Reciprocal changes in phosphorylation and methylation of mammalian brain sodium channels in response to seizures

Journal of Biological Chemistry

Volumn 289, Issue 22, 2014, Pages 15363-15373

  Baek, Je Hyun ^a   Rubinstein, Moran ^b   Scheuer, Todd ^b   Trimmer, James S ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; MAMMALS; METHYLATION; PHOSPHORYLATION;

MAMMALIAN BRAIN; MASS SPECTROMETRIC ANALYSIS; SODIUM CHANNEL; SODIUM CHANNEL FUNCTIONS;

TOXIC MATERIALS;

PROTEIN ARGININE METHYLTRANSFERASE; SODIUM CHANNEL NAV1.2;

ACTION POTENTIAL; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; MALE; MASS SPECTROMETRY; MOUSE; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RAT; SEIZURE;

ELECTROPHYSIOLOGY; EPILEPSY; ION CHANNELS; MASS SPECTROMETRY (MS); PROTEOMICS;

ACTION POTENTIALS; ANIMALS; ARGININE; BRAIN; CELL LINE; DISEASE MODELS, ANIMAL; EPILEPSY; EXCITATORY AMINO ACID AGONISTS; KAINIC ACID; KIDNEY; MALE; MASS SPECTROMETRY; METHYLATION; NAV1.2 VOLTAGE-GATED SODIUM CHANNEL; PHOSPHORYLATION; PROTEOMICS; RATS;

EID: 84901724023     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.562785     Document Type: Article

References (54)

1. Catterall, W. A., Goldin, A. L., and Waxman, S. G. (2005) International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol. Rev. 57, 397-409
2. + channels: An unexpected form of cellular plasticity. Nat. Rev. Neurosci. 2, 397-407
3. Berendt, F. J., Park, K. S., and Trimmer, J. S. (2010) Multisite phosphorylation of voltage-gated sodium channel α subunits from rat brain. J. Proteome Res. 9, 1976-1984
4. Vacher, H., Mohapatra, D. P., and Trimmer, J. S. (2008) Localization and targeting of voltage-dependent ion channels in mammalian central neurons. Physiol. Rev. 88, 1407-1447
5. Scheuer, T. (2011) Regulation of sodium channel activity by phosphorylation. Semin. Cell Dev. Biol. 22, 160-165
6. Baek, J. H., Cerda, O., and Trimmer, J. S. (2011) Mass spectrometry-based phosphoproteomics reveals multisite phosphorylation on mammalian brain voltage-gated sodium and potassium channels. Semin. Cell Dev. Biol. 22, 153-159
7. Trimmer, J. S., and Misonou, H. (2014) Phosphorylation of voltage-gated ion channels. in Handbook of Ion Channels (Zheng, J., and Trudeau, M. C., eds) CRC Press, Inc., Boca Raton, FL
8. Bréchet, A., Fache, M. P., Brachet, A., Ferracci, G., Baude, A., Irondelle, M., Pereira, S., Leterrier, C., and Dargent, B. (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
9. + channel required for modulation by protein kinase C. Science 254, 866-868
10. + channel slow inactivation via cAMP-dependent protein kinase and protein kinase C. Neuron 49, 409-420
11. Ben-Ari, Y. (2006) Seizures beget seizures: The quest for GABA as a key player. Crit. Rev. Neurobiol. 18, 135-144
12. Qiao, X., Werkman, T. R., Gorter, J. A., Wadman, W. J., and van Vliet, E. A. (2013) Expression of sodium channel α subunits 1.1, 1.2 and 1.6 in rat hippocampus after kainic acid-induced epilepsy. Epilepsy Res. 106, 17-28
13. Guo, F., Xu, X., Cai, J., Hu, H., Sun, W., He, G., Shao, D., Wang, L., Chen, T., Shaw, C., Zhu, T., and Hao, L. (2013) The up-regulation of voltagegated sodium channels subtypes coincides with an increased sodium current in hippocampal neuronal culture model. Neurochem. Int. 62, 287-295
14. Jung, S., Bullis, J. B., Lau, I. H., Jones, T. D., Warner, L. N., and Poolos, N. P. (2010) Downregulation of dendritic HCN channel gating in epilepsy is mediated by altered phosphorylation signaling. J. Neurosci. 30, 6678-6688
15. Williams, C. A., and Battaglia, A. (2013) Molecular biology of epilepsy genes. Exp. Neurol. 244, 51-58
16. White, H. S., Smith, M. D., and Wilcox, K. S. (2007) Mechanisms of action of antiepileptic drugs. Int. Rev. Neurobiol. 81, 85-110
17. Vreugdenhil, M., and Wadman, W. J. (1999) Modulation of sodium currents in rat CA1 neurons by carbamazepine and valproate after kindling epileptogenesis. Epilepsia 40, 1512-1522
18. + channels in hippocampal neurons of control and chronically epileptic rats. Eur. J. Neurosci. 17, 2648-2658
19. Schaub, C., Uebachs, M., and Beck, H. (2007) Diminished response of CA1 neurons to antiepileptic drugs in chronic epilepsy. Epilepsia 48, 1339-1350
20. Jeub, M., Beck, H., Siep, E., Rüschenschmidt, C., Speckmann, E. J., Ebert, U., Potschka, H., Freichel, C., Reissmüller, E., and Löscher, W. (2002) Effect of phenytoin on sodium and calcium currents in hippocampal CA1 neurons of phenytoin-resistant kindled rats. Neuropharmacology 42, 107-116
21. Curia, G., Aracri, P., Sancini, G., Mantegazza, M., Avanzini, G., and Franceschetti, S. (2004) Protein-kinase C-dependent phosphorylation inhibits the effect of the antiepileptic drug topiramate on the persistent fraction of sodium currents. Neuroscience 127, 63-68
22. Vreugdenhil, M., Hoogland, G., van Veelen, C. W., and Wadman, W. J. (2004) Persistent sodium current in subicular neurons isolated from patients with temporal lobe epilepsy. Eur. J. Neurosci. 19, 2769-2778
23. Curia, G., Aracri, P., Colombo, E., Scalmani, P., Mantegazza, M., Avanzini, G., and Franceschetti, S. (2007) Phosphorylation of sodium channels mediated by protein kinase-C modulates inhibition by topiramate of tetrodotoxin- sensitive transient sodium current. Br. J. Pharmacol. 150, 792-797
24. Beck, H. (2007) Plasticity of antiepileptic drug targets. Epilepsia 48, Suppl. 1, 14-18
25. Agrawal, N., Alonso, A., and Ragsdale, D. S. (2003) Increased persistent sodium currents in rat entorhinal cortex layer V neurons in a post-status epilepticus model of temporal lobe epilepsy. Epilepsia 44, 1601-1604
26. Hargus, N. J., Merrick, E. C., Nigam, A., Kalmar, C. L., Baheti, A. R., Bertram, E. H., 3rd, and Patel, M. K. (2011) Temporal lobe epilepsy induces intrinsic alterations in Na channel gating in layer II medial entorhinal cortex neurons. Neurobiol. Dis. 41, 361-376
27. + channels following pilocarpine-induced status epilepticus in rat dentate granule cells. Neuroscience 119, 323-333
28. Misonou, H., Mohapatra, D. P., Park, E. W., Leung, V., Zhen, D., Misonou, K., Anderson, A. E., and Trimmer, J. S. (2004) Regulation of ion channel localization and phosphorylation by neuronal activity. Nat. Neurosci. 7, 711-718
29. Racine, R., Okujava, V., and Chipashvili, S. (1972) Modification of seizure activity by electrical stimulation. 3. Mechanisms. Electroencephalogr. Clin. Neurophysiol. 32, 295-299
30. + channel polypeptide in rat brain. Proc. Natl. Acad. Sci. U.S.A. 88, 10764-10768
31. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. (2011) Andromeda: A peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805
32. Kim, S., Mischerikow, N., Bandeira, N., Navarro, J. D., Wich, L., Mohammed, S., Heck, A. J., and Pevzner, P. A. (2010) The generating function of CID, ETD, and CID/ETD pairs of tandem mass spectra: applications to database search. Mol. Cell Proteomics 9, 2840-2852
33. Lee, J., Sayegh, J., Daniel, J., Clarke, S., and Bedford, M. T. (2005) PRMT8, a new membrane-bound tissue-specific member of the protein arginine methyltransferase family. J. Biol. Chem. 280, 32890-32896
34. Catterall, W. A. (2012) Voltage-gated sodium channels at 60: structure, function and pathophysiology. J. Physiol. 590, 2577-2589
35. Beacham, D., Ahn, M., Catterall, W. A., and Scheuer, T. (2007) Sites and molecular mechanisms of modulation of Na(v)1.2 channels by Fyn tyrosine kinase. J. Neurosci. 27, 11543-11551
36. Velisek, L. (2006) Models of chemically-induced acute seizures. in Models of Seizures and Epilepsy (Pitkanen, A., Schwartzkroin, P. A., and Moshe, S. L. eds) pp. 127-152, Elsevier Academic Press, San Diego
37. Ketelaars, S. O., Gorter, J. A., van Vliet, E. A., Lopes da Silva, F. H., and Wadman, W. J. (2001) Sodium currents in isolated rat CA1 pyramidal and dentate granule neurones in the post-status epilepticus model of epilepsy. Neuroscience 105, 109-120
38. Vreugdenhil, M., Faas, G. C., and Wadman, W. J. (1998) Sodium currents in isolated rat CA1 neurons after kindling epileptogenesis. Neuroscience 86, 99-107
39. Rakhade, S. N., and Jensen, F. E. (2009) Epileptogenesis in the immature brain: emerging mechanisms. Nat. Rev. Neurol. 5, 380-391
40. Bartolomei, F., Gastaldi, M., Massacrier, A., Planells, R., Nicolas, S., and Cau, P. (1997) Changes in the mRNAs encoding subtypes I, II and III sodium channel α subunits following kainate-induced seizures in rat brain. J. Neurocytol. 26, 667-678
41. Whitaker, W. R., Faull, R. L., Dragunow, M., Mee, E. W., Emson, P. C., and Clare, J. J. (2001) Changes in the mRNAs encoding voltage-gated sodium channel types II and III in human epileptic hippocampus. Neuroscience 106, 275-285
42. Minge, D., and Bähring, R. (2011) Acute alterations of somatodendritic action potential dynamics in hippocampal CA1 pyramidal cells after kainate- induced status epilepticus in mice. PLoS One 6, e26664
43. Schmidt, J. W., and Catterall, W. A. (1986) Biosynthesis and processing of the alpha subunit of the voltage-sensitive sodium channel in rat brain neurons. Cell 46, 437-444
44. Bosmans, F., Milescu, M., and Swartz, K. J. (2011) Palmitoylation influences the function and pharmacology of sodium channels. Proc. Natl. Acad. Sci. U.S.A. 108, 20213-20218
45. Isaev, D., Isaeva, E., Shatskih, T., Zhao, Q., Smits, N. C., Shworak, N. W., Khazipov, R., and Holmes, G. L. (2007) Role of extracellular sialic acid in regulation of neuronal and network excitability in the rat hippocampus. J. Neurosci. 27, 11587-11594
46. Badeaux, A. I., and Shi, Y. (2013) Emerging roles for chromatin as a signal integration and storage platform. Nat. Rev. Mol. Cell Biol. 14, 211-224
47. Ubersax, J. A., and Ferrell, J. E., Jr. (2007) Mechanisms of specificity in protein phosphorylation. Nat. Rev. Mol. Cell Biol. 8, 530-541
48. Liu, F., Zhao, X., Perna, F., Wang, L., Koppikar, P., Abdel-Wahab, O., Harr, M. W., Levine, R. L., Xu, H., Tefferi, A., Deblasio, A., Hatlen, M., Menendez, S., and Nimer, S. D. (2011) JAK2V617F-mediated phosphorylation of PRMT5 downregulates its methyltransferase activity and promotes myeloproliferation. Cancer Cell 19, 283-294
49. Kanade, S. R., and Eckert, R. L. (2012) Protein arginine methyltransferase 5 (PRMT5) signaling suppresses protein kinase Cδ- and p38δ-dependent signaling and keratinocyte differentiation. J. Biol. Chem. 287, 7313-7323
50. Taneda, T., Miyata, S., Kousaka, A., Inoue, K., Koyama, Y., Mori, Y., and Tohyama, M. (2007) Specific regional distribution of protein arginine methyltransferase 8 (PRMT8) in the mouse brain. Brain Res. 1155, 1-9
51. Kousaka, A., Mori, Y., Koyama, Y., Taneda, T., Miyata, S., and Tohyama, M. (2009) The distribution and characterization of endogenous protein arginine N-methyltransferase 8 in mouse CNS. Neuroscience 163, 1146-1157
52. Barth, T. K., and Imhof, A. (2010) Fast signals and slow marks: The dynamics of histone modifications. Trends Biochem. Sci. 35, 618-626
53. Beltran-Alvarez, P., Pagans, S., and Brugada, R. (2011) The cardiac sodium channel is post-translationally modified by arginine methylation. J. Proteome Res. 10, 3712-3719
54. Beltran-Alvarez, P., Espejo, A., Schmauder, R., Beltran, C., Mrowka, R., Linke, T., Batlle, M., Pérez-Villa, F., Pérez, G. J., Scornik, F. S., Benndorf, K., Pagans, S., Zimmer, T., and Brugada, R. (2013) Protein arginine methyl transferases-3 and -5 increase cell surface expression of cardiac sodium channel. FEBS Lett. 587, 3159-3165