Toward a high-resolution structure of IP3R channel

Cell Calcium

Volumn 56, Issue 3, 2014, Pages 125-132

  Serysheva, Irina I ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

3D structure; Calcium signaling; Electron cryomicroscopy; IP3R; Single particle reconstruction

Indexed keywords

INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; CALCIUM;

BINDING AFFINITY; BINDING SITE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; STRUCTURE ANALYSIS; ANIMAL; CHEMISTRY; HUMAN; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

EUKARYOTA;

ANIMALS; CALCIUM; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; ION CHANNEL GATING; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

EID: 84926182977     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.08.002     Document Type: Review

References (79)

1. Furuichi T., Yoshikawa S., Miyawaki A., Wada K., Maeda N., Mikoshiba K. Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400. Nature 1989, 342:32-38.
2. Mignery G.A., Sudhof T.C., Takei K., De Camilli P. Putative receptor for inositol 1,4,5-trisphosphate similar to ryanodine receptor. Nature 1989, 342:192-195.
3. Bezprozvanny I. Inositol 1,4,5-tripshosphate receptor, calcium signalling and Huntington's disease. Subcell. Biochem. 2007, 45:323-335.
4. Jacobsen A.N., Du X.J., Lambert K.A., Dart A.M., Woodcock E.A. Arrythmogenic action of thrombin during myocardial reperfusion via release of inositol 1,4,5-triphosphate. Circulation 1996, 93:23-26.
5. Marks A.R. Intracellular calcium-release channels: regulators of cell life and death. Am. J. Physiol. 1997, 272:H597-H605.
6. Matsumoto M., Nakagawa T., Innoe T., et al. Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-triphosphate receptor. Nature 1996, 379:168-171.
7. Durham W., Wehrens X., Sood S., Hamilton S.L. Diseases Associated with Altered Ryanodine Activity Calcium Signalling and Disease 2007, 273-321. Springer, New York, NY 10013, USA. E. Carfoli, M. Brini (Eds.).
8. Treves S., Jungbluth H., Muntoni F., Zorzato F. Congenital muscle disorders with cores: the ryanodine receptor calcium channel paradigm. Curr. Opin. Pharmacol. 2008, 8:319-326.
9. Ludtke S.J., Tran T.P., Ngo Q.T., Moiseenkova-Bell V.Y., Chiu W., Serysheva I.I. Flexible architecture of IP3R1 by Cryo-EM. Structure 2011, 19:1192-1199. 10.1016/j.str.2011.05.003.
10. Murray S.C., Flanagan J., Popova O.B., Chiu W., Ludtke S.J., Serysheva I.I. Validation of cryo-EM structure of IP(3)R1 channel. Structure 2013, 21:900-909. 10.1016/j.str.2013.04.016.
11. Cong Y., Ludtke S.J. Single particle analysis at high resolution. Methods Enzymol. 2010, 482:211-235. 10.1016/S0076-6879(10)82009-9.
12. Tusnady G.E., Dosztanyi Z., Simon I. Transmembrane proteins in the Protein Data Bank: identification and classification. Bioinformatics 2004, 20:2964-2972. 10.1093/bioinformatics/bth340.
13. Bosanac I., Alattia J.R., Mal T.K., et al. Structure of the inositol 1,4,5-trisphosphate receptor binding core in complex with its ligand. Nature 2002, 420:696-700.
14. Bosanac I., Yamazaki H., Matsu-Ura T., Michikawa T., Mikoshiba K., Ikura M. Crystal structure of the ligand binding suppressor domain of type 1 inositol 1,4,5-trisphosphate receptor. Mol. Cell 2005, 17:193-203.
15. Lin C.C., Baek K., Lu Z. Apo and InsP-bound crystal structures of the ligand-binding domain of an InsP receptor. Nat. Struct. Mol. Biol. 2011, 18:1172-1174.
16. Seo M.D., Velamakanni S., Ishiyama N., et al. Structural and functional conservation of key domains in InsP3 and ryanodine receptors. Nature 2012, 483:108-112. 10.1038/nature10751.
17. Ehrlich B.E., Watras J. Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum. Nature 1988, 336:583-586. 10.1038/336583a0.
18. Ferris C.D., Huganir R.L., Supattapone S., Snyder S.H. Purified inositol 1,4,5-trisphosphate receptor mediates calcium flux in reconstituted lipid vesicles. Nature 1989, 342:87-89.
19. Iino M. Calcium dependent inositol trisphosphate-induced calcium release in the guinea-pig taenia caeci. Biochem. Biophys. Res. Commun. 1987, 142:47-52.
20. 2+ release channels. Physiol. Rev. 2007, 87:593-658.
21. Fedorenko O.A., Popugaeva E., Enomoto M., et al. Itracellular calcium channels: inositol-1,4,5-trisphosphate receptors. Eur. J. Pharm. 2014, 739:39-48.
22. Mignery G.A., Newton C.L., Archer B.T., Sudhof T.C. Structure and expression of the rat inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 1990, 265:12679-12685.
23. Yoshikawa S., Tanimura T., Miyawaki A., et al. Molecular cloning and characterization of the inositol 1,4,5-trisphosphate receptor in Drosophila melanogaster. J. Biol. Chem. 1992, 267:16613-16619.
24. Supattapone S., Worley P.F., Baraban J.M., Snyder S.H. Solubilization, purification and characteriztion of an inositol triphosphate receptor. J. Biol. Chem. 1988, 263:1530-1534.
25. Maeda N., Niinobe M., Nakahira K., Mikoshiba K. Purification and characterization of P400 protein, a glycoprotein characteristic of Purkinje cell, from mouse cerebellum. J. Neurochem. 1988, 51:1724-1730.
26. Jiang W., Baker M.L., Jakana J., Weigele P.R., King J., Chiu W. Backbone structure of the infectious epsilon15 virus capsid revealed by electron cryomicroscopy. Nature 2008, 451:1130-1134.
27. Zhang X., Settembre E., Xu C., et al. Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:1867-1872.
28. Ludtke S.J., Baker M.L., Chen D.H., Song J.L., Chuang D.T., Chiu W. De novo backbone trace of GroEL from single particle electron cryomicroscopy. Structure 2008, 16:441-448. 10.1016/j.str.2008.02.007.
29. Yu X., Jin L., Zhou Z.H. 3.88Å structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature 2008, 453:415-419.
30. Cong Y., Baker M.L., Jakana J., et al. 4.0-Å resolution cryo-EM structure of the mammalian chaperonin TRiC/CCT reveals its unique subunit arrangement. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4967-4972. 10.1073/pnas.0913774107.
31. Zhang J., Baker M.L., Schroder G.F., et al. Mechanism of folding chamber closure in a group II chaperonin. Nature 2010, 463:379-383. 10.1038/nature08701.
32. Cheng L., Zhu J., Hui W.H., et al. Backbone model of an aquareovirus virion by cryo-electron microscopy and bioinformatics. J. Mol. Biol. 2010, 397:852-863.
33. Liu X., Zhang Q., Murata K., et al. Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat. Struct. Mol. Biol. 2010, 17:830-836.
34. Liu H., Jin L., Koh S.B., et al. Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science 2010, 329:1038-1043.
35. Chen J.Z., Settembre E.C., Aoki S.T., et al. Molecular interactions in rotavirus assembly and uncoating seen by high-resolution cryo-EM. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:10644-10648.
36. Bai X.C., Martin T.G., Scheres S.H., Dietz H. Cryo-EM structure of a 3D DNA-origami object. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:20012-20017. 10.1073/pnas.1215713109.
37. Serysheva I.I., Ludtke S.J. 3D Structure of IP(3) Receptor. Curr. Top. Membr. 2010, 66C:171-189. 10.1016/S1063-5823(10)66008-5.
38. Jiang Q.X., Thrower E.C., Chester D.W., Ehrlich B.E., Sigworth F.J. Three-dimensional structure of the type 1 inositol 1,4,5-trisphosphate receptor at 24Å resolution. EMBO J. 2002, 21:3575-3581.
39. Sato C., Hamada K., Ogura T., et al. Inositol 1,4,5-trisphosphate receptor contains multiple cavities and L-shaped ligand-binding domains. J. Mol. Biol. 2004, 336:155-164.
40. Serysheva I.I., Bare D.J., Ludtke S.J., Kettlun C.S., Chiu W., Mignery G.A. Structure of the type 1 inositol 1,4,5-trisphosphate receptor revealed by electron cryomicroscopy. J. Biol. Chem. 2003, 278:21319-21322.
41. Scheres S.H., Chen S. Prevention of overfitting in cryo-EM structure determination. Nat. Methods 2012, 9:853-854. 10.1038/nmeth.2115.
42. Henderson R., Chen S., Chen J.Z., et al. Tilt-pair analysis of images from a range of different specimens in single-particle electron cryomicroscopy. J. Mol. Biol. 2011, 413:1028-1046. 10.1016/j.jmb.2011.09.008.
43. Choe C.U., Ehrlich B.E. The inositol 1,4,5-trisphosphate receptor (IP3R) and its regulators: sometimes good and sometimes bad teamwork. Sci. STKE 2006, 2006:re15.
44. + conduction and selectivity. Science 1998, 280:69-77.
45. Kuo A., Gulbis J.M., Antcliff J.F., et al. Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 2003, 300:1922-1926.
46. + channel Kir2.2 at 3.1Å resolution. Science 2009, 326:1668-1674.
47. Ludtke S.J., Serysheva I.I., Hamilton S.L., Chiu W. The pore structure of the closed RyR1 channel. Structure (Camb) 2005, 13:1203-1211.
48. Samso M., Wagenknecht T., Allen P.D. Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM. Nat. Struct. Mol. Biol. 2005, 12:539-544.
49. Unwin N. Nicotinic acetylcholine receptor at 9Å resolution. J. Mol. Biol. 1993, 229:1101-1124.
50. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4Å resolution. J. Mol. Biol. 2005, 346:967-989.
51. Taylor C.W., Tovey S.C. IP(3) receptors: toward understanding their activation. Cold Spring Harb. Perspect. Biol. 2010, 2:a004010. 10.1101/cshperspect.a004010.
52. Szlufcik K., Bultynck G., Callewaert G., Missiaen L., Parys J.B., De Smedt H. The suppressor domain of inositol 1,4,5-trisphosphate receptor plays an essential role in the protection against apoptosis. Cell Calcium 2006, 39:325-336. 10.1016/j.ceca.2005.11.007.
53. Uchida K., Miyauchi H., Furuichi T., Michikawa T., Mikoshiba K. Critical regions for activation gating of the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 2003, 278:16551-16560.
54. Yoshikawa F., Iwasaki H., Michikawa T., Furuichi T., Mikoshiba K. Trypsinized cerebellar inositol 1,4,5-trisphosphate receptor. Structural and functional coupling of cleaved ligand binding and channel domains. J. Biol. Chem. 1999, 274:316-327.
55. Chan J., Whitten A.E., Jeffries C.M., et al. Ligand-induced conformational changes via flexible linkers in the amino-terminal region of the inositol 1,4,5-trisphosphate receptor. J. Mol. Biol. 2007, 373:1269-1280.
56. Hamada K., Terauchi A., Mikoshiba K. Three-dimensional rearrangements within inositol 1,4,5-trisphosphate receptor by calcium. J. Biol. Chem. 2003, 278:52881-52889.
57. Baker M.L., Zhang J., Ludtke S.J., Chiu W. Cryo-EM of macromolecular assemblies at near-atomic resolution. Nat. Protoc. 2010, 5:1697-1708. 10.1038/nprot.2010.126.
58. Yamazaki H., Chan J., Ikura M., Michikawa T., Mikoshiba K. Tyr-167/Trp-168 in type 1/3 inositol 1,4,5-trisphosphate receptor mediates functional coupling between ligand binding and channel opening. J. Biol. Chem. 2010, 285:36081-36091.
59. Boehning D., Joseph S.K. Direct association of ligand-binding and pore domains in homo- and heterotetrameric inositol 1,4,5-trisphosphate receptors. EMBO J. 2000, 19:5450-5459.
60. Schug Z.T., Joseph S.K. The role of the S4-S5 linker and C-terminal tail in inositol 1,4,5-trisphosphate receptor function. J. Biol. Chem. 2006, 281:24431-24440.
61. Chan J., Yamazaki H., Ishiyama N., et al. Structural studies of inositol 1,4,5-trisphosphate receptor: coupling ligand binding to channel gating. J. Biol. Chem. 2010, 285:36092-36099.
62. Egelman E.H. Problems in fitting high resolution structures into electron microscopic reconstructions. HFSP J. 2008, 2:324-331. 10.2976/1.2992221.
63. Wang L., Sigworth F.J. Structure of the BK potassium channel in a lipid membrane from electron cryomicroscopy. Nature 2009, 461:292-295.
64. Popot J.L., Althoff T., Bagnard D., et al. Amphipols from A to Z. Annu. Rev. Biophys. 2011, 40:379-408. 10.1146/annurev-biophys-042910-155219.
65. Liao M., Cao E., Julius D., Cheng Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 2013, 504:107-112. 10.1038/nature12822.
66. Bammes B.E., Rochat R.H., Jakana J., Chen D.H., Chiu W. Direct electron detection yields cryo-EM reconstructions at resolutions beyond 3/4 Nyquist frequency. J. Struct. Biol. 2012, 177:589-601. 10.1016/j.jsb.2012.01.008.
67. Campbell M.G., Cheng A., Brilot A.F., et al. Movies of ice-embedded particles enhance resolution in electron cryo-microscopy. Structure 2012, 10.1016/j.str.2012.08.026.
68. Li X., Zheng S.Q., Egami K., Agard D.A., Cheng Y. Influence of electron dose rate on electron counting images recorded with the K2 camera. J. Struct. Biol. 2013, 10.1016/j.jsb.2013.08.005.
69. Li X., Mooney P., Zheng S., et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 2013, 10:584-590. 10.1038/nmeth.2472.
70. Cao E., Liao M., Cheng Y., Julius D. TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 2013, 504:113-118. 10.1038/nature12823.
71. Berridge M.J., Fain J.N. Inhibition of phosphatidylinositol synthesis and the inactivation of calcium entry after prolonged exposure of the blowfly salivary gland to 5-hydroxytryptamine. Biochem. J. 1979, 178:59-69.
72. Berridge M.J. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem. J. 1983, 212:849-858.
73. 2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 1983, 306:67-69.
74. Chadwick C.C., Saito A., Fleischer S. Isolation and characteriztion of the inositol triphosphate receptor from smooth muscle. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:2132-2136.
75. Mignery G.A., Sudhof T.C. The ligand binding site and transduction mechanism in the inositol-1,4,5-triphosphate receptor. EMBO J. 1990, 9:3893-3898.
76. 2+ release analysed using region-specific monoclonal antibodies. Biochem. J. 1991, 277(Pt. 1):125-131.
77. Katayama E., Funahashi H., Michikawa T., et al. Native structure and arrangement of inositol-1,4,5-triphosphate receptor molecules in bovine cerebellar Purkinje cells as studied by quick-freeze deep-etch electron microscopy. EMBO J. 1996, 15:4844-4851.
78. Hamada K., Miyata T., Mayanagi K., Hirota J., Mikoshiba K. Two-state conformational changes in inositol 1,4,5-trisphosphate receptor regulated by calcium. J. Biol. Chem. 2002, 277:21115-21118.
79. da Fonseca P.C., Morris S.A., Nerou E.P., Taylor C.W., Morris E.P. Domain organization of the type 1 inositol 1,4,5-trisphosphate receptor as revealed by single-particle analysis. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:3936-3941.