Translocation between PI(4,5)P 2 -poor and PI(4,5)P 2 -rich microdomains during store depletion determines STIM1 conformation and Orai1 gating

Nature Communications

Volumn 5, Issue , 2014, Pages

  Maléth, Jozsef ^a,b   Choi, Seok ^a,c   Muallem, Shmuel ^a   Ahuja, Malini ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b UNIVERSITY OF SZEGED   (Hungary)

^c Chosun University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; STROMAL INTERACTION MOLECULE 1; CALCIUM; CALCIUM CHANNEL; ESYT1 PROTEIN, HUMAN; MEMBRANE PROTEIN; ORAI1 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN BINDING; RECOMBINANT PROTEIN; SEPT4 PROTEIN, HUMAN; SEPTIN; STIM1 PROTEIN, HUMAN; SYNAPTOTAGMIN; TMEM66 PROTEIN, HUMAN; TUMOR PROTEIN;

CALCIUM; GENE EXPRESSION; ION EXCHANGE; PROBE; TRANSLOCATION;

ARTICLE; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DEPLETION; ENDOPLASMIC RETICULUM; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; BINDING SITE; CALCIUM SIGNALING; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; METABOLISM; PLASMID; PROTEIN TERTIARY STRUCTURE; TRANSPORT AT THE CELLULAR LEVEL;

BINDING SITES; BIOLOGICAL TRANSPORT; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMANS; ION CHANNEL GATING; MEMBRANE PROTEINS; NEOPLASM PROTEINS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PLASMIDS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEPTINS; SYNAPTOTAGMINS; TRANSFECTION;

EID: 84922704564     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6843     Document Type: Article

References (39)

1. Berridge, M. J., Bootman, M. D. & Roderick, H. L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529 (2003).
2. Berridge, M. J. Calcium signalling remodelling and disease. Biochem. Soc. Trans. 40, 297-309 (2012).
3. Parekh, A. B. & Putney, Jr J. W. Store-operated calcium channels. Physiol. Rev. 85, 757-810 (2005).
4. Lee, K. P. et al. An endoplasmic reticulum/plasma membrane junction: STIM1/Orai1/TRPCs. FEBS Lett. 584, 2022-2027 (2010).
5. Prakriya, M. The molecular physiology of CRAC channels. Immunol. Rev. 231, 88-98 (2009).
6. Liou, J. et al. STIM is a Ca2 sensor essential for Ca2-store-depletiontriggered Ca2 influx. Curr. Biol. 15, 1235-1241 (2005).
7. Muik, M. et al. STIM1 couples to ORAI1 via an intramolecular transition into an extended conformation. EMBO J. 30, 1678-1689 (2011).
8. Korzeniowski, M. K., Manjarres, I. M., Varnai, P. & Balla, T. Activation of STIM1-Orai1 involves an intramolecular switching mechanism. Sci. Signal. 3, ra82 (2010).
9. Yuan, J. P. et al. SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat. Cell Biol. 11, 337-343 (2009).
10. Park, C. Y. et al. STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136, 876-890 (2009).
11. Palty, R., Raveh, A., Kaminsky, I., Meller, R. & Reuveny, E. SARAF inactivates the store operated calcium entry machinery to prevent excess calcium refilling. Cell 149, 425-438 (2012).
12. Jha, A. et al. The STIM1 CTID domain determines access of SARAF to SOAR to regulate Orai1 channel function. J. Cell Biol. 202, 71-79 (2013).
13. Liou, J., Fivaz, M., Inoue, T. & Meyer, T. Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca2 store depletion. Proc. Natl Acad. Sci. USA 104, 9301-9306 (2007).
14. Manford, A. G., Stefan, C. J., Yuan, H. L., Macgurn, J. A. & Emr, S. D. ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev. Cell 23, 1129-1140 (2012).
15. Min, S. W., Chang, W. P. & Sudhof, T. C. E-Syts, a family of membranous Ca2-sensor proteins with multiple C2 domains. Proc. Natl Acad. Sci. USA 104, 3823-3828 (2007).
16. Loewen, C. J., Young, B. P., Tavassoli, S. & Levine, T. P. Inheritance of cortical ER in yeast is required for normal septin organization. J. Cell Biol. 179, 467-483 (2007).
17. Schauder, C. M. et al. Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510, 552-555 (2014).
18. Giordano, F. et al. PI(4,5)P(2)-dependent and Ca(2)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153, 1494-1509 (2013).
19. Chang, C. L. et al. Feedback regulation of receptor-induced Ca2 signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep. 5, 813-825 (2013).
20. Sharma, S. et al. An siRNA screen for NFAT activation identifies septins as coordinators of store-operated Ca2 entry. Nature 499, 238-242 (2013).
21. Korzeniowski, M. K. et al. Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides. J. Biol. Chem. 284, 21027-21035 (2009).
22. Scrimgeour, N., Litjens, T., Ma, L., Barritt, G. J. & Rychkov, G. Y. Properties of Orai1 mediated store-operated current depend on the expression levels of STIM1 and Orai1 proteins. J. Physiol. 587, 2903-2918 (2009).
23. Hoover, P. J. & Lewis, R. S. Stoichiometric requirements for trapping and gating of Ca2 release-activated Ca2 (CRAC) channels by stromal interaction molecule 1 (STIM1). Proc. Natl Acad. Sci. USA 108, 13299-13304 (2011).
24. Muik, M. et al. Dynamic coupling of the putative coiled-coil domain of ORAI1 with STIM1 mediates ORAI1 channel activation. J. Biol. Chem. 283, 8014-8022 (2008).
25. Gao, X. & Zhang, J. Spatiotemporal analysis of differential Akt regulation in plasma membrane microdomains. Mol. Biol. Cell 19, 4366-4373 (2008).
26. Arozarena, I., Calvo, F. & Crespo, P. Ras, an actor on many stages: posttranslational modifications, localization, and site-specified events. Genes Cancer 2, 182-194 (2011).
27. Derler, I. et al. A Ca2( )release-activated Ca2() (CRAC) modulatory domain (CMD) within STIM1 mediates fast Ca2()-dependent inactivation of ORAI1 channels. J. Biol. Chem. 284, 24933-24938 (2009).
28. Lee, K. P. et al. Molecular determinants of fast Ca2-dependent inactivation and gating of the Orai channels. Proc. Natl Acad. Sci. USA 106, 14687-14692 (2009).
29. Mullins, F. M., Park, C. Y., Dolmetsch, R. E. & Lewis, R. S. STIM1 and calmodulin interact with Orai1 to induce Ca2-dependent inactivation of CRAC channels. Proc. Natl Acad. Sci. USA 106, 15495-15500 (2009).
30. Quest, A. F., Leyton, L. & Parraga, M. Caveolins, caveolae, and lipid rafts in cellular transport, signaling, and disease. Biochem. Cell Biol. 82, 129-144 (2004).
31. Mostowy, S. & Cossart, P. Septins: the fourth component of the cytoskeleton. Nat. Rev. Mol. Cell Biol. 13, 183-194 (2012).
32. Balla, T. Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol. Rev. 93, 1019-1137 (2013).
33. McNally, B. A., Somasundaram, A., Jairaman, A., Yamashita, M. & Prakriya, M. The C-and N-terminal STIM1 binding sites on Orai1 are required for both trapping and gating CRAC channels. J. Physiol. 591, 2833-2850 (2013).
34. Seth, M. et al. TRPC1 channels are critical for hypertrophic signaling in the heart. Circ. Res. 105, 1023-1030 (2009).
35. Navarro-Borelly, L. et al. STIM1-Orai1 interactions and Orai1 conformational changes revealed by live-cell FRET microscopy. J. Physiol. 586, 5383-5401 (2008).
36. Wlodarczyk, J. et al. Analysis of FRET signals in the presence of free donors and acceptors. Biophys. J. 94, 986-1000 (2008).
37. Zal, T. & Gascoigne, N. R. Photobleaching-corrected FRET efficiency imaging of live cells. Biophys. J. 86, 3923-3939 (2004).
38. Varnai, P., Thyagarajan, B., Rohacs, T. & Balla, T. Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J. Cell Biol. 175, 377-382 (2006).
39. Toth, D. J. et al. Acute depletion of plasma membrane phosphatidylinositol 4,5-bisphosphate impairs specific steps in endocytosis of the G-protein-coupled receptor. J. Cell Sci. 125, 2185-2197 (2012).