DOC2A and DOC2B are sensors for neuronal activity with unique calcium-dependent and kinetic properties

Journal of Neurochemistry

Volumn 97, Issue 3, 2006, Pages 818-833

  Groffen, Alexander J A ^a,c   Friedrich, Reut ^b   Brian, Elisabeth C ^a   Ashery, Uri ^b   Verhage, Matthijs ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b TEL AVIV UNIVERSITY   (Israel)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Ca2+ regulated exocytosis; DOC2; Munc13; Priming; Short term plasticity; Synaptotagmin

Indexed keywords

ASPARTIC ACID DERIVATIVE; CALCIUM; DOUBLE C 2A PROTEIN; DOUBLE C 2B PROTEIN; DYE; PROTEIN; STYRYL DYE; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DEPOLARIZATION; EMBRYO; FLUORESCENCE; HIPPOCAMPUS; HUMAN; HUMAN CELL; KINETICS; MUTATION; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; SENSOR; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; CALCIMYCIN; CALCIUM; CALCIUM-BINDING PROTEINS; CATS; CELL MEMBRANE; CELLS, CULTURED; CHELATING AGENTS; CHROMAFFIN CELLS; CRICETINAE; DIAGNOSTIC IMAGING; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; EGTAZIC ACID; ELECTRIC STIMULATION; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HUMANS; IONOPHORES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTAGENESIS; NERVE TISSUE PROTEINS; NEURONS; POTASSIUM CHLORIDE; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; RATS; SEQUENCE ALIGNMENT; TIME FACTORS; TRANSFECTION;

ANIMALIA;

EID: 33645861074     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03755.x     Document Type: Article

References (67)

1. Ales E. Fuentealba J. Garcia A. G. Lopez M. G. 2005 Depolarization evokes different patterns of calcium signals and exocytosis in bovine and mouse chromaffin cells: the role of mitochondria. Eur J. Neurosci. 21 142 150.
2. Aravamudan B. Fergestad T. Davis W. S. Rodesch C. K. Broadie K. 1999 Drosophila UNC-13 is essential for synaptic transmission. Nat. Neurosci. 2 965 971.
3. Ashery U. Betz A. Xu T. Brose N. Rettig J. 1999 An efficient method for infection of adrenal chromaffin cells using the Semliki Forest virus gene expression system. Eur J. Cell Biol. 78 525 532.
4. Ashery U. Varoqueaux F. Voets T. Betz A. Thakur P. Koch H. Neher E. Brose N. Rettig J. 2000 Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. EMBO J. 19 3586 3596.
5. Augustin I. Rosenmund C. Sudhof T. C. Brose N. 1999 Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400 457 461.
6. Bittner M. A. Holz R. W. 1992 Kinetic analysis of secretion from permeabilized adrenal chromaffin cells reveals distinct components. J. Biol. Chem. 267 16 219 16 225.
7. 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.
8. Campbell R. E. Tour O. Palmer A. E. Steinbach P. A. Baird G. S. Zacharias D. A. Tsien R. Y. 2002 A monomeric red fluorescent protein. Proc. Natl Acad. Sci. USA 99 7877 7882.
9. Chen J. Anderson J. B. DeWeese-Scott C. et al. q29 2003 MMDB: Entrez's 3D-structure database. Nucl Acids Res. 31 474 477.
10. Chung S. H. Takai Y. Holz R. W. 1995 Evidence that the Rab3a-binding protein, rabphilin3a, enhances regulated secretion. Studies in adrenal chromaffin cells. J. Biol. Chem. 270 16 714 16 718.
11. Chung S. H. Song W. J. Kim K. Bednarski J. J. Chen J. Prestwich G. D. Holz R. W. 1998 The C2 domains of Rabphilin3A specifically bind phosphatidylinositol 4,5-bisphosphate containing vesicles in a Ca2+-dependent manner. In vitro characteristics and possible significance. J. Biol. Chem. 273 10 240 10 248.
12. Duncan R. R. Betz A. Shipston M. J. Brose N. Chow R. H. 1999 Transient, phorbol ester-induced DOC2-Munc13 interactions in vivo. J. Biol. Chem. 274 27 347 27 350.
13. Fernández-Alfonso T. Ryan T. A. 2004 The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41 943 953.
14. Fernandez-Chacon R. Konigstorfer A. Gerber S. H. et al. q30 2001 Synaptotagmin I functions as a calcium regulator of release probability. Nature 410 41 49.
15. Fernandez-Chacon R. Shin O. H. Konigstorfer A. et al. q31 2002 Structure/function analysis of Ca2+ binding to the C2A domain of synaptotagmin 1. J. Neurosci. 22 8438 8446.
16. Fukuda M. Mikoshiba K. 2000 Doc2gamma, a third isoform of double C2 protein, lacking calcium-dependent phospholipid binding activity. Biochem. Biophys. Res. Commun. 276 626 632.
17. Fukuda M. Saegusa C. Kanno E. Mikoshiba K. 2001 The C2A domain of double C2 protein gamma contains a functional nuclear localization signal. J. Biol. Chem. 276 24 441 24 444.
18. Groffen A. J. Brian E. C. Dudok J. J. Kampmeijer J. Toonen R. F. Verhage M. 2004 Ca (2+)-induced recruitment of the secretory vesicle protein DOC2B to the target membrane. J. Biol. Chem. 279 23 740 23 747.
19. Grynkiewicz G. Poenie M. Tsien R. Y. 1985 A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260 3440 3450.
20. Habets R. L. Borst J. G. 2005 Post-tetanic potentiation in the rat calyx of Held synapse. J. Physiol. 564 173 187.
21. Hori T. Takai Y. Takahashi T. 1999 Presynaptic mechanism for phorbol ester-induced synaptic potentiation. J. Neurosci. 19 7262 7267.
22. Hui E. Bai J. Wang P. Sugimori M. Llinas R. R. Chapman E. R. 2005 Three distinct kinetic groupings of the synaptotagmin family: candidate sensors for rapid and delayed exocytosis. Proc. Natl Acad. Sci. USA 102 5210 5214.
23. Jahn R. Lang T. Sudhof T. C. 2003 Membrane fusion. Cell 112 519 533.
24. Joberty G. Stabila P. F. Coppola T. Macara I. G. Regazzi R. 1999 High affinity Rab3 binding is dispensable for Rabphilin-dependent potentiation of stimulated secretion. J. Cell Sci. 112 3579 3587.
25. Kojima T. Fukuda M. Aruga J. Mikoshiba K. 1996 Calcium-dependent phospholipid binding to the C2A domain of a ubiquitous form of double C2 protein (Doc2 beta). J. Biochem. (Tokyo) 120 671 676.
26. Korogod N. Lou X. Schneggenburger R. 2005 Presynaptic Ca2+ requirements and developmental regulation of posttetanic potentiation at the calyx of Held. J. Neurosci. 25 5127 5137.
27. Lindau M. 2003 Synaptotagmin function illuminated. J. General Physiol. 122 251 253.
28. Lou X. Scheuss V. Schneggenburger R. 2005 Allosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion. Nature 435 497 501.
29. Marchler-Bauer A. Anderson J. B. Cherukuri P. F. et al. q32 2005 CDD: a Conserved Domain Database for protein classification. Nucl. Acids Res. 33 D192 D196.
30. Martin T. F. 2002 Prime movers of synaptic vesicle exocytosis. Neuron 34 9 12.
31. Meinrenken C. J. Borst J. G. Sakmann B. 2003 Local routes revisited: the space and time dependence of the Ca2+ signal for phasic transmitter release at the rat calyx of Held. J. Physiol. 547 665 689.
32. Mochida S. Orita S. Sakaguchi G. Sasaki T. Takai Y. 1998 Role of the Doc2 alpha-Munc13-1 interaction in the neurotransmitter release process. Proc. Natl Acad. Sci. USA 95 11 418 11 422.
33. Naito A. Orita S. Wanaka A. Sasaki T. Sakaguchi G. Maeda M. Igarashi H. Tohyama M. Takai Y. 1997 Molecular cloning of mouse Doc2alpha and distribution of its mRNA in adult mouse brain. Brain Res. Mol. Brain Res. 44 198 204.
34. Orita S. Sasaki T. Komuro R. Sakaguchi G. Maeda M. Igarashi H. Takai Y. 1996 Doc2 enhances Ca2+-dependent exocytosis from PC12 cells. J. Biol. Chem. 271 7257 7260.
35. Orita S. Naito A. Sakaguchi G. Maeda M. Igarashi H. Sasaki T. Takai Y. 1997 Physical and functional interactions of Doc2 and Munc13 in Ca2+-dependent exocytotic machinery. J. Biol. Chem. 272 16 081 16 084.
36. Orita S. Sasaki T. Takai Y. 2001 Doc2 alpha as modulator of Ca (2+)-dependent exocytosis. Meth. Enzymol. 329 83 90.
37. Rhee J. S. Betz A. Pyott S. et al. q36 2002 Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108 121 133.
38. Richmond J. E. Davis W. S. Jorgensen E. M. 1999 UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat. Neurosci. 2 959 964.
39. Rizo J. Sudhof T. C. 1998 C2-domains, structure and function of a universal Ca2+-binding domain. J. Biol. Chem. 273 15 879 15 882.
40. von Ruden L. Neher E. 1993 A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. Science 262 1061 1065.
41. Ryan T. A. Smith S. J. 1995 Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14 983 989.
42. Sakaguchi G. Manabe T. Kobayashi K. et al. q37 1999 Doc2alpha is an activity-dependent modulator of excitatory synaptic transmission. Eur. J. Neurosci. 11 4262 4268.
43. Shao X. Davletov B. A. Sutton R. B. Sudhof T. C. Rizo J. 1996 Bipartite Ca2+-binding motif in C2 domains of synaptotagmin and protein kinase C. Science 273 248 251.
44. Shao X. Li C. Fernandez I. Zhang X. Sudhof T. C. Rizo J. 1997 Synaptotagmin-syntaxin interaction: the C2 domain as a Ca2+-dependent electrostatic switch. Neuron 18 133 142.
45. Shao X. Fernandez I. Sudhof T. C. Rizo J. 1998 Solution structures of the Ca2+-free and Ca2+-bound C2A domain of synaptotagmin I: does Ca2+ induce a conformational change? Biochemistry 37 16 106 16 115.
46. Smith C. Moser T. Xu T. Neher E. 1998 Cytosolic Ca2+ acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells. Neuron 20 1243 1253.
47. Stevens C. F. Sullivan J. M. 2003 The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39 299 308.
48. Stevens C. F. Wesseling J. F. 1999 Augmentation is a potentiation of the exocytotic process. Neuron 22 139 146.
49. Stojilkovic S. S. 2005 Ca2+-regulated exocytosis and SNARE function. Trends Endocrinol. Metab. 16 81 83.
50. Sudhof T. C. 2004 The synaptic vesicle cycle. Annu. Rev. Neurosci. 27 509 547.
51. Sutton R. B. Davletov B. A. Berghuis A. M. Sudhof T. C. Sprang S. R. 1995 Structure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold. Cell 80 929 938.
52. Sutton R. B. Ernst J. A. Brunger A. T. 1999 Crystal structure of the cytosolic C2A-C2B domains of synaptotagmin III. Implications for Ca (+2) -independent snare complex interaction. J. Cell Biol. 147 589 598.
53. Sutton R. B. Sprang S. R. 1998 Structure of the protein kinase Cbeta phospholipid-binding C2 domain complexed with Ca2+. Structure 6 1395 1405.
54. Thompson J. D. Higgins D. G. Gibson T. J. 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22 4673 4680.
55. Ubach J. Zhang X. Shao X. Sudhof T. C. Rizo J. 1998 Ca2+ binding to synaptotagmin: how many Ca2+ ions bind to the tip of a C2-domain? EMBO J. 17 3921 3930.
56. Ubach J. Garcia J. Nittler M. P. Sudhof T. C. Rizo J. 1999 Structure of the Janus-faced C2B domain of rabphilin. Nat. Cell Biol. 1 106 112.
57. 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.
58. Verdaguer N. Corbalan-Garcia S. Ochoa W. F. Fita I. Gomez-Fernandez J. C. 1999 Ca (2+) bridges the C2 membrane-binding domain of protein kinase Calpha directly to phosphatidylserine. EMBO J. 18 6329 6338.
59. Verhage M. de Vries K. J. Roshol H. Burbach J. P. Gispen W. H. Sudhof T. C. 1997 DOC2 proteins in rat brain: complementary distribution and proposed function as vesicular adapter proteins in early stages of secretion. Neuron 18 453 461.
60. Villalobos C. Nunez L. Montero M. Garcia A. G. Alonso M. T. Chamero P. Alvarez J. Garcia-Sancho J. 2002 Redistribution of Ca2+ among cytosol and organella during stimulation of bovine chromaffin cells. FASEB J. 16 343 353.
61. Voets T. Moser T. Lund P. E. Chow R. H. Geppert M. Sudhof T. C. Neher E. 2001 Intracellular calcium dependence of large dense-core vesicle exocytosis in the absence of synaptotagmin I. Proc. Natl Acad. Sci. USA 98 11 680 11 685.
62. Wang L. Y. Kaczmarek L. K. 1998 High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394 384 388.
63. Wang P. Wang C. T. Bai J. Jackson M. B. Chapman E. R. 2003 Mutations in the effector binding loops in the C2A and C2B domains of synaptotagmin I disrupt exocytosis in a nonadditive manner. J. Biol. Chem. 278 47 030 47 037.
64. Yizhar O. Matti U. Melamed R. Hagalili Y. Bruns D. Rettig J. Ashery U. 2004 Tomosyn inhibits priming of large dense-core vesicles in a calcium-dependent manner. Proc. Natl Acad. Sci. USA 101 2578 2583.
65. Zhang X. Rizo J. Sudhof T. C. 1998 Mechanism of phospholipid binding by the C2A-domain of synaptotagmin I. Biochemistry 37 12 395 12 403.
66. Zucker R. S. 1999 Calcium- and activity-dependent synaptic plasticity. Curr. Opin. Neurobiol. 9 305 313.
67. Zucker R. S. Regehr W. G. 2002 Short-term synaptic plasticity. Annu. Rev. Physiol. 64 355 405.