Modular architecture of Munc13/calmodulin complexes: Dual regulation by Ca 2 and possible function in short-term synaptic plasticity

EMBO Journal

Volumn 29, Issue 3, 2010, Pages 680-691

  Rodríguez Castãeda, Fernando ^a,d   Maestre Martínez, Mitcheell ^a   Coudevylle, Nicolas ^a,e   Dimova, Kalina ^b   Junge, Harald ^b,f   Lipstein, Noa ^b   Lee, Donghan ^a   Becker, Stefan ^a   Brose, Nils ^b,c   Jahn, Olaf ^b,c   Carlomagno, Teresa ^a,g   Griesinger, Christian ^a,c  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^c Deutsche Forschungsgemeinschaft   (Germany)

^d UNIVERSITY OF YORK   (United Kingdom)

^e MFPL   (Austria)

^f GENENTECH INC   (United States)

^g EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Calcium; Calmodulin; Munc13; Neurotransmitter release; Short term plasticity

Indexed keywords

CALCIUM ION; CALMODULIN; CALMODULIN BINDING PROTEIN; EGTAZIC ACID; MEMBRANE PROTEIN; MUNC13 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NERVE CELL; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CALMODULIN; HUMANS; MAMMALS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP; SYNAPSES; TIME FACTORS;

EID: 76349121068     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.373     Document Type: Article

References (65)

1. Augustin I, Rosenmund C, Südhof TC, Brose N (1999) Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400: 457-461
2. Basu J, Shen N, Dulubova I, Lu J, Guan R, Guryev O, Grishin NV, Rosenmund C, Rizo J (2005) A minimal domain responsible for Munc13 activity. Nat Struct Mol Biol 12: 1017-1018
3. Bax A, Grishaev A (2005) Weak alignment NMR: a hawk-eyed view of biomolecular structure. Curr Opin Struct Biol 15: 563-570
4. Bayley PM, Findlay WA, Martin SR (1996) Target recognition by calmodulin: dissecting the kinetics and affinity of interaction using short peptide sequences. Protein Sci 5: 1215-1228
5. Bertini I, Del Bianco C, Gelis I, Katsaros N, Luchinat C, Parigi G, Peana M, Provenzali A, Zoroddu MA (2004) Experimentally exploring the conformational space sampled by domain reorientation in calmodulin. Proc Natl Acad Sci USA 101: 6841-6846
6. Bertini I, Gelis I, Katsaros N, Luchinat C, Provenzali A (2003) Tuning the affinity for lanthanides of calcium binding proteins. Biochemistry 42: 8011-8021
7. Betz A, Asheri U, Rickmann M, Augustin I, Neher E, Sudhof TC, Rettig J, Brose N (1998) Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 21: 123-126
8. Betz A, Okamoto M, Brose N (1997) Direct interaction of the rat unc-13 homologue Munc13-1 with the N-terminus of syntaxin. J Biol Chem 272: 2520-2526
9. 2+-calmodu-lin binding interactions of the microtubule-associated protein F-STOP. Biochemistry 42: 11484-11493
10. Brose N, Rosenmund C (2002) Move over protein kinase C, you've got company: alternative cellular effectors of diacylglycerol and phorbol esters. J Cell Sci 115: 4399-4411
11. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289-302
12. Craik DJ, Wilce JA (1997) Studies of protein-ligand interactions by NMR. Methods Mol Biol 60: 195-232
13. Crivici A, Ikura M (1995) Molecular and structural basis of target recognition by calmodulin. Annu Rev Biophys Biomol Struct 24: 85-116
14. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) Nmrpipe: a multidimensional spectral processing system based on Unix pipes. J Biomol NMR 6: 277-293
15. 2+ selectivity in the calmodulin regulation of CaV channels. Nature 451: 830-834
16. Dimova K, Kalkhof S, Pottratz I, Ihling C, Rodriguez-Castaneda F, Liepold T, Griesinger C, Brose N, Sinz A, Jahn O (2009) Structural insights into the Calmodulin-Munc13 interaction obtained by cross-linking and mass spectrometry. Biochemistry 48: 5908-5921
17. Dimova K, Kawabe H, Betz A, Brose N, Jahn O (2006) Characterization of the Munc13-calmodulin interaction by photo-affinity labeling. Biochim Biophys Acta 1763: 1256-1265
18. Drum CL, Yan S-Z, Bard J, Shen Y-Q, Lu D, Soelaiman S, Grabarek Z, Bohm A, Tang W-J (2002) Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415: 396-402
19. 2+ target recognition activates the Bcl-2 regulator FKBP38. J Biol Chem 282: 36496-36504
20. 2+ pump. Biochemistry 38: 12320-12332
21. Goddard TD, Kneller DG (1999) SPARKY 3. San Francisco: University of California
22. Guan R, Dai H, Rizo J (2008) Binding of the Munc13-1 MUN domain to membrane-anchored SNARE complexes. Biochemistry 47: 1474-1481
23. Guerini D, Krebs J, Carafoli E (1984) Stimulation of the purified erythrocyte Ca2+-ATPase by tryptic fragments of calmodulin. J Biol Chem 259: 15172-15177
24. Güntert P (2003) Automated NMR protein structure calculation. Prog Nucl Magn Reson Spectrosc 44: 33-96
25. Haberz P, Rodŕiguez-Castañeda F, Junker J, Becker S, Leonov A, Griesinger C (2006) Two new chiral EDTA-based metal chelates for weak alignment of proteins in solution. Org Lett 8: 1275-1278
26. Herrmann T, Güntert P, Wüthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319: 209-227
27. Herrmann T, Güntert P, Wüthrich K (2002b) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J Biomol NMR 24: 171-189 (Pubitemid 36113646)
28. Hoeflich KP, Ikura M (2002) Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108: 739-742
29. Hosoi N, Sakaba T, Neher E (2007) Quantitative analysis of calcium-dependent vesicle recruitment and its functional role at the calyx of Held synapse. J Neurosci 27: 14286-14298
30. Ikura M (1996) Calcium binding and conformational response in EF-hand proteins. Trends Biochem Sci 21: 14-17
31. Jahn O, Eckart K, Brauns O, Tezval H, Spiess J (2002) The binding protein of corticotropin-releasing factor: ligand-binding site and subunit structure. Proc Natl Acad Sci USA 99: 12055-12060
32. Jahn R, Scheller RH (2006) SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7: 631-643
33. 2+ sensor/effector complex that controls short-term synaptic plasticity. Cell 118: 389-401
34. Jurado LA, Chockalingam PS, Jarrett HW (1999) Apocalmodulin. Physiol Rev 79: 661-682
35. Kuboniwa H, Tjandra N, Grzesiek S, Ren H, Klee CB, Bax A (1995) Solution structure of calcium-free calmodulin. Nat Struct Biol 2: 768-776
36. Larsson G, Schleucher J, Onions J, Hermann S, Grundström T, Wijmenga SS (2001) A novel target recognition revealed by calmodulin in complex with the basic helix-loop-helix transcription factor SEF2-1/E2-2. Protein Sci 10: 169-186
37. Laskowski RA, Rullmann JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486
38. Lee D, Walsh JD, Yu P, Markus MA, Choli-Papadopoulou T, Schwieters CD, Krueger S, Draper DE, Wang Y-X (2007) The structure of free L11 and functional dynamic of L11 in free, L11-rRNA(58nt) binary and L11-rRNA(58nt)-thiostrepton ternary complexes. J Mol Biol 367: 1007-1022
39. Leite JF, Dougherty DA, Lester HA, Shahgholi M (2003) Investigation of apparent mass deviations in electrospray ioniza-tion tandem mass spectrometry of a benzophenone-labeled peptide. Rapid Commun Mass Spectrom 17: 1677-1684
40. Mirzoeva S, Weigand S, Lukas TJ, Shuvalova L, Anderson WF, Watterson DM (1999) Analysis of the functional coupling between calmodulin's calcium binding and peptide recognition properties. Biochemistry 38: 3936-3947
41. Neher E (2006) A comparison between exocytic control mechanisms in adrenal chromaffin cells and a glutamatergic synapse. Pflugers Arch 453: 261-268
42. Neher E, Sakaba T (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59: 861-872
43. Osawa M, Swindella MB, Tanikawa J, Tanaka T, Mase T, Furuya T, Ikura M (1998) Solution structure of calmodulin-w-7 complex: the basis of diversity in molecular recognition. J Mol Biol 276: 165-176
44. Ottiger M, Delaglio F, Bax A (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J Magn Res 131: 373-378
45. 2+ binding and implications for kinase activation. Protein Sci 6: 794-807
46. Rettig J, Neher E (2002) Emerging roles of presynaptic proteins in Ca++-triggered exocytosis. Science 298: 781-785
47. Rhee J-S, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Südhof TC, Takahashi M, Rosenmund C, Brose N (2002) b Phorbol ester-and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108: 121-133
48. Rhoads AR, Friedberg F (1997) Sequence motifs for calmodulin recognition. FASEB J 11: 331-340
49. Richmond JE, Weimer RM, Jorgensen EM (2001) An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming. Nature 412: 338-341
50. Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, Rhee JS (2002) Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33: 411-424
51. Sakaba T, Neher E (2001) Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32: 1119-1131
52. 2+/calmodulin. Nature 410: 1120-1124
53. Schweitzer E (1987) Coordinated release of ATP and ACh from cholinergic synaptosomes and its inhibition by calmodulin antagonists. J Neurosci 7: 2948-2956
54. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160: 65-73
55. 2+/calmodulin-dependent protein kinase II (CaKII) is activated by calmodulin with two bound calciums. Proc Natl Acad Sci USA 103: 13968-13973
56. Silinsky EM, Searl TJ (2003) Phorbol esters and neurotransmitter release: more than just protein kinase C? Br J Pharmacol 138: 1191-1201
57. Stevens DR, Wu Z-X, Matti U, Junge HJ, Schirra C, Becherer U, Wojcik SM, Brose N, Rettig J (2005) Identification of the minimal protein domain required for priming activity of Munc13-1. Curr Biol 15: 2243-2248
58. Südhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547
59. Varoqueaux F, Sigler A, Rhee J-S, Brose N, Enk C, Reim K, Rosenmund C (2002) Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc Natl Acad Sci USA 99: 9037-9042
60. Vetter SW, Leclerc E (2003) Novel aspects of calmodulin target recognition and activation. Eur J Biochem 270: 404-414
61. Wojcik SM, Brose N (2007) Regulation of membrane fusion in synaptic excitation-secretion coupling: speed and accuracy matter. Neuron 55: 11-24
62. Xia Z, Storm DR (2005) The role of calmodulin as a signal integrator for synaptic plasticity. Nat Rev Neurosci 6: 267-276
63. Zhang M, Tanaka T, Ikura M (1995) Calcium-induced conforma-tional transition revealed by the solution structure of apo-Calmodulin. Nat Struct Biol 2: 758-767
64. Zikich D, Mezer A, Varoqueaux F, Sheinin A, Junge HJ, Nachliel E, Melamed R, Brose N, Gutman M, Ashery U (2008) Vesicle priming and recruitment by ubMunc13-2 are differentially regulated by calcium and calmodulin. J Neurosci 28: 1949-1960
65. Zweckstetter M, Bax A (2000) Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR. J Am Chem Soc 122: 3791-3792