Phosphatidylinositol 4,5-biphosphate (PIP2) modulates interaction of syntaxin-1A with sulfonylurea receptor 1 to regulate pancreatic β-cell ATP-sensitive potassium channels

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 6028-6040

  Liang, Tao ^a   Xie, Li ^a   Chao, Christin ^a   Kang, Youhou ^a   Lin, Xianguang ^a   Qin, Tairan ^a   Xie, Huanli ^a   Feng, Zhong Ping ^a   Gaisano, Herbert Y ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CLUSTER FORMATIONS; COMPLEX MODULATION; DOSE-DEPENDENT; ELECTROPHYSIOLOGICAL STUDIES; FORSTER RESONANCE ENERGY TRANSFER; PHOSPHATIDYLINOSITOL 4; POTASSIUM CHANNELS; SULFONYLUREA RECEPTORS;

CELL MEMBRANES; CHEMICAL ACTIVATION; ELECTROPHYSIOLOGY; ENERGY TRANSFER; PHOSPHOLIPIDS; POTASSIUM;

CYTOLOGY;

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; PHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BIPHOSPHATE; SULFONYLUREA RECEPTOR 1; SYNAPTOJANIN; SYNAPTOJANIN 1; SYNTAXIN 1A; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL ACTIVATION; COMPLEX FORMATION; CONTROLLED STUDY; ENERGY TRANSFER; ENZYME REGULATION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; PANCREAS ISLET BETA CELL; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION;

ATP-SENSITIVE POTASSIUM CHANNEL; INSULIN SECRETION; KIR6.2; PHOSPHOLIPID; PIP2; PLASMA MEMBRANE; POTASSIUM CHANNELS; SNARE PROTEINS; SUR1; SYNTAXIN-1A;

ANIMALS; CELL LINE, TUMOR; HEK293 CELLS; HUMANS; INSULIN-SECRETING CELLS; MALE; MUTATION; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, WISTAR; SULFONYLUREA RECEPTORS; SYNTAXIN 1;

EID: 84896852216     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.511808     Document Type: Article

References (39)

1. Aittoniemi, J., Fotinou, C., Craig, T. J., de Wet H., Proks, P., and Ashcroft, F. M. (2009) Review. SUR1. A unique ATP-binding cassette protein that functions as an ion channel regulator. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 257-267
2. Aguilar-Bryan, L., and Bryan, J. (1999) Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocr. Rev. 20, 101-135 (Pubitemid 29339588)
3. Nichols, C. G., Shyng, S. L., Nestorowicz, A., Glaser, B., Clement, J. P., 4th, Gonzalez, G., Aguilar-Bryan, L., Permutt, M. A., and Bryan, J. (1996) Adenosine diphosphate as an intracellular regulator of insulin secretion. Science 272, 1785-1787 (Pubitemid 26256397)
4. Hou, J. C., Min, L., and Pessin, J. E. (2009) Insulin granule biogenesis, trafficking and exocytosis. Vitamins and hormones. Vitam. Horm. 80, 473-506
5. Ashcroft, F. M., and Gribble, F. M. (1999) Differential sensitivity of betacell and extrapancreatic K(ATP) channels to gliclazide. Diabetologia 42, 903-919
6. Rohács, T., Lopes, C. M., Jin, T., Ramdya, P. P., Molnár, Z., and Logothetis, D. E. (2003) Specificity of activation by phosphoinositides determines lipid regulation of Kir channels. Proc. Natl. Acad. Sci. U.S.A. 100, 745-750 (Pubitemid 36126123)
7. Kwiatkowska, K. (2010) One lipid, multiple functions. How various pools of PI(4,5)P(2) are created in the plasma membrane. Cell Mol. Life Sci. 67, 3927-3946
8. Cremona, O., and De Camilli, P. (2001) Phosphoinositides in membrane traffic at the synapse. J. Cell Sci. 114, 1041-1052 (Pubitemid 32288519)
9. Hilgemann, D. W., Feng, S., and Nasuhoglu, C. (2001) The complex and intriguing lives of PIP2 with ion channels and transporters. Sci. STKE 2001, re19
10. 3. Complex roles at the cell surface. Cell 100, 603-606
11. Martin, T. F. (2001) PI(4,5)P(2) regulation of surface membrane traffic. Curr. Opin. Cell Biol. 13, 493-499
12. Haider, S., Tarasov, A. I., Craig, T. J., Sansom, M. S., and Ashcroft, F. M. (2007) Identification of the PIP2-binding site on Kir6.2 by molecular modelling and functional analysis. EMBO J. 26, 3749-3759 (Pubitemid 47295876)
13. Fan, Z., and Makielski, J. C. (1997) Anionic phospholipids activate ATPsensitive potassium channels. J. Biol. Chem. 272, 5388-5395 (Pubitemid 27102355)
14. Baukrowitz, T., Schulte, U., Oliver, D., Herlitze, S., Krauter, T., Tucker, S. J., Ruppersberg, J. P., and Fakler, B. (1998) PIP2 and PIP as determinants for ATP inhibition of KATP channels. Science 282, 1141-1144 (Pubitemid 28516246)
15. Enkvetchakul, D., Loussouarn, G., Makhina, E., Shyng, S. L., and Nichols, C. G. (2000) The kinetic and physical basis of K(ATP) channel gating. Toward a unified molecular understanding. Biophys. J. 78, 2334-2348 (Pubitemid 30313793)
16. Pratt, E. B., Tewson, P., Bruederle, C. E., Skach, W. R., Shyng, S. L. (2011) N-terminal transmembrane domain of SUR1 controls gating of Kir6.2 by modulating channel sensitivity to PIP2. J. Gen. Physiol. 137, 299-314
17. Stansfeld, P. J., Hopkinson, R., Ashcroft, F. M., and Sansom, M. S. (2009) PIP(2)-binding site in Kir channels. Definition by multiscale biomolecular simulations. Biochemistry 48, 10926-10933
18. Lin, C. W., Yan, F., Shimamura, S., Barg, S., and Shyng, S. L. (2005) Membrane phosphoinositides control insulin secretion through their effects on ATP-sensitive K+ channel activity. Diabetes 54, 2852-2858 (Pubitemid 41401079)
19. Olsen, H. L., Hoy, M., Zhang, W., Bertorello, A. M., Bokvist, K., Capito, K., Efanov, A. M., Meister, B., Thams, P., Yang, S. N., Rorsman, P., Berggren, P. O., and Gromada, J. (2003) Phosphatidylinositol 4-kinase serves as a metabolic sensor and regulates priming of secretory granules in pancreatic beta cells. Proc. Natl. Acad. Sci. U.S.A. 100, 5187-5192 (Pubitemid 36542680)
20. 2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nat. Struct. Mol. Biol. 11, 36-44
21. Murray, D. H., and Tamm, L. K. (2011) Molecular mechanism of cholesterol-and polyphosphoinositide-mediated syntaxin clustering. Biochemistry 50, 9014-9022
22. Murray, D. H., and Tamm, L. K. (2009) Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol. Biochemistry 48, 4617-4625
23. 2+-dependent manner. In vitro characteristics and possible significance. J. Biol. Chem. 273, 10240-10248
24. Chen, Y. A., and Scheller, R. H. (2001) SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell Biol. 2, 98-106 (Pubitemid 33674038)
25. + channels. Tuning beta-cell excitability with syntaxin-1A and other exocytotic proteins. Endocr. Rev. 28, 653-663
26. Kang, Y. H., Leung, Y.-M., Manning-Fox, J., Xia, F., Xie, H., Sheu, L., Tsushima, R. G., Light, P., and Gaisano, H. Y. (2004) Syntaxin-1A inhibits cardiac KATP channels by its actions on nucleotide binding folds 1 and 2 of sulfonylurea receptor 2A. J. Biol. Chem. 279, 47125-47131 (Pubitemid 39518369)
27. Cui, N., Kang, Y., He, Y., Leung, Y. M., Xie, H., Pasyk, E. A., Gao, X., Sheu, L., Hansen, J. B., Wahl, P., Tsushima, R. G., and Gaisano, H. Y. (2004)H3domain of syntaxin 1A inhibits KATP channels by its actions on the sulfonylurea receptor 1 nucleotide-binding folds-1 and -2. J. Biol. Chem. 279, 53259-53265 (Pubitemid 40051829)
28. Chang, N., Liang, T., Lin, X., Kang, Y., Xie, H., Feng, Z. P., and Gaisano, H. Y. (2011) Syntaxin-1A interacts with distinct domains within nucleotide-binding folds of sulfonylurea receptor 1 to inhibit β-cell ATP-sensitive potassium channels. J. Biol. Chem. 286, 23308-23318
29. Lam, A. D., Tryoen-Toth, P., Tsai, B., Vitale, N., and Stuenkel, E. L. (2008) SNARE-catalyzed fusion events are regulated by Syntaxin1A-lipid interactions. Mol. Biol. Cell 19, 485-497 (Pubitemid 351272138)
30. Milosevic, I., Sørensen, J. B., Lang, T., Krauss, M., Nagy, G., Haucke, V., Jahn, R., and Neher, E. (2005) Plasmalemmal phosphatidylinositol-4, 5-bisphosphate level regulates the releasable vesicle poolsize in chromaffin cells. J. Neurosci. 25, 2557-2565 (Pubitemid 40365167)
31. van den Bogaart, G., Meyenberg, K., Risselada, H. J., Amin, H., Willig, K. I., Hubrich, B. E., Dier, M., Hell, S. W., Grubmüller, H., Diederichsen, U., and Jahn, R. (2011) Membrane protein sequestering by ionic protein-lipid interactions. Nature 479, 552-555
32. Leung, Y. M., Kang, Y., Gao, X., Xia, F., Xie, H., Sheu, L., Tsuk, S., Lotan, I., Tsushima, R. G., and Gaisano, H. Y. (2003) Syntaxin 1A binds to the cytoplasmic C terminus of Kv2.1 to regulate channel gating and trafficking. J. Biol. Chem. 278, 17532-17538 (Pubitemid 36799641)
33. Chao, C., Liang, T., Kang, Y., Lin, X., Xie, H., Feng, Z. P., and Gaisano, H. Y. (2011) Syntaxin-1A inhibits KATP channels by interacting with specific conserved motifs within sulfonylurea receptor 2A. J. Mol. Cell Cardiol. 51, 790-802
34. Pasyk, E. A., Kang, Y., Huang, X., Cui, N., Sheu, L., and Gaisano, H. Y. (2004) Syntaxin-1A binds the nucleotide-binding folds of sulphonylurea receptor 1 to regulate the KATP channel. J. Biol. Chem. 279, 4234-4240 (Pubitemid 38199010)
35. Lin, Y. W., Jia, T., Weinsoft, A. M., and Shyng, S. L. (2003) Stabilization of the activity of ATP-sensitive potassium channels by ion pairs formed between adjacent Kir6.2 subunits. J. Gen. Physiol. 122, 225-237 (Pubitemid 37064686)
36. Shyng, S. L., and Nichols, C. G. (1998) Membrane phospholipid control of nucleotide sensitivity of KATP channels. Science 282, 1138-1141
37. James, D. J., Khodthong, C., Kowalchyk, J. A., and Martin, T. F. (2008) Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. J. Cell Biol. 182, 355-366
38. McLaughlin, S., Wang, J., Gambhir, A., and Murray, D. (2002) PIP(2) and proteins. Interactions, organization, and information flow. Annu. Rev. Biophys. Biomol. Struct. 31, 151-175
39. Ostenson, C. G., Gaisano, H., Sheu, L., Tibell, A., and Bartfai, T. (2006) Impaired gene and protein expression of exocytotic soluble N-ethylmaleimide attachment protein receptor complex proteins in pancreatic islets of type 2 diabetic patients. Diabetes 55, 435-440 (Pubitemid 43343274)