Crystal structure of calmodulin binding domain of Orai1 in complex with Ca2+ ·calmodulin displays a unique binding mode

Journal of Biological Chemistry

Volumn 287, Issue 51, 2012, Pages 43030-43041

  Liu, Yanshun ^a   Zheng, Xunhai ^a   Mueller, Geoffrey A ^a   Sobhany, Mack ^a   DeRose, Eugene F ^a   Zhang, Yingpei ^a   London, Robert E ^a   Birnbaumer, Lutz ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC LEVELS; BINDING MODES; CALCIUM INFLUX; CALMODULIN BINDING DOMAIN; CYTOSOLS; EXTRACELLULAR ENVIRONMENTS; GEL-FILTRATION CHROMATOGRAPHY; HYDROPHOBIC INTERACTIONS; HYDROPHOBIC POCKETS; ISOTHERMAL TITRATION CALORIMETRY; NMR DATA; PLASMA MEMBRANE PROTEIN; PROTEIN COMPLEXES; PULLDOWN ASSAYS; TARGET BINDING; TWO-STEP MECHANISMS;

BINDING ENERGY; CALCIUM; CAMS; CELL MEMBRANES; GEL PERMEATION CHROMATOGRAPHY; HYDROPHOBICITY;

CALMODULIN;

CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; CALMODULIN; CALMODULIN BINDING PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; GEL PERMEATION CHROMATOGRAPHY; HYDROPHOBICITY; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TARGETING;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CALCIUM CHANNELS; CALMODULIN; CALORIMETRY; CHROMATOGRAPHY, GEL; CRYSTALLOGRAPHY, X-RAY; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; SOLUTIONS;

EID: 84871118027     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.380964     Document Type: Article

References (39)

1. Takemura, H., and Putney, J. W., Jr. (1989) Capacitative calcium entry in parotid acinar cells. Biochem. J. 258, 409-412 (Pubitemid 19075512)
2. Feske, S., Gwack, Y., Prakriya, M., Srikanth, S., Puppel, S. H., Tanasa, B., Hogan, P. G., Lewis, R. S., Daly, M., and Rao, A. (2006)Amutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441, 179-185
3. Roos, J., DiGregorio, P. J., Yeromin, A. V., Ohlsen, K., Lioudyno, M., Zhang, S., Safrina, O., Kozak, J. A., Wagner, S. L., Cahalan, M. D., Veliçelebi, G., and Stauderman, K. A. (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J. Cell Biol. 169, 435-445 (Pubitemid 40686694)
4. Vig, M., Peinelt, C., Beck, A., Koomoa, D. L., Rabah, D., Koblan-Huberson, M., Kraft, S., Turner, H., Fleig, A., Penner, R., and Kinet, J. P. (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312, 1220-1223 (Pubitemid 43801149)
5. Yeromin, A. V., Zhang, S. L., Jiang, W., Yu, Y., Safrina, O., and Cahalan, M. D. (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443, 226-229 (Pubitemid 44387612)
6. 2+ channel activity. Proc. Natl. Acad. Sci. U.S.A. 103, 9357-9362
7. 2+ store to the plasma membrane. Nature 437, 902-905
8. Liou, J., Fivaz, M., Inoue, T., and 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. U.S.A. 104, 9301-9306 (Pubitemid 47185774)
9. Luik, R. M., Wang, B., Prakriya, M., Wu, M. M., and Lewis, R. S. (2008) Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454, 538-542
10. Wu, M. M., Luik, R. M., and Lewis, R. S. (2007) Some assembly required: constructing the elementary units of store-operated Ca2+ entry. Cell Calcium 42, 163-172 (Pubitemid 47029602)
11. Park, C. Y., Hoover, P. J., Mullins, F. M., Bachhawat, P., Covington, E. D., Raunser, S., Walz, T., Garcia, K. C., Dolmetsch, R. E., and Lewis, R. S. (2009) STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136, 876-890
12. Yuan, J. P., Zeng, W., Dorwart, M. R., Choi, Y. J., Worley, P. F., and Muallem, S. (2009) SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat. Cell Biol. 11, 337-343
13. 2+-dependent inactivation of CRAC channels. Proc. Natl. Acad. Sci. U.S.A. 106, 15495-15500
14. 2+-dependent way. Biochemistry 23, 400-403
15. Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C. B., and Bax, A. (1995) Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 2, 768-776
16. Zhang, M., Tanaka, T., and Ikura, M. (1995) Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat. Struct. Biol. 2, 758-767
17. 2+/calmodulin. Nature 410, 1120-1124
18. Yap, K. L., Yuan, T., Mal, T. K., Vogel, H. J., and Ikura, M. (2003) Structural basis for simultaneous binding of two carboxyl-terminal peptides of plant glutamate decarboxylase to calmodulin. J. Mol. Biol. 328, 193-204 (Pubitemid 36390291)
19. Hayashi, N., Matsubara, M., Takasaki, A., Titani, K., and Taniguchi, H. (1998) An expression system of rat calmodulin using T7 phage promoter in Escherichia coli. Protein Expr. Purif. 12, 25-28 (Pubitemid 28361965)
20. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
21. 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., McCoy, 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
22. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
23. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (Pubitemid 47321791)
24. Press, W. H., Flannery, B. P., Teukolsky, S. A., and Vetterling, W. T. (1989) Numerical recipes in FORTRAN. The art of scientific computing. Cambridge University Press, Cambridge, UK
25. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe. A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
26. Johnson, B. A., and Blevins, R. A. (1994)NMRVIEW. A computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614
27. 13C HMQC-NOESY experiment for extracting intermolecular NOE contacts in molecular complexes. FEBS Lett. 350, 87-90
28. Babu, Y. S., Bugg, C. E., and Cook, W. J. (1988) Structure of calmodulin refined at 2.2-Å resolution. J. Mol. Biol. 204, 191-204 (Pubitemid 19011741)
29. Ataman, Z. A., Gakhar, L., Sorensen, B. R., Hell, J. W., and Shea, M. A. (2007) The NMDA receptor NR1 C1 region bound to calmodulin. Structural insights into functional differences between homologous domains. Structure 15, 1603-1617 (Pubitemid 350213408)
30. Hoeflich, K. P., and Ikura, M. (2002) Calmodulin in action. Diversity in target recognition and activation mechanisms. Cell 108, 739-742 (Pubitemid 34327526)
31. V1.5. J. Mol. Biol. 406, 106-119
32. V1.2 voltage-dependent sodium channel. Structure 19, 733-747
33. Putkey, J. A., Kleerekoper, Q., Gaertner, T. R., and Waxham, M. N. (2003) A new role for IQ motif proteins in regulating calmodulin function. J. Biol. Chem. 278, 49667-49670 (Pubitemid 37548796)
34. Putkey, J. A., Waxham, M. N., Gaertner, T. R., Brewer, K. J., Goldsmith, M., Kubota, Y., and Kleerekoper, Q. K. (2008) Acidic/IQ motif regulator of calmodulin. J. Biol. Chem. 283, 1401-1410
35. Wang, X., Kleerekoper, Q. K., Xiong, L. W., and Putkey, J. A. (2010) Intrinsically disordered PEP-19 confers unique dynamic properties to apo and calcium calmodulin. Biochemistry 49, 10287-10297
36. 2+ pump. Biochemistry 38, 12320-12332
37. Ikura, M., Clore, G. M., Gronenborn, A. M., Zhu, G., Klee, C. B., and Bax, A. (1992) Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256, 632-638
38. 2+ pump anchored by a novel 18-1 motif. J. Biol. Chem. 285, 4015-4024
39. Penna, A., Demuro, A., Yeromin, A. V., Zhang, S. L., Safrina, O., Parker, I., and Cahalan, M. D. (2008) The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers. Nature 456, 116-120