CaBP1, a neuronal Ca2+ sensor protein, inhibits inositol trisphosphate receptors by clamping intersubunit interactions

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 21, 2013, Pages 8507-8512

  Li, Congmin ^a   Enomoto, Masahiro ^b   Rossi, Ana M ^c   Seo, Min Duk ^b,d   Rahman, Taufiq ^c   Stathopulos, Peter B ^b   Taylor, Colin W ^c   Ikura, Mitsuhiko ^b   Ames, James B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d Ajou University   (South Korea)

Author keywords

EF hand; Intracellular Ca2+ channel; Ion channel; Ryanodine receptor

Indexed keywords

CALCIUM BINDING PROTEIN 1; INOSITOL TRISPHOSPHATE; NEURONAL CALCIUM SENSOR; RYANODINE RECEPTOR; UNCLASSIFIED DRUG; CA2+ BINDING PROTEIN 1; CA2+-BINDING PROTEIN-1; CALCIUM BINDING PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; ION CHANNEL; NERVE PROTEIN;

ARTICLE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; HETERONUCLEAR SINGLE QUANTUM COHERENCE; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DOCKING; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; SITE DIRECTED MUTAGENESIS; STOICHIOMETRY; ANIMAL; CELL LINE; CHEMICAL PHENOMENA; CHEMISTRY; EF HAND; GENETICS; INTRACELLULAR CA2+ CHANNEL; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PHYSIOLOGY; PROTEIN BINDING; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; RAT;

EF HAND; INTRACELLULAR CA2+ CHANNEL; ION CHANNEL; RYANODINE RECEPTOR;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL LINE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; ION CHANNEL GATING; MOLECULAR DOCKING SIMULATION; NERVE TISSUE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS;

MLCS; MLOWN;

EID: 84878133688     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220847110     Document Type: Article

References (47)

1. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: Dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4(7): 517-529.
2. Haynes LP, McCue HV, Burgoyne RD (2012) Evolution and functional diversity of the Calcium Binding Proteins (CaBPs). Front Mol Neurosci 5:e9.
3. Barbara JG (2002) IP3-dependent calcium-induced calcium release mediates bidirectional calcium waves in neurones: Functional implications for synaptic plasticity. Biochim Biophys Acta 1600(1-2): 12-18.
4. 2+ channels - a growing community. Mol Cell Endocrinol 353(1-2): 21-28.
5. 2+ release channels. Physiol Rev 87(2): 593-658.
6. Taylor CW, Tovey SC (2010) IP3 receptors: Toward understanding their activation. Cold Spring Harb Perspect Biol 2(12):a004010.
7. 2+ signals. Semin Cell Dev Biol 23(2): 172-180.
8. 2+ signaling. EMBO J 20(7): 1674-1680.
9. 2+. Cell Calcium 32(5-6): 321-334.
10. 2+ release mediated by type-1, -2 and -3 inositol trisphosphate receptors. Biochem J 345(Pt 2): 357-363.
11. Michikawa T, et al. (1999) Calmodulin mediates calcium-dependent inactivation of the cerebellar type 1 inositol 1,4,5-trisphosphate receptor. Neuron 23(4): 799-808.
12. 2+ mobilization. Proc Natl Acad Sci USA 94(21): 11627-11632.
13. 2+ release channel. J Biol Chem 281(30): 20825-20833.
14. Schlecker C, et al. (2006) Neuronal calcium sensor-1 enhancement of InsP3 receptor activity is inhibited by therapeutic levels of lithium. J Clin Invest 116(6): 1668-1674.
15. 2+ release channels. Proc Natl Acad Sci USA 99(11): 7711-7716.
16. 2+-binding proteins. EMBO J 23(2): 312-321.
17. 2+- binding protein (CABP) subfamily with similarity to calmodulin. J Biol Chem 275(2): 1247-1260.
18. 2+-dependent regulation of inositol 1,4,5- trisphosphate receptors by CaBP1. J Biol Chem 284(4): 2472-2481.
19. Findeisen F, Minor DL, Jr. (2010) Structural basis for the differential effects of CaBP1 and calmodulin on CaV1.2 calcium-dependent inactivation. Structure 18(12): 1617-1631.
20. Haynes LP, Tepikin AV, Burgoyne RD (2004) Calcium-binding protein 1 is an inhibitor of agonist-evoked, inositol 1,4,5-trisphosphate-mediated calcium signaling. J Biol Chem 279(1): 547-555.
21. Menger N, Seidenbecher CI, Gundelfinger ED, Kreutz MR (1999) The cytoskeletonassociated neuronal calcium-binding protein caldendrin is expressed in a subset of amacrine, bipolar and ganglion cells of the rat retina. Cell Tissue Res 298(1): 21-32.
22. Seidenbecher CI, Reissner C, Kreutz MR (2002) Caldendrins in the inner retina. Adv Exp Med Biol 514: 451-463.
23. 2+-binding protein 1. Nat Neurosci 5(3): 210-217.
24. 2+-binding protein-1. J Biol Chem 280(33): 29612-29619.
25. 2+-binding protein 1 in Xenopus oocytes. Pflugers Arch 450(5): 345-354.
26. Bosanac I, et al. (2002) Structure of the inositol 1,4,5-trisphosphate receptor binding core in complex with its ligand. Nature 420(6916): 696-700.
27. Bosanac I, et al. (2005) Crystal structure of the ligand binding suppressor domain of type 1 inositol 1,4,5-trisphosphate receptor. Mol Cell 17(2): 193-203.
28. Rossi AM, et al. (2009) Synthetic partial agonists reveal key steps in IP3 receptor activation. Nat Chem Biol 5(9): 631-639.
29. Seo MD, et al. (2012) Structural and functional conservation of key domains in InsP3 and ryanodine receptors. Nature 483(7387): 108-112.
30. Rahman T, Taylor CW (2010) Nuclear patch-clamp recording from inositol 1,4,5- trisphosphate receptors. Methods Cell Biol 99: 199-224.
31. Clore GM, Tang C, Iwahara J (2007) Elucidating transient macromolecular interactions using paramagnetic relaxation enhancement. Curr Opin Struct Biol 17(5): 603-616.
32. Dominguez C, Boelens R, Bonvin AM (2003) HADDOCK: A protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125(7): 1731-1737.
33. Ikura M (1996) Calcium binding and conformational response in EF-hand proteins. Trends Biochem Sci 21(1): 14-17.
34. Ludtke SJ, et al. (2011) Flexible architecture of IP3R1 by cryo-EM. Structure 19(8): 1192-1199.
35. Tung CC, Lobo PA, Kimlicka L, Van Petegem F (2010) The amino-terminal disease hotspot of ryanodine receptors forms a cytoplasmic vestibule. Nature 468(7323): 585-588.
36. Zhang M, Tanaka T, Ikura M (1995) Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat Struct Biol 2(9): 758-767.
37. Gagné SM, Tsuda S, Li MX, Smillie LB, Sykes BD (1995) Structures of the troponin C regulatory domains in the apo and calcium-saturated states. Nat Struct Biol 2(9): 784-789.
38. Yamazaki H, Chan J, Ikura M, Michikawa T, Mikoshiba K (2010) 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 285(46): 36081-36091.
39. Amador FJ, et al. (2009) Crystal structure of type I ryanodine receptor amino-terminal beta-trefoil domain reveals a disease-associated mutation "hot spot" loop. Proc Natl Acad Sci USA 106(27): 11040-11044.
40. 2+ binding to CaBP1, a neuron-specific regulator of calcium channels. J Biol Chem 280(45): 37461-37470.
41. Chan J, et al. (2007) Ligand-induced conformational changes via flexible linkers in the amino-terminal region of the inositol 1,4,5-trisphosphate receptor. J Mol Biol 373(5): 1269-1280.
42. Tugarinov V, Kay LE (2004) An isotope labeling strategy for methyl TROSY spectroscopy. J Biomol NMR 28(2): 165-172.
43. Tugarinov V, Sprangers R, Kay LE (2004) Line narrowing in methyl-TROSY using zeroquantum 1H-13C NMR spectroscopy. J Am Chem Soc 126(15): 4921-4925.
44. de Vries SJ, van Dijk M, Bonvin AM (2010) The HADDOCK web server for data-driven biomolecular docking. Nat Protoc 5(5): 883-897.
45. Battiste JL, Wagner G (2000) Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data. Biochemistry 39(18): 5355-5365.
46. 2+ channels. Nat Protoc 1(1): 259-263.
47. 2+. Nature 458(7238): 655-659.