Cell. Neurosci. 34, 366-377
16. Wozniak, D. F., Xiao, M., Xu, L., Yamada, K. A., and Ornitz, D. M. (2007) Impaired spatial learning and defective θ burst induced LTP in mice lacking fibroblast growth factor. Neurobiol. Dis. 1, 14-26
17. Wang, Q., Bardgett, M. E., Wong, M., Wozniak, D. F., Lou, J., McNeil, B. D., Chen, C., Nardi, A., Reid, D. C., Yamada, K., and Ornitz, D. M. (2002) Ataxia and paroxysmal dyskinesia in mice lacking axonally transported FGF14. Neuron 35, 25-38
18. Brusse, E., de Koning, I., Maat-Kievit, A., Oostra, B. A., Heutink, P., and van Swieten, J. C. (2006) Spinocerebellar ataxia associated with a mutation in the fibroblast growth factor 14 gene (SCA27): A new phenotype. Mov. Disord. 21, 396-401
19. van Swieten, J. C., Brusse, E., de Graaf, B. M., Krieger, E., van de Graaf, R., de Koning, I., Maat-Kievit, A., Leegwater, P., Dooijes, D., Oostra, B. A., and Heutink, P. (2003) A mutation in the fibroblast growth factor 14 gene is associated with autosomal dominant cerebellar ataxia (corrected). Am. J. Hum. Genet. 72, 191-199
20. Wildburger, N. C., and Laezza, F. (2012) Control of neuronal ion channel function by glycogen synthase kinase-3: new prospective for an old kinase. Front. Mol. Neurosci. 5, 80
21. Schiavon, E., Sacco, T., Cassulini, R. R., Gurrola, G., Tempia, F., Possani, L. D., and Wanke, E. (2006) Resurgent current and voltage sensor trapping enhanced activation by a β-scorpion toxin solely in Nav1.6 channel. Significance in mice Purkinje neurons. J. Biol. Chem. 281, 20326-20337
22. Trimmer, J. S. (1991) Immunological identification and characterization of a delayed rectifier K+ channel polypeptide in rat brain. Proc. Natl. Acad. Sci. U.S.A. 88, 10764-10768
23. Berendt, F. J., Park, K. S., and Trimmer, J. S. (2010) Multisite phosphorylation of voltage-gated sodium channel β subunits from rat brain. J. Proteome Res. 9, 1976-1984
24. Liao, Y., Deprez, L., Maljevic, S., Pitsch, J., Claes, L., Hristova, D., Jordanova, A., Ala-Mello, S., Bellan-Koch, A., Blazevic, D., Schubert, S., Thomas, E. A., Petrou, S., Becker, A. J., De Jonghe, P., and Lerche, H. (2010) Molecular correlates of age-dependent seizures in an inherited neonatalinfantile epilepsy. Brain 133, 1403-1414
25. Goslin, K., Asmussen, H., and Banker, G. (1998) in Culturing Nerve Cells (Banker, G., and Goslin, K., eds) pp. 339-370, MIT Press, Cambridge,MA
26. Luker, K. E., Smith, M. C., Luker, G. D., Gammon, S. T., Piwnica-Worms, H., and Piwnica-Worms, D. (2004) Kinetics of regulated protein/protein interactions revealed with firefly luciferase complementation imaging in cells and living animals. Proc. Natl. Acad. Sci. U.S.A. 101, 12288-12293
27. Schütz, S. V., Cronauer, M. V., and Rinnab, L. (2010) Inhibition of glycogen synthase kinase-3β promotes nuclear export of the androgen receptor through a CRM1-dependent mechanism in prostate cancer cell lines. J. Cell. Biochem. 109, 1192-1200
28. Rinnab, L., Schütz, S. V., Diesch, J., Schmid, E., Küfer, R., Hautmann, R. E., Spindler, K. D., and Cronauer, M. V. (2008) Inhibition of glycogen synthase kinase-3 in androgen-responsive prostate cancer cell lines: are GSK inhibitors therapeutically useful? Neoplasia 10, 624-634
29. Eldar-Finkelman, H., and Martinez, A. (2011) GSK-3 inhibitors: preclinical and clinical focus on CNS. Front. Mol. Neurosci. 4, 32
30. Kim, Y. T., Hur, E. M., Snider, W. D., and Zhou, F. Q. (2011) Role of GSK3 signaling in neuronal morphogenesis. Front. Mol. Neurosci. 4, 48
31. Peineau, S., Taghibiglou, C., Bradley, C., Wong, T. P., Liu, L., Lu, J., Lo, E., Wu, D., Saule, E., Bouschet, T., Matthews, P., Isaac, J. T., Bortolotto, Z. A., Wang, Y. T., and Collingridge, G. L. (2007) LTP inhibits LTD in the hippocampus via regulation of GSK3β. Neuron 53, 703-717
32. Hernández, F., Gómez de Barreda, E., Fuster-Matanzo, A., Lucas, J. J., and Avila, J. (2010) GSK3: a possible link between β-amyloid peptide and tau protein. Exp. Neurol. 223, 322-325
33. Jope, R. S., and Roh, M. S. (2006) Glycogen synthase kinase-3 (GSK3) in psychiatric diseases and therapeutic interventions. Curr. Drug Targets 7, 1421-1434
34. Polter, A. M., Yang, S., Jope, R. S., and Li, X. (2012) Functional significance of glycogen synthase kinase-3 regulation by serotonin. Cell. Signal. 24, 265-271
35. Li, X., and Jope, R. S. (2010) Is glycogen synthase kinase-3 a central modulator in mood regulation? Neuropsychopharmacology 35, 2143-2154
36. Clayton, E. L., Sue, N., Smillie, K. J., O'Leary, T., Bache, N., Cheung, G., Cole, A. R., Wyllie, D. J., Sutherland, C., Robinson, P. J., and Cousin, M. A. (2010) Dynamin I phosphorylation by GSK3 controls activity-dependent bulk endocytosis of synaptic vesicles. Nat. Neurosci. 13, 845-851
37. Tang, M., Villaescusa, J. C., Luo, S. X., Guitarte, C., Lei, S., Miyamoto, Y., Taketo, M. M., Arenas, E., and Huang, E. J. (2010) Interactions of Wnt/+- catenin signaling and sonic hedgehog regulate the neurogenesis of ventral midbrain dopamine neurons. J. Neurosci. 30, 9280-9291
38. Komada, M., and Soriano, P. (2002) βIV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J. Cell Biol. 156, 337-348
39. Anastassiadis, T., Deacon, S. W., Devarajan, K., Ma, H., and Peterson, J. R. (2011) Comprehensive assay of kinase catalytic activity reveals features of kinase inhibitor selectivity. Nat. Biotechnol. 29, 1039-1045
40. Van Wart, A., Trimmer, J. S., and Matthews, G. (2007) Polarized distribution of ion channels within microdomains of the axon initial segment. J. Comp. Neurol. 500, 339-352
41. Garrido, J. J., Fernandes, F., Giraud, P., Mouret, I., Pasqualini, E., Fache, M. P., Jullien, F., and Dargent, B. (2001) Identification of an axonal determinant in the C terminus of the sodium channel Nav1.2. EMBO J. 20, 5950-5961
42. Leroy, K., and Brion, J. P. (1999) Developmental expression and localization of glycogen synthase kinase-3β in rat brain. J. Chem. Neuroanat. 16, 279-293
43. Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A., and Kaibuchi, K. (2005) GSK-3β regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120, 137-149
44. Kim, W. Y., and Snider, W. D. (2011) Functions of GSK-3 signaling in development of the nervous system. Front. Mol. Neurosci. 4, 44
45. Namekata, K., Harada, C., Guo, X., Kimura, A., Kittaka, D., Watanabe, H., and Harada, T. (2012) Dock3 stimulates axonal outgrowth via GSK-3β- mediated microtubule assembly. J. Neurosci. 32, 264-274