Crystal structure and molecular imaging of the Nav channelβ3 subunit indicates a trimeric assembly

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10797-10811

  Namadurai, Sivakumar ^a   Balasuriya, Dilshan ^a   Rajappa, Rajit ^b   Wiemhöfer, Martin ^b   Stott, Katherine ^a   Klingauf, Jurgen ^b   Edwardson, J Michael ^a   Chirgadze, Dimitri Y ^a   Jackson, Antony P ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ATOMIC FORCE MICROSCOPY; CELL MEMBRANES; MOLECULAR IMAGING; MONOMERS; SODIUM;

ANALYTICAL ULTRACENTRIFUGATION; ASYMMETRIC UNIT; CHANNEL MUTATIONS; CYSTEINE RESIDUES; FREE SOLUTIONS; ION-CONDUCTING; PHOTO-ACTIVATED; STRUCTURAL INSIGHTS;

DIMERS;

VOLTAGE GATED SODIUM CHANNEL BETA 3 SUBUNIT;

ARTICLE; ATOMIC FORCE MICROSCOPY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; FLUORESCENCE MICROSCOPY; FLUORESCENCE PHOTOACTIVATED LOCALIZATION MICROSCOPY; HUMAN; HUMAN CELL; IN VIVO STUDY; MOLECULAR CLONING; MOLECULAR IMAGING; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; ULTRACENTRIFUGATION;

ANALYTICAL ULTRACENTRIFUGATION; ATOMIC FORCE MICROSCOPY; IN VIVO IMAGING; PHOTOACTIVATED LOCALIZATION MICROSCOPY; PROTEIN TRIMERIZATION; SODIUM CHANNELS; X-RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BINDING SITES; CLONING, MOLECULAR; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HEK293 CELLS; HUMANS; IMMUNOGLOBULINS; MICROSCOPY, ATOMIC FORCE; MOLECULAR SEQUENCE DATA; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; PROTEIN CONFORMATION; ULTRACENTRIFUGATION; VOLTAGE-GATED SODIUM CHANNEL BETA-3 SUBUNIT;

EID: 84898618987     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.527994     Document Type: Article

References (62)

1. Waxman, S. G. (2012) Sodium channels, the electrogenisome and the electrogenistat: lessons and questions from the clinic. J. Physiol. 590, 2601-2612
2. Catterall, W. A. (2012) Voltage-gated sodium channels at 60: structure, function and pathophysiology. J. Physiol. 590, 2577-2589
3. + channelopathies and sinus node dysfunction. Prog. Biophys. Mol. Biol. 98, 171-178
4. Brackenbury, W. J., and Isom, L. L. (2011) Na channel β subunits: overachievers of the ion channel family. Front. Pharmacol. 2, 53
5. + channel β-subunits in development and disease. Neurosci. Lett. 486, 53-59
6. Cusdin, F. S., Clare, J. J., and Jackson, A. P. (2008) Trafficking and cellular distribution of voltage-gated sodium channels. Traffic 9, 17-26
7. McEwen, D. P., and Isom, L. L. (2004) Heterophilic interactions of sodium channel β1 subunits with axonal and glial cell adhesion molecules. J. Biol. Chem. 279, 52744-52752
8. Srinivasan, J., Schachner, M., and Catterall, W. A. (1998) Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R. Proc. Natl. Acad. Sci. U.S.A. 95, 15753-15757
9. Ratcliffe, C. F., Westenbroek, R. E., Curtis, R., and Catterall, W. A. (2001) Sodium channel β1 and β3 subunits associate with neurofascin through their extracellular immunoglobulin-like domain. J. Cell Biol. 154, 427-434
10. Yu, E. J., Ko, S. H., Lenkowski, P. W., Pance, A., Patel, M. K., and Jackson, A. P. (2005) Distinct domains of the sodium channel β-3-subunit modulate channel-gating kinetics and subcellular location. Biochem. J. 392, 519-526
11. Morgan, K., Stevens, E. B., Shah, B., Cox, P. J., Dixon, A. K., Lee, K., Pinnock, R. D., Hughes, J., Richardson, P. J., Mizuguchi, K., and Jackson, A. P. (2000) β-3: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics. Proc. Natl. Acad. Sci. U.S.A. 97, 2308-2313
12. Cusdin, F. S., Nietlispach, D., Maman, J., Dale, T. J., Powell, A. J., Clare, J. J., and Jackson, A. P. (2010) The sodium channel β-3-subunit induces multiphasic gating in NaV1.3 and affects fast inactivation via distinct intracellular regions. J. Biol. Chem. 285, 33404-33412
13. Yereddi, N. R., Cusdin, F. S., Namadurai, S., Packman, L. C., Monie, T. P., Slavny, P., Clare, J. J., Powell, A. J., and Jackson, A. P. (2013) The immunoglobulin domain of the sodium channel β-3 subunit contains a surfacelocalized disulfide bond that is required for homophilic binding. FASEB J. 27, 568-580
14. Hakim, P., Brice, N., Thresher, R., Lawrence, J., Zhang, Y., Jackson, A. P., Grace, A. A., and Huang, C. L. (2010) Scn3b knockout mice exhibit abnormal sino-atrial and cardiac conduction properties. Acta Physiol. 198, 47-59
15. Hakim, P., Gurung, I. S., Pedersen, T. H., Thresher, R., Brice, N., Lawrence, J., Grace, A. A., and Huang, C. L. (2008) Scn3b knockout mice exhibit abnormal ventricular electrophysiological properties. Prog. Biophys. Mol. Biol. 98, 251-266
16. Matthews, B. W. (1968) Solvent content of protein crystals. J. Mol. Biol. 33, 491-497
17. Kabsch, W. (2010) Integration, scaling, space-group assignment and postrefinement. Acta Crystallogr. D Biol. Crystallogr. 66, 133-144
18. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc- Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
19. Shi, J., Blundell, T. L., and Mizuguchi, K. (2001) FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310, 243-257
20. Leppänen, V. M., Prota, A. E., Jeltsch, M., Anisimov, A., Kalkkinen, N., Strandin, T., Lankinen, H., Goldman, A., Ballmer-Hofer, K., and Alitalo, K. (2010) Structural determinants of growth factor binding and specificity by VEGF receptor 2. Proc. Natl. Acad. Sci. U.S.A. 107, 2425-2430
21. Stamper, C. C., Zhang, Y., Tobin, J. F., Erbe, D. V., Ikemizu, S., Davis, S. J., Stahl, M. L., Seehra, J., Somers, W. S., and Mosyak, L. (2001) Crystal structure of the B7-1/CTLA-4 complex that inhibits human immune responses. Nature 410, 608-611
22. Kostrewa, D., Brockhaus, M., D'Arcy, A., Dale, G. E., Nelboeck, P., Schmid, G., Mueller, F., Bazzoni, G., Dejana, E., Bartfai, T., Winkler, F. K., and Hennig, M. (2001) X-ray structure of junctional adhesion molecule: Structural basis for homophilic adhesion via a novel dimerization motif. EMBO J. 20, 4391-4398
23. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
24. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
25. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797
26. Laue, T., Shah, B., Ridgeway, T., and Pelletier, S. (1992) in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S., and Rowe, A., eds) pp. 90-125, Royal Society of Chemistry, Cambridge, UK
27. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
28. + channel with 4-fold symmetry. J. Biol. Chem. 287, 37021-37029
29. Schneider, S. W., Lärmer, J., Henderson, R. M., and Oberleithner, H. (1998) Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy. Pflügers Arch. 435, 362-367
30. Neaves, K. J., Cooper, L. P., White, J. H., Carnally, S. M., Dryden, D. T., Edwardson, J. M., and Henderson, R. M. (2009) Atomic force microscopy of the EcoKI type IDNArestriction enzyme bound toDNAshows enzyme dimerization and DNA looping. Nucleic Acids Res. 37, 2053-2063
31. Balasuriya, D., Stewart, A. P., and Edwardson, J. M. (2013) The σ-1 receptor interacts directly with GluN1 but not GluN2A in the GluN1/GluN2A NMDA receptor. J. Neurosci. 33, 18219-18224
32. Scott, D. W. (1979) On optimal and data-based histograms. Biometrika 66, 605-610
33. Welch, B. (1947) The generalisation of student's problems when several different population variances are involved. Biometrika 34, 28-35
34. Niu, L., and Yu, J. (2008) Investigating intracellular dynamics of FtsZ cytoskeleton with photoactivation single-molecule tracking. Biophys. J. 95, 2009-2016
35. Chaudhuri, S., Chakraborty, S., and Sengupta, P. K. (2011) Probing the interactions of hemoglobin with antioxidant flavonoids via fluorescence spectroscopy and molecular modeling studies. Biophys. Chem. 154, 26-34
36. Veatch, S. L., Machta, B. B., Shelby, S. A., Chiang, E. N., Holowka, D. A., and Baird, B. A. (2012) Correlation functions quantify super-resolution images and estimate apparent clustering due to over-counting. PLoS One 7, e31457
37. Isom, L. L., De Jongh, K. S., Patton, D. E., Reber, B. F., Offord, J., Charbonneau, H., Walsh, K., Goldin, A. L., and Catterall, W. A. (1992) Primary structure and functional expression of the β1 subunit of the rat brain sodium channel. Science 256, 839-842
38. Isom, L. L., Ragsdale, D. S., De Jongh, K. S., Westenbroek, R. E., Reber, B. F., Scheuer, T., and Catterall, W. A. (1995) Structure and function of the β2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell 83, 433-442
39. Yu, F. H., Westenbroek, R. E., Silos-Santiago, I., McCormick, K. A., Lawson, D., Ge, P., Ferriera, H., Lilly, J., DiStefano, P. S., Catterall, W. A., Scheuer, T., and Curtis, R. (2003) Sodium channel β4, a new disulfidelinked auxiliary subunit with similarity to β2. J. Neurosci. 23, 7577-7585
40. Bork, P., Holm, L., and Sander, C. (1994) The immunoglobulin fold. Structural classification, sequence patterns and common core. J. Mol. Biol. 242, 309-320
41. Hess, S. T., Girirajan, T. P., and Mason, M. D. (2006) Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91, 4258-4272
42. Betzig, E., Patterson, G. H., Sougrat, R., Lindwasser, O. W., Olenych, S., Bonifacino, J. S., Davidson, M. W., Lippincott-Schwartz, J., and Hess, H. F. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642-1645
43. McKinney, S. A., Murphy, C. S., Hazelwood, K. L., Davidson, M. W., and Looger, L. L. (2009) A bright and photostable photoconvertible fluorescent protein. Nat. Methods 6, 131-133
44. Sengupta, P., Jovanovic-Talisman, T., Skoko, D., Renz, M., Veatch, S. L., and Lippincott-Schwartz, J. (2011) Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nat. Methods 8, 969-975
45. Sherwood, T. W., Frey, E. N., and Askwith, C. C. (2012) Structure and activity of the acid-sensing ion channels. Am. J. Physiol. Cell Physiol. 303, C699-C710
46. Tsien, R. Y. (1998) The green fluorescent protein. Annu. Rev. Biochem. 67, 509-544
47. Fahmi, A. I., Patel, M., Stevens, E. B., Fowden, A. L., John, J. E., 3rd, Lee, K., Pinnock, R., Morgan, K., Jackson, A. P., and Vandenberg, J. I. (2001) The sodium channelβ-subunit SCN3b modulates the kinetics of SCN5a and is expressed heterogeneously in sheep heart. J. Physiol. 537, 693-700
48. van der Merwe, P. A., and Barclay, A. N. (1994) Transient intercellular adhesion: The importance of weak protein-protein interactions. Trends Biochem. Sci. 19, 354-358
49. Gratkowski, H., Lear, J. D., and DeGrado, W. F. (2001) Polar side chains drive the association of model transmembrane peptides. Proc. Natl. Acad. Sci. U.S.A. 98, 880-885
50. Spampanato, J., Kearney, J. A., de Haan, G., McEwen, D. P., Escayg, A., Aradi, I., MacDonald, B. T., Levin, S. I., Soltesz, I., Benna, P., Montalenti, E., Isom, L. L., Goldin, A. L., and Meisler, M. H. (2004) A novel epilepsy mutation in the sodium channel SCN1A identifies a cytoplasmic domain for β subunit interaction. J. Neurosci. 24, 10022-10034
51. Valdivia, C. R., Medeiros-Domingo, A., Ye, B., Shen, W. K., Algiers, T. J., Ackerman, M. J., and Makielski, J. C. (2010) Loss-of-function mutation of the SCN3B-encoded sodium channel β-3 subunit associated with a case of idiopathic ventricular fibrillation. Cardiovasc. Res. 86, 392-400
52. Wang, P., Yang, Q., Wu, X., Yang, Y., Shi, L., Wang, C., Wu, G., Xia, Y., Yang, B., Zhang, R., Xu, C., Cheng, X., Li, S., Zhao, Y., Fu, F., Liao, Y., Fang, F., Chen, Q., Tu, X., and Wang, Q. K. (2010) Functional dominant-negative mutation of sodium channel subunit gene SCN3B associated with atrial fibrillation in a Chinese GeneID population. Biochem. Biophys. Res. Commun. 398, 98-104
53. Tan, B. H., Pundi, K. N., Van Norstrand, D. W., Valdivia, C. R., Tester, D. J., Medeiros-Domingo, A., Makielski, J. C., and Ackerman, M. J. (2010) Sudden infant death syndrome-associated mutations in the sodium channel β-subunits. Heart Rhythm 7, 771-778
54. Ishikawa, T., Takahashi, N., Ohno, S., Sakurada, H., Nakamura, K., On, Y. K., Park, J. E., Makiyama, T., Horie, M., Arimura, T., Makita, N., and Kimura, A. (2013) Novel SCN3B mutation associated with brugada syndrome affects intracellular trafficking and function of Nav1.5. Circ. J. 77, 959-967
55. Mercier, A., Clément, R., Harnois, T., Bourmeyster, N., Faivre, J. F., Findlay, I., Chahine, M., Bois, P., and Chatelier, A. (2012) The α1-subunit of Na(v) 1.5 cardiac sodium channel is required for a dominant negative effect through α- α interaction. PLoS One 7, e48690
56. Veitia, R. A. (2007) Exploring the molecular etiology of dominant-negative mutations. Plant Cell 19, 3843-3851
57. Fendri-Kriaa, N., Kammoun, F., Salem, I. H., Kifagi, C., Mkaouar-Rebai, E., Hsairi, I., Rebai, A., Triki, C., and Fakhfakh, F. (2011) New mutation c. 374C3T and a putative disease-associated haplotype within SCN1B gene in Tunisian families with febrile seizures. Eur. J. Neurol. 18, 695-702
58. Patino, G. A., Claes, L. R., Lopez-Santiago, L. F., Slat, E. A., Dondeti, R. S., Chen, C., O'Malley, H. A., Gray, C. B., Miyazaki, H., Nukina, N., Oyama, F., De Jonghe, P., and Isom, L. L. (2009) A functional null mutation of SCN1B in a patient with Dravet syndrome. J. Neurosci. 29, 10764-10778
59. + channel function in the extracellular domain of the β1 subunit. J. Biol. Chem. 273, 3954-3962
60. Islas, A. A., Sánchez-Solano, A., Scior, T., Millan- Perezpeña, L., and Salinas- Stefanon, E. M. (2013) Identification of Nav β1 residues involved in the modulation of the sodium channel nav1.4. PLoS One 8, e81995
61. + channel α and β2 subunits. J. Biol. Chem. 287, 39061-39069
62. Gilchrist, J., Das, S., Van Petegem, F., and Bosmans, F. (2013) Crystallographic insights into sodium-channel modulation by the β4 subunit. Proc. Natl. Acad. Sci. U.S.A. 110, E5016-E5024