Two potential calmodulin-binding sequences in the ryanodine receptor contribute to a mobile, intra-subunit calmodulin-binding domain

Journal of Cell Science

Volumn 126, Issue 19, 2013, Pages 4527-4535

  Huang, Xiaojun ^a,b   Liu, Ying ^a   Wang, Ruiwu ^c   Zhong, Xiaowei ^c   Liu, Yingjie ^c   Koop, Andrea ^c   Chen, S R Wayne ^c   Wagenknecht, Terence ^a,b   Liu, Zheng ^a  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

Calmodulin; Cryo EM; FRET; Ryanodine receptor calcium release channel

Indexed keywords

ARGININE; CAFFEINE; CALMODULIN; COMPLEMENTARY DNA; CYAN FLUORESCENT PROTEIN; LYSINE; RECEPTOR SUBUNIT; RYANODINE RECEPTOR 2;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL STRAIN HEK293; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SUBUNIT; SEQUENCE ANALYSIS; SIGNAL DETECTION; THREE DIMENSIONAL IMAGING;

CALMODULIN; CRYO-EM; FRET; RYANODINE RECEPTOR/CALCIUM RELEASE CHANNEL;

ANIMALS; BINDING SITES; CALMODULIN; HUMANS; MICE; PROTEIN BINDING; PROTEIN SUBUNITS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84885439108     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.133454     Document Type: Article

References (46)

1. Ai, X., Curran, J. W., Shannon, T. R., Bers, D. M. and Pogwizd, S. M. (2005). Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ. Res. 97, 1314-1322.
2. Aracena, P., Hidalgo, C. and Hamilton, S. L. (2005). RyR1 modulation by calmodulin. In Ryanodine Receptors: Structure, Function and Dysfunction in Clinical Disease (ed. X. H. T. Wehrens and A. R. Marks), pp. 163-168. New York, NY: Springer.
3. Bähler, M. and Rhoads, A. (2002). Calmodulin signaling via the IQ motif. FEBS Lett. 513, 107-113.
4. Balshaw, D. M., Xu, L., Yamaguchi, N., Pasek, D. A. and Meissner, G. (2001). Calmodulin binding and inhibition of cardiac muscle calcium release channel (ryanodine receptor). J. Biol. Chem. 276, 20144-20153.
5. Buratti, R., Prestipino, G., Menegazzi, P., Treves, S. and Zorzato, F. (1995). Calcium dependent activation of skeletal muscle Ca2+ release channel (ryanodine receptor) by calmodulin. Biochem. Biophys. Res. Commun. 213, 1082-1090.
6. Cannell, M. B. and Kong, C. H. T. (2012). Local control in cardiac E-C coupling. J. Mol. Cell. Cardiol. 52, 298-303.
7. Chen, S. R. and MacLennan, D. H. (1994). Identification of calmodulin-, Ca(2+)-, and ruthenium red-binding domains in the Ca2+ release channel (ryanodine receptor) of rabbit skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 269, 22698-22704.
8. Chen, S. R. W., Li, X., Ebisawa, K. and Zhang, L. (1997). Functional characterization of the recombinant type 3 Ca2+ release channel (ryanodine receptor) expressed in HEK293 cells. J. Biol. Chem. 272, 24234-24246.
9. Damiani, E. and Margreth, A. (2000). Pharmacological clues to calmodulin-mediated activation of skeletal ryanodine receptor using [3H]-ryanodine binding. J. Muscle Res. Cell Motil. 21, 1-8.
10. Girgenrath, T., Mahalingam, M., Svensson, B., Nitu, F. R., Cornea, R. L. and Fessenden, J. D. (2013). N-terminal and central segments of the type 1 ryanodine receptor mediate its interaction with FK506-binding proteins. J. Biol. Chem. 288, 16073-16084.
11. Guerrini, R., Menegazzi, P., Anacardio, R., Marastoni, M., Tomatis, R., Zorzato, F. and Treves, S. (1995). Calmodulin binding sites of the skeletal, cardiac, and brain ryanodine receptor Ca2+ channels: modulation by the catalytic subunit of cAMPdependent protein kinase?. Biochemistry 34, 5120-5129.
12. Huang, X., Fruen, B., Farrington, D. T., Wagenknecht, T. and Liu, Z. (2012). Calmodulin-binding locations on the skeletal and cardiac ryanodine receptors. J. Biol. Chem. 287, 30328-30335.
13. Jones, P. P., Meng, X., Xiao, B., Cai, S., Bolstad, J., Wagenknecht, T., Liu, Z. and Chen, S. R. W. (2008). Localization of PKA phosphorylation site, Ser(2030), in the three-dimensional structure of cardiac ryanodine receptor. Biochem. J. 410, 261-270.
14. Kratz, P. A., Böttcher, B. and Nassal, M. (1999). Native display of complete foreign protein domains on the surface of hepatitis B virus capsids. Proc. Natl. Acad. Sci. USA 96, 1915-1920.
15. Kushnir, A., Mollah, A. K. M. M. and Wehrens, X. H. T. (2005). Evolution of the ryanodine receptor gene family. In Ryanodine Receptors: Structure, Function and Dysfunction in Clinical Disease (ed. X. H. T. Wehrens and A. R. Marks), pp. 1-8. New York, NY: Springer.
16. Li, P. and Chen, S. R. W. (2001). Molecular basis of Ca(2)+ activation of the mouse cardiac Ca(2)+ release channel (ryanodine receptor). J. Gen. Physiol. 118, 33-44.
17. Liu, Z., Zhang, J., Li, P., Chen, S. R. W. and Wagenknecht, T. (2002). Threedimensional reconstruction of the recombinant type 2 ryanodine receptor and localization of its divergent region 1. J. Biol. Chem. 277, 46712-46719.
18. Liu, Z., Wang, R., Tian, X., Zhong, X., Gangopadhyay, J., Cole, R., Ikemoto, N., Chen, S. R. W. and Wagenknecht, T. (2010). Dynamic, inter-subunit interactions between the N-terminal and central mutation regions of cardiac ryanodine receptor. J. Cell Sci. 123, 1775-1784.
19. Menegazzi, P., Larini, F., Treves, S., Guerrini, R., Quadroni, M. and Zorzato, F. (1994). Identification and characterization of three calmodulin binding sites of the skeletal muscle ryanodine receptor. Biochemistry 33, 9078-9084.
20. Meng, X., Xiao, B., Cai, S., Huang, X., Li, F., Bolstad, J., Trujillo, R., Airey, J., Chen, S. R. W., Wagenknecht, T. et al. (2007). Three-dimensional localization of serine 2808, a phosphorylation site in cardiac ryanodine receptor. J. Biol. Chem. 282, 25929-25939.
21. Moore, C. P., Rodney, G., Zhang, J.-Z., Santacruz-Toloza, L., Strasburg, G. and Hamilton, S. L. (1999). Apocalmodulin and Ca2+ calmodulin bind to the same region on the skeletal muscle Ca2+ release channel. Biochemistry 38, 8532-8537.
22. Rodney, G. G., Williams, B. Y., Strasburg, G. M., Beckingham, K. and Hamilton, S. L. (2000). Regulation of RYR1 activity by Ca(2+) and calmodulin. Biochemistry 39, 7807-7812.
23. Rodney, G. G., Moore, C. P., Williams, B. Y., Zhang, J.-Z., Krol, J., Pedersen, S. E. and Hamilton, S. L. (2001). Calcium binding to calmodulin leads to an N-terminal shift in its binding site on the ryanodine Receptor. J. Biol. Chem. 276, 2069-2074.
24. Samsó, M. and Wagenknecht, T. (2002). Apocalmodulin and Ca2+-calmodulin bind to neighboring locations on the ryanodine receptor. J. Biol. Chem. 277, 1349-1353.
25. Samsó, M., Feng, W., Pessah, I. N. and Allen, P. D. (2009). Coordinated movement of cytoplasmic and transmembrane domains of RyR1 upon gating. PLoS Biol. 7, e85.
26. Sharma, M. R., Penczek, P., Grassucci, R., Xin, H.-B., Fleischer, S. and Wagenknecht, T. (1998). Cryoelectron microscopy and image analysis of the cardiac ryanodine receptor. J. Biol. Chem. 273, 18429-18434.
27. Sharma, P., Ishiyama, N., Nair, U., Li, W., Dong, A., Miyake, T., Wilson, A., Ryan, T., MacLennan, D. H., Kislinger, T. et al. (2012). Structural determination of the phosphorylation domain of the ryanodine receptor. FEBS J. 279, 3952-3964.
28. Stern, M. D. and Cheng, H. (2004). Putting out the fire: what terminates calciuminduced calcium release in cardiac muscle?. Cell Calcium 35, 591-601.
29. Takeshima, H., Nishimura, S., Matsumoto, T., Ishida, H., Kangawa, K., Minamino, N., Matsuo, H., Ueda, M., Hanaoka, M., Hirose, T. et al. (1989). Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339, 439-445.
30. Tian, X., Liu, Y., Liu, Y., Wang, R., Wagenknecht, T., Liu, Z. and Chen, S. R. W. (2013). Ligand-dependent conformational changes in the clamp region of the cardiac ryanodine receptor. J. Biol. Chem. 288, 4066-4075.
31. Tripathy, A., Xu, L., Mann, G. and Meissner, G. (1995). Calmodulin activation and inhibition of skeletal muscle Ca2+ release channel (ryanodine receptor). Biophys. J. 69, 106-119.
32. Tung, C. C., Lobo, P. A., Kimlicka, L. and Van Petegem, F. (2010). The aminoterminal disease hotspot of ryanodine receptors forms a cytoplasmic vestibule. Nature 468, 585-588.
33. Wagenknecht, T., Radermacher, M., Grassucci, R., Berkowitz, J., Xin, H.-B. and Fleischer, S. (1997). Locations of calmodulin and FK506-binding protein on the three-dimensional architecture of the skeletal muscle ryanodine receptor. J. Biol. Chem. 272, 32463-32471.
34. Wang, R., Chen, W., Cai, S., Zhang, J., Bolstad, J., Wagenknecht, T., Liu, Z. and Chen, S. R. W. (2007). Localization of an NH(2)-terminal disease-causing mutation hot spot to the "clamp" region in the three-dimensional structure of the cardiac ryanodine receptor. J. Biol. Chem. 282, 17785-17793.
35. Wang, R., Zhong, X., Meng, X., Koop, A., Tian, X., Jones, P. P., Fruen, B. R., Wagenknecht, T., Liu, Z. and Chen, S. R. W. (2011). Localization of the dantrolene-binding sequence near the FK506-binding protein-binding site in the three-dimensional structure of the ryanodine receptor. J. Biol. Chem. 286, 12202- 12212.
36. Xiong, L.-W., Newman, R. A., Rodney, G. G., Thomas, O., Zhang, J.-Z., Persechini, A., Shea, M. A. and Hamilton, S. L. (2002). Lobe-dependent regulation of ryanodine receptor type 1 by calmodulin. J. Biol. Chem. 277, 40862-40870.
37. Xu, L. and Meissner, G. (2004). Mechanism of calmodulin inhibition of cardiac sarcoplasmic reticulum Ca2+ release channel (ryanodine receptor). Biophys. J. 86, 797-804.
38. Yamaguchi, N., Xin, C. and Meissner, G. (2001). Identification of apocalmodulin and Ca2+-calmodulin regulatory domain in skeletal muscle Ca2+ release channel, ryanodine receptor. J. Biol. Chem. 276, 22579-22585.
39. Yamaguchi, N., Xu, L., Pasek, D. A., Evans, K. E. and Meissner, G. (2003). Molecular basis of calmodulin binding to cardiac muscle Ca(2+) release channel (ryanodine receptor). J. Biol. Chem. 278, 23480-23486.
40. Yamaguchi, N., Xu, L., Pasek, D. A., Evans, K. E., Chen, S. R. W. and Meissner, G. (2005). Calmodulin regulation and identification of calmodulin binding region of type-3 ryanodine receptor calcium release channel. Biochemistry 44, 15074-15081.
41. Yuchi, Z., Lau, K. and Van Petegem, F. (2012). Disease mutations in the ryanodine receptor central region: crystal structures of a phosphorylation hot spot domain. Structure 20, 1201-1211.
42. Zhang, H., Zhang, J.-Z., Danila, C. I. and Hamilton, S. L. (2003a). A noncontiguous, intersubunit binding site for calmodulin on the skeletal muscle Ca2+ release channel. J. Biol. Chem. 278, 8348-8355.
43. Zhang, J., Liu, Z., Masumiya, H., Wang, R., Jiang, D., Li, F., Wagenknecht, T. and Chen, S. R. W. (2003b). Three-dimensional localization of divergent region 3 of the ryanodine receptor to the clamp-shaped structures adjacent to the FKBP binding sites. J. Biol. Chem. 278, 14211-14218.
44. Zhao, M., Li, P., Li, X., Zhang, L., Winkfein, R. J. and Chen, S. R. W. (1999). Molecular identification of the ryanodine receptor pore-forming segment. J. Biol. Chem. 274, 25971-25974.
45. Zhu, X., Ghanta, J., Walker, J. W., Allen, P. D. and Valdivia, H. H. (2004). The calmodulin binding region of the skeletal ryanodine receptor acts as a self-modulatory domain. Cell Calcium 35, 165-177.
46. Zhu, L., Zhong, X., Chen, S. R. W., Banavali, N. and Liu, Z. (2013). Modeling a ryanodine receptor N-terminal domain connecting the central vestibule and the corner clamp region. J. Biol. Chem. 288, 903-914.