STIM1 couples to ORAI1 via an intramolecular transition into an extended conformation

EMBO Journal

Volumn 30, Issue 9, 2011, Pages 1678-1689

  Muik, Martin ^a   Fahrner, Marc ^a   Schindl, Rainer ^a   Stathopulos, Peter ^b   Frischauf, Irene ^a   Derler, Isabella ^a   Plenk, Peter ^a   Lackner, Barbara ^a   Groschner, Klaus ^c   Ikura, Mitsuhiko ^b   Romanin, Christoph ^a  

^a JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF GRAZ   (Austria)

Author keywords

FRET sensor; intramolecular transition; ORAI1; STIM1

Indexed keywords

CALCIUM; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; MUTANT PROTEIN; STROMAL INTERACTION MOLECULE 1;

ARTICLE; CALCIUM CURRENT; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CYTOSOL; ENDOPLASMIC RETICULUM; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; HYDROPHOBICITY; MUTATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SENSOR; T LYMPHOCYTE ACTIVATION;

BLOTTING, WESTERN; CALCIUM CHANNELS; CALCIUM SIGNALING; CHROMATOGRAPHY, GEL; CLONING, MOLECULAR; ELECTROPHYSIOLOGY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MUTAGENESIS, SITE-DIRECTED; NEOPLASM PROTEINS; PROTEIN CONFORMATION; TRANSFECTION;

EID: 79955628984     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.79     Document Type: Article

References (60)

1. Baba Y, Hayashi K, Fujii Y, Mizushima A, Watarai H, Wakamori M, Numaga T, Mori Y, Iino M, Hikida M, Kurosaki T (2006) Coupling of STIM1 to store-operated Ca2+ entry through its constitutive and inducible movement in the endoplasmic reticulum. Proc Natl Acad Sci USA 103: 16704-16709 (Pubitemid 44737317)
2. Barr VA, Bernot KM, Srikanth S, Gwack Y, Balagopalan L, Regan CK, Helman DJ, Sommers CL, Oh-Hora M, Rao A, Samelson LE (2008) Dynamic movement of the calcium sensor STIM1 and the calcium channel Orai1 in activated T-cells: Puncta and Distal caps. Mol Biol Cell 19: 2802-2817
3. Berney C, Danuser G (2003) FRET or no FRET: a quantitative comparison. Biophys J 84: 3992-4010 (Pubitemid 36637892)
4. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529 (Pubitemid 36773404)
5. Calloway NT, Holowka DA, Baird BA (2010) A basic sequence in STIM1 promotes Ca2+ influx by interacting with the C-terminal acidic coiled-coil of Orai1. Biochemistry 49: 1067-1071
6. Covington ED, Wu MM, Lewis RS (2010) Essential role for the CRAC activation domain in store-dependent oligomerization of STIM1. Mol Biol Cell 21: 1897-1907
7. DeHaven WI, Smyth JT, Boyles RR, Bird GS, Putney Jr JW (2008) Complex actions of 2-aminoethyldiphenyl borate on store-operated calcium entry. J Biol Chem 283: 19265-19273
8. Derler I, Fahrner M, Carugo O, Muik M, Bergsmann J, Schindl R, Frischauf I, Eshaghi S, Romanin C (2009) Increased hydro-phobicity at the N terminus/membrane interface impairs gating of the severe combined immunodeficiency-related ORAI1 mutant. J Biol Chem 284: 15903-15915
9. Derler I, Hofbauer M, Kahr H, Fritsch R, Muik M, Kepplinger K, Hack ME, Moritz S, Schindl R, Groschner K, Romanin C (2006) Dynamic but not constitutive association of calmodulin with rat TRPV6 channels enables fine tuning of Ca2+-dependent inacti-vation. J Physiol 577: 31-44 (Pubitemid 44698238)
10. Feske S (2007) Calcium signalling in lymphocyte activation and disease. Nat Rev Immunol 7: 690-702 (Pubitemid 47327393)
11. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441: 179-185
12. Finn BE, Evenas J, Drakenberg T, Waltho JP, Thulin E, Forsen S (1995) Calcium-induced structural changes and domain autonomy in calmodulin. Nat Struct Biol 2: 777-783
13. Frischauf I, Muik M, Derler I, Bergsmann J, Fahrner M, Schindl R, Groschner K, Romanin C (2009) Molecular determinants of the coupling between STIM1 and Orai channels: differential activation of Orai1-3 channels by a STIM1 coiled-coil mutant. J Biol Chem 284: 21696-21706
14. Grigoryan G, Keating AE (2008) Structural specificity in coiled-coil interactions. Curr Opin Struct Biol 18: 477-483
15. Gruber M, Soding J, Lupas AN (2006) Comparative analysis of coiled-coil prediction methods. J Struct Biol 155: 140-145 (Pubitemid 44278640)
16. Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28: 491-533
17. Hong JH, Li Q, Kim MS, Shin DM, Feske S, Birnbaumer L, Cheng KT, Ambudkar IS, Muallem S (2011) Polarized but differential localization and recruitment of STIM1, Orai1 and TRPC channels in secretory cells. Traffic 12: 232-245
18. Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355: 353-356
19. Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S, Worley PF (2006) STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat Cell Biol 8: 1003-1010 (Pubitemid 44314732)
20. Korzeniowski MK, Manjarres IM, Varnai P, Balla T (2010) Activation of STIM1-Orai1 involves an intramolecular switching mechanism. Sci Signal 3: ra82
21. Liou J, Fivaz M, Inoue T, Meyer T (2007) 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 (Pubitemid 47185774)
22. Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell Jr JE, Meyer T (2005) STIM is a Ca2+ sensor essential for Ca2+-store-deple-tion-triggered Ca2+ influx. Curr Biol 15: 1235-1241 (Pubitemid 40950523)
23. Lis A, Peinelt C, Beck A, Parvez S, Monteilh-Zoller M, Fleig A, Penner R (2007) CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties. Curr Biol 17: 794-800 (Pubitemid 46635119)
24. Luik RM, Wang B, Prakriya M, Wu MM, Lewis RS (2008) Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454: 538-542
25. Luik RM, Wu MM, Buchanan J, Lewis RS (2006) The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J Cell Biol 174: 815-825 (Pubitemid 44373731)
26. Martin SR, Bayley PM (1986) The effects of Ca2+ and Cd2+ on the secondary and tertiary structure of bovine testis calmodulin. A circular-dichroism study. Biochem J 238: 485-490 (Pubitemid 16008520)
27. Mercer JC, Dehaven WI, Smyth JT, Wedel B, Boyles RR, Bird GS, Putney Jr JW (2006) Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracel-lular calcium sensor, Stim1. J Biol Chem 281: 24979-24990 (Pubitemid 44274268)
28. Muik M, Fahrner M, Derler I, Schindl R, Bergsmann J, Frischauf I, Groschner K, Romanin C (2009) A cytosolic homomerization and a modulatory domain within STIM1 C terminus determine coupling to ORAI1 channels. J Biol Chem 284: 8421-8426
29. Muik M, Frischauf I, Derler I, Fahrner M, Bergsmann J, Eder P, Schindl R, Hesch C, Polzinger B, Fritsch R, Kahr H, Madl J, Gruber H, Groschner K, Romanin C (2008) Dynamic coupling of the putative coiled-coil domain of ORAI1 with STIM1 mediates ORAI1 channel activation. J Biol Chem 283: 8014-8022
30. Navarro-Borelly L, Somasundaram A, Yamashita M, Ren D, Miller RJ, Prakriya M (2008) STIM1-Orai1 interactions and Orai1 conformational changes revealed by live-cell FRET microscopy. J Physiol 586: 5383-5401
31. Oh-hora M, Rao A (2008) Calcium signaling in lymphocytes. Curr Opin Immunol 20: 250-258
32. Parekh AB, Putney Jr JW (2005) Store-operated calcium channels. Physiol Rev 85: 757-810 (Pubitemid 40404641)
33. Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S, Walz T, Garcia KC, Dolmetsch RE, Lewis RS (2009) STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136: 876-890
34. Park CY, Shcheglovitov A, Dolmetsch R (2010) The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science 330: 101-105
35. Parry DA, Fraser RD, Squire JM (2008) Fifty years of coiled-coils and alpha-helical bundles: a close relationship between sequence and structure. J Struct Biol 163: 258-269
36. Peinelt C, Lis A, Beck A, Fleig A, Penner R (2008) 2-Amino-ethoxydiphenyl borate directly facilitates and indirectly inhibits STIM1-dependent gating of CRAC channels. J Physiol 586: 3061-3073 (Pubitemid 351984690)
37. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443: 230-233 (Pubitemid 44387613)
38. Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Velicelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169: 435-445 (Pubitemid 40686694)
39. Schindl R, Bergsmann J, Frischauf I, Derler I, Fahrner M, Muik M, Fritsch R, Groschner K, Romanin C (2008) 2-aminoethoxy-diphenyl borate alters selectivity of Orai3 channels by increasing their pore size. J Biol Chem 283: 20261-20267
40. Singh A, Hamedinger D, Hoda JC, Gebhart M, Koschak A, Romanin C, Striessnig J (2006) C-terminal modulator controls Ca2+-de-pendent gating of Ca(v)1.4 L-type Ca2+ channels. Nat Neurosci 9: 1108-1116 (Pubitemid 44306303)
41. Smyth JT, Dehaven WI, Jones BF, Mercer JC, Trebak M, Vazquez G, Putney Jr JW (2006) Emerging perspectives in store-operated Ca2+ entry: roles of Orai, Stim and TRP. Biochim Biophys Acta 1763: 1147-1160 (Pubitemid 44794538)
42. Soboloff J, Spassova MA, Hewavitharana T, He LP, Xu W, Johnstone LS, Dziadek MA, Gill DL (2006) STIM2 is an inhibitor of STIM1-mediated store-operated Ca(2+) entry. Curr Biol 16: 1465-1470 (Pubitemid 44088459)
43. Srikanth S, Jung HJ, Kim KD, Souda P, Whitelegge J, Gwack Y (2010) A novel EF-hand protein, CRACR2A, is a cytosolic Ca2+ sensor that stabilizes CRAC channels in T cells. Nat Cell Biol 12: 436-446
44. Stathopulos PB, Zheng L, Ikura M (2009) Stromal interaction molecule (STIM) 1 and STIM2 calcium sensing regions exhibit distinct unfolding and oligomerization kinetics. J Biol Chem 284: 728-732
45. Stathopulos PB, Zheng L, Li GY, Plevin MJ, Ikura M (2008) Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry. Cell 135: 110-122
46. Steinmetz MO, Jelesarov I, Matousek WM, Honnappa S, Jahnke W, Missimer JH, Frank S, Alexandrescu AT, Kammerer RA (2007) Molecular basis of coiled-coil formation. Proc Natl Acad Sci USA 104: 7062-7067 (Pubitemid 47186009)
47. Tamarina NA, Kuznetsov A, Philipson LH (2008) Reversible translocation of EYFP-tagged STIM1 is coupled to calcium influx in insulin secreting beta-cells. Cell Calcium 44: 533-544
48. Vig M, Beck A, Billingsley JM, Lis A, Parvez S, Peinelt C, Koomoa DL, Soboloff J, Gill DL, Fleig A, Kinet JP, Penner R (2006a) CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr Biol 16: 2073-2079 (Pubitemid 44573821)
49. Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP (2006b) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312: 1220-1223 (Pubitemid 43801149)
50. Wang Y, Deng X, Gill DL (2010) Calcium signaling by STIM and Orai: intimate coupling details revealed. Sci Signal 3: pe42
51. Wang Y, Deng X, Zhou Y, Hendron E, Mancarella S, Ritchie MF, Tang XD, Baba Y, Kurosaki T, Mori Y, Soboloff J, Gill DL (2009) STIM protein coupling in the activation of Orai channels. Proc Natl Acad Sci USA 106: 7391-7396
52. Woolfson DN (2005) The design of coiled-coil structures and assemblies. Adv Protein Chem 70: 79-112 (Pubitemid 40544781)
53. Wu MM, Buchanan J, Luik RM, Lewis RS (2006) Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol 174: 803-813 (Pubitemid 44373730)
54. Xia Z, Liu Y (2001) Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes. Biophys J 81: 2395-2402 (Pubitemid 32917186)
55. Xu P, Lu J, Li Z, Yu X, Chen L, Xu T (2006) Aggregation of STIM1 underneath the plasma membrane induces clustering of Orai1. Biochem Biophys Res Commun 350: 969-976 (Pubitemid 44584187)
56. Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O, Cahalan MD (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443: 226-229 (Pubitemid 44387612)
57. Yuan JP, Zeng W, Dorwart MR, Choi YJ, Worley PF, Muallem S (2009) SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol 11: 337-343
58. Zhang SL, Kozak JA, Jiang W, Yeromin AV, Chen J, Yu Y, Penna A, Shen W, Chi V, Cahalan MD (2008) Store-dependent and -independent modes regulating Ca2+ release-activated Ca2+ channel activity of human Orai1 and Orai3. J Biol Chem 283: 17662-17671
59. Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, Cahalan MD (2006) Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc Natl Acad Sci USA 103: 9357-9362 (Pubitemid 43902581)
60. Zhang SL, Yu Y Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437: 902-905 (Pubitemid 41486767)