Palmitoylation of the β4-subunit regulates surface expression of large conductance calcium-activated potassium channel splice variants

Journal of Biological Chemistry

Volumn 288, Issue 18, 2013, Pages 13136-13144

  Chen, Lie ^a   Bi, Danlei ^a   Tian, Lijun ^a   McClafferty, Heather ^a   Steeb, Franziska ^b   Ruth, Peter ^b   Knaus, Hans Guenther ^c   Shipston, Michael J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM-ACTIVATED POTASSIUM; CELL SURFACE EXPRESSION; ENDOPLASMIC RETICULUM; FUNCTIONAL DIVERSITY; POST-TRANSCRIPTIONAL; POST-TRANSLATIONAL MODIFICATIONS; SURFACE EXPRESSION; VOLTAGE-ACTIVATED POTASSIUM;

ACYLATION; AMINO ACIDS; CALCIUM;

CELL MEMBRANES;

LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL BETA SUBUNIT; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL BETA4 SUBUNIT; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; CELL STRAIN HEK293; CELL SURFACE; CEREBELLUM; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NERVE CELL; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING;

ION CHANNELS; MEMBRANE TRANSPORT; POTASSIUM CHANNELS; PROTEIN PALMITOYLATION; S-ACYLATION; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; ANIMALS; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; LIPOYLATION; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; PROTEIN TRANSPORT;

EID: 84877147153     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.461830     Document Type: Article

References (32)

1. Orio, P., Rojas, P., Ferreira, G., and Latorre, R. (2002) New disguises for an old channel: MaxiK channel β-subunits. News Physiol. Sci. 17, 156-161
2. Yan, J., and Aldrich, R. W. (2012) BK potassium channel modulation by leucine-rich repeat-containing proteins. Proc. Natl. Acad. Sci. U.S.A. 109, 7917-7922
3. Brenner, R., Peréz, G. J., Bonev, A. D., Eckman, D. M., Kosek, J. C., Wiler, S. W., Patterson, A. J., Nelson, M. T., and Aldrich, R. W. (2000) Vasoregulation by the β1 subunit of the calcium-activated potassium channel. Nature 407, 870-876
4. -/- is linked to deficient K secretion and aldosteronism. Proc. Natl. Acad. Sci. U.S.A. 106, 11800-11805
5. Holtzclaw, J. D., Grimm, P. R., and Sansom, S. C. (2010) Intercalated cell BK-β/β4 channels modulate sodium and potassium handling during potassium adaptation. J. Am. Soc. Nephrol. 21, 634-645
6. Brenner, R., Chen, Q. H., Vilaythong, A., Toney, G. M., Noebels, J. L., and Aldrich, R. W. (2005) BK channel β4 subunit reduces dentate gyrus excitability and protects against temporal lobe seizures. Nat. Neurosci. 8, 1752-1759 (Pubitemid 41683204)
7. Shipston, M. J. (2011) Ion channel regulation by protein palmitoylation. J. Biol. Chem. 286, 8709-8716
8. Chen, L., Tian, L., MacDonald, S. H.-F., McClafferty, H., Hammond, M. S. L., Huibant, J.-M., Ruth, P., Knaus, H.-G., and Shipston, M. J. (2005) Functionally diverse complement of large conductance calcium- and voltage-activated potassium channel (BK) β-subunits generated from a single site of splicing. J. Biol. Chem. 280, 33599-33609 (Pubitemid 41397161)
9. Ca channels formed by bicistronic expression of hSloß and β1-4 subunits in HEK293 cells. J. Membr. Biol. 192, 141-148
10. Ren, J., Wen, L., Gao, X., Jin, C., Xue, Y., and Yao, X. (2008) CSS-Palm 2.0: an updated software for palmitoylation sites prediction. Protein Eng. Des. Sel. 21, 639-644
11. Tian, L., Jeffries, O., McClafferty, H., Molyvdas, A., Rowe, I. C. M., Saleem, F., Chen, L., Greaves, J., Chamberlain, L. H., Knaus, H.-G., Ruth, P., and Shipston, M. J. (2008) Palmitoylation gates phosphorylation-dependent regulation of BK potassium channels. Proc. Natl. Acad. Sci. U.S.A. 105, 21006-21011
12. Tian, L., McClafferty, H., Jeffries, O., and Shipston, M. J. (2010) Multiple palmitoyltransferases are required for palmitoylation-dependent regulation of large conductance calcium- and voltage-activated potassium channels. J. Biol. Chem. 285, 23954-23962
13. Forrester, M. T., Hess, D. T., Thompson, J. W., Hultman, R., Moseley, M. A., Stamler, J. S., and Casey, P. J. (2011) Site-specific analysis of protein S-acylation by resin-assisted capture. J. Lipid Res. 52, 393-398
14. Petrik, D., and Brenner, R. (2007) Regulation of STREX exon large conductance, calcium-activated potassium channels by the β4 accessory subunit. Neuroscience 149, 789-803 (Pubitemid 350122887)
15. Shruti, S., Urban-Ciecko, J., Fitzpatrick, J. A., Brenner, R., Bruchez, M. P., and Barth, A. L. (2012) The brain-specific β4 subunit downregulates BK channel cell surface expression. PLoS ONE 7, e33429
16. Jin, P., Weiger, T. M., and Levitan, I. B. (2002) Reciprocal modulation between the β and β4 subunits of hSlo calcium-dependent potassium channels. J. Biol. Chem. 277, 43724-43729 (Pubitemid 36157789)
17. Yang, C.-T., Zeng, X.-H., Xia, X.-M., and Lingle, C. J. (2009) Interactions between β subunits of the KCNMB family and Slo3: β4 selectively modulates Slo3 expression and function. PLoS ONE 4, e6135
18. Tian, L., McClafferty, H., Knaus, H.-G., Ruth, P., and Shipston, M. J. (2012) Distinct acyl protein transferases and thioesterases control surface expression of calcium-activated potassium channels. J. Biol. Chem. 287, 14718-14725
19. Jeffries, O., Geiger, N., Rowe, I. C. M., Tian, L., McClafferty, H., Chen, L., Bi, D., Knaus, H.-G., Ruth, P., and Shipston, M. J. (2010) Palmitoylation of the S0-S1 linker regulates cell surface expression of voltage- and calcium-activated potassium (BK) channels. J. Biol. Chem. 285, 33307-33314
20. Chiu, Y.-H., Alvarez-Baron, C., Kim, E. Y., and Dryer, S. E. (2010) Dominant-negative regulation of cell surface expression by a pentapeptide motif at the extreme COOH terminus of an Slo1 calcium-activated potassium channel splice variant. Mol. Pharmacol. 77, 497-507
21. Kim, E. Y., Ridgway, L. D., Zou, S., Chiu, Y.-H., and Dryer, S. E. (2007) Alternatively spliced C-terminal domains regulate the surface expression of large conductance calcium-activated potassium channels. Neuroscience 146, 1652-1661 (Pubitemid 46783216)
22. + channel isoform. J. Neurophysiol. 97, 3508-3516
23. 2+-gated (Slo1) potassium channels. FEBS Lett. 581, 1000-1008
24. + channel resistant to charybdotoxin and iberiotoxin. Proc. Natl. Acad. Sci. U.S.A. 97, 5562-5567
25. Behrens, R., Nolting, A., Reimann, F., Schwarz, M., Waldschütz, R., and Pongs, O. (2000) hKCNMB3 and hKCNMB4, cloning and characterization of two members of the large-conductance calcium-activated potassium channel β subunit family. FEBS Lett. 474, 99-106 (Pubitemid 30320840)
26. Nyholm, T. K. M., Ozdirekcan, S., and Killian, J. A. (2007) How protein transmembrane segments sense the lipid environment. Biochemistry 46, 1457-1465
27. Abrami, L., Kunz, B., Iacovache, I., and van der Goot, F. G. (2008) Palmitoylation and ubiquitination regulate exit of the Wnt signaling protein LRP6 from the endoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 105, 5384-5389 (Pubitemid 351753872)
28. Wu, R. S., Chudasama, N., Zakharov, S. I., Doshi, D., Motoike, H., Liu, G., Yao, Y., Niu, X., Deng, S.-X., Landry, D. W., Karlin, A., and Marx, S. O. (2009) Location of the β4 transmembrane helices in the BK potassium channel. J. Neurosci. 29, 8321-8328
29. Jin, P. (2002) Phosphorylation-dependent functional coupling of hSlo cal-cium- dependent potassium channel and its hβ4 subunit. J. Biol. Chem. 277, 10014-10020
30. Martin, G. E., Hendrickson, L. M., Penta, K. L., Friesen, R. M., Pietrzykowski, A. Z., Tapper, A. R., and Treistman, S. N. (2008) Identification of a BK channel auxiliary protein controlling molecular and behavioral tolerance to alcohol. Proc. Natl. Acad. Sci. U.S.A. 105, 17543-17548
31. King, J. T., Lovell, P. V., Rishniw, M., Kotlikoff, M. I., Zeeman, M. L., and McCobb, D. P. (2006) β2 and β4 subunits of BK channels confer differential sensitivity to acute modulation by steroid hormones. J. Neurophysiol. 95, 2878-2888
32. Burgoyne, J. R., Haeussler, D. J., Kumar, V., Ji, Y., Pimental, D. R., Zee, R. S., Costello, C. E., Lin, C., McComb, M. E., Cohen, R. A., and Bachschmid, M. M. (2012) Oxidation of HRas cysteine thiols by metabolic stress prevents palmitoylation in vivo and contributes to endothelial cell apoptosis. FASEB J. 26, 832-841