DOC2B, C2 domains, and calcium: A tale of intricate interactions

Molecular Neurobiology

Volumn 41, Issue 1, 2010, Pages 42-51

  Friedrich, Reut ^a   Yeheskel, Adva ^a   Ashery, Uri ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

C2 domain; Calcium; DOC2B; Exocytosis; Munc13

Indexed keywords

CALCIUM; CELL PROTEIN; DOUBLE C2 DOMAIN A; DOUBLE C2 DOMAIN B; MEMBRANE PROTEIN; MUNC13 PROTEIN; MUNC18 PROTEIN; PHOSPHOLIPID; RABPHILIN 3A; SYNTAXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; BIOINFORMATICS; CALCIUM BINDING; CALCIUM SIGNALING; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA LIBRARY; EXOCYTOSIS; MOLECULAR DOCKING; NONHUMAN; PHEOCHROMOCYTOMA CELL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RAT; REVIEW; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

EID: 77950458573     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12035-009-8094-8     Document Type: Review

References (72)

1. Fukuda M, Mikoshiba K (2001) Doc2gamma, a third isoform of double C2 protein, lacking calcium-dependent phospholipid binding activity. Biochem Biophys Res Commun 276: 626-632
2. 2. Verhage M, de Vries KJ, Røshol H, Burbach JP, Crispen WH, Südhof TC (1997) DOC2 proteins in rat brain: complementary distribution and proposed function as vesicular adapter proteins in early stages of secretion. Neuron 18: 453-461 (Pubitemid 27138792)
3. Orita S, Sasaki T, Naito A, Komuro R, Ohtsuka T, Maeda M, Suzuki H, Igarashi H, Takai Y (1995) Doc2: a novel brain protein having two repeated C2-like domains. Biochem Biophys Res Commun 206: 439-448
4. Duncan RR, Shipston MJ, Chow RH (2000) Double C2 protein. A review. Biochimie 82: 421-426
5. 5. Korteweg N, Denekamp FA, Verhage M, Burbach HP (2000) Different spatiotemporal expression of DOC2 genes in the developing rat brain argues for an additional, nonsynaptic role of DOC2B in early development. Eur J Neurosci 12: 165-171 (Pubitemid 30068422)
6. (2+) dependent secretory lysosome exocytosis in mast cells. J Immunol 180: 4774-4784
7. Friedrich R, Groffen AJ, Connell E, van Weering JR, Gutman O, Henis YI, Davletov B, Ashery U (2008) DOC2B acts as a calcium switch and enhances vesicle fusion. J Neurosci 28: 6794-6806
8. Bhangu PS, Genever PG, Spencer GJ, Grewal TS, Skerry TM (2001) Evidence for targeted vesicular glutamate exocytosis in osteoblasts. Bone 29: 16-23
9. Nishizuka Y (1988) The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334: 661-665
10. 10. Nalefski E, Falke J (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5: 2375-2390 (Pubitemid 26424851)
11. 2+-binding domain. J Biol Chem 273: 15879-15882
12. 12. Verdaguer N, Corbalan-Garcia S, Ochoa WF, Fita I, GómezFernández JC (1999) Ca(2+) bridges the C2 membrane-binding domain of protein kinase C alpha directly to phosphatidylserine. EMBO J 18: 6329-6338 (Pubitemid 29533237)
13. (2+)-induced recruitment of the secretory vesicle protein DOC2B to the target membrane. J Biol Chem 279: 23740-23747
14. Groffen AJ, Friedrich R, Brian EC, Ashery U, Verhage M (2006) DOC2A and DOC2B are sensors for neuronal activity with unique calcium-dependent and kinetic properties. J Neurochem 97: 818-833
15. 15. Malkinson G, Spira ME (2006) Calcium concentration threshold and translocation kinetics of EGFP-DOC2B expressed in cultured Aplysia neurons. Cell Calcium 39: 85-93 (Pubitemid 43009888)
16. 16. Kojima T, Fukuda M, Aruga J, Mikoshiba K (1996) Calcium-dependent phospholipid binding to the C2.A domain of a ubiquitous form of double C2 protein (Doc2 beta). J Biochem 120: 671-676 (Pubitemid 26331660)
17. Coudevylle N, Montaville P, Leonov A, Zweckstetter M, Becker S (2008) Structural, determinants for Ca2 + and phosphatidylinositol 4, 5-bisphosphate binding by the C2A domain of rabphilin-3A. J Biol Chem 283: 35918-35928
18. Biadene M, Montaville P, Sheldrick GM, Becker S (2006) Structure of the C2A domain of rabphilin-3A. Acta Crystallogr D Biol Crystallogr 62: 793-799
19. Myers JK, Pace CN (1996) Hydrogen bonding stabilizes globular proteins. Biophys J 71: 2033-2039
20. 20. Pace CN, Shirley BA, McNutt M, Gajiwala K (1996) Forces contributing to the conformational stability of proteins. FASEB J 10: 75-83 (Pubitemid 26035509)
21. 21. Pace C, Horn G, Hebert EJ, Bechert J, Shaw K, Urbanikova L, Scholtz JM, Sevcik J (2001) Tyrosine hydrogen bonds make a large contribution to protein stability. J Mol Biol 312: 393-404 (Pubitemid 32928134)
22. 22. Pokkuluri PR, Raffen R, Dieckman L, Boogaard C, Stevens FJ, Schiffer M (2002) Increasing protein stability by polar surface residues: domain-wide consequences of interactions within a loop. Biophys J 82: 391-398 (Pubitemid 34289811)
23. Fernández-Chacón RKA, Gerber SH, García J, Matos MF, Stevens CF, Brose N, Rizo J, Rosenmund C, Südhof TC (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature 410: 41-49
24. Perm MS, Fried. VA, Mignery GA, Jahn R, Südhof TC (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345: 260-263
25. 2+binding loop of synaptotagmin with lipid bilayers. J Biol Chem 273: 13995-14001
26. Bai J, Earles CA, Lewis JL, Chapman ER (2000) Membraneembedded synaptotagmin penetrates cis or trans target membranes and clusters via a novel mechanism. J Biol Chem 275: 25427-25435
27. 27. Bai J, Tucker WC, Chapman ER. (2004) PIP2 increases the speed-of-response of synaptotagmin and steers its membrane penetration activity toward the plasma membrane. Nat Struct Mol Biol 11: 36-44 (Pubitemid 38173439)
28. (2+)triggered membrane penetration activity within the C2B domain of synaptotagmin I. Proc Natl Acad Sci USA 99: 1665-1670
29. 29. Hui E, Bai J, Chapman ER (2006) Ca2+-triggered simultaneous membrane penetration of the tandem C2-domains of synaptotagmin I. Biophys J 91: 1767-1777 (Pubitemid 44352441)
30. 30. Herrick DZ, Sterbling S, Rasch KA, Hinderliter A, Cafiso DS (2006) Position of synaptotagmin I at the membrane interface: cooperative interactions of tandem C2 domains. Biochemistry 45: 9668-9674 (Pubitemid 44257414)
31. 2+ binding to the C2A domain of synaptotagmin I. J Neurosci 22:8438-8446
32. 2+-dependent phospholipid binding by the C2A domain from synaptotagmin I. Diabetes 51: 512-518
33. 33. Weinreb G, Lentz BR. (2007) Analysis of membrane fusion as a two-state sequential process: evaluation of the stalk model. Biophys J 92: 4012-4029 (Pubitemid 46910587)
34. 34. Martens S, Kozlov MM, McMahon HT (2007) How synaptotagmin promotes membrane fusion. Science 316: 1205-1208 (Pubitemid 46877485)
35. 35. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Söllner TH, Rothman JE (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92: 759-772 (Pubitemid 28155315)
36. 36. Rickman C, Jiménez JL, Graham ME, Archer DA, Soloviev M, Burgoyne RD, Davletov B (2006) Conserved profusion protein assembly in regulated exocytosis. Mol Biol Cell 17: 283-294 (Pubitemid 43049481)
37. (2+)-regulated fusion. Cell 138: 709-721
38. Amatore C, Arbault S, Bouret Y, Guille M, Lemaître F, Verchier Y (2006) Regulation of exocytosis in chromaffin cells by trans-insertion of lysophosphatidylcholine and arachidonic acid into the outer leaflet of the cell membrane. Chembiochem 7(12): 1998-2003
39. Fang Q, Berberian K, Gong L, Hafez I, Sorensen JB, Lindau M (2008) The role of the C terminus of the SNARE protein SNAP25 in fusion pore opening and a model for fusion pore mechanics. PNAS 105: 15388-15392
40. Alberts B, Bray D, Johnson A, Lewis J, Raff M, Roberts K, Walter P (1998) Essential cell biology. Garland, New York
41. Fukuda N, Emoto M, Nakamori Y, Taguchi A, Miyamoto S, Uraki S, Oka Y, Tanizawa Y (2009) DOC2B: a novel syntaxin-4 binding protein mediating insulin-regulated GLUT4 vesicle fusion in adipocytes. Diabetes 58: 377-384
42. 42. Ke B, Oh E, Thurmond DC (2007) Doc2beta is a novel Munc18c-interacting partner and positive effector of syntaxin 4-mediated exocytosis. J Biol Chem 282: 21786-21797 (Pubitemid 47195780)
43. Miyazaki M, Emoto M, Fukuda N, Hatanaka M, Taguchi A, Miyamoto S, Tanizawa Y (2009) DOC2b is a SNARE regulator of glucose-stimulated delayed insulin secretion. Biochem Biophys Res Commun 384: 461-465
44. Sakaguchi G, Manabe T, Kobayashi K, Orita S, Sasaki T, Naito A, Maeda M, Igarashi H, Katsuura G, Nishioka H, Mizoguchi A, Itohara S, Takahashi T, Takai Y (1999) Doc2alpha is an activity-dependent modulator of excitatory synaptic transmission. Eur J Neurosci 11: 4262-4268
45. (2+) sensors with distinct Ca(2+) affinities. EMBO J 21: 270-280
46. Deák F, Shin OH, Tang J, Hanson P, Ubach J, Jahn R, Rizo J, Kavalali ET, Südhof TC (2006) Rabphilin regulates SNARE-dependent re-priming of synaptic vesicles for fusion. EMBO J 25: 2856-2866
47. 47. Montaville P, Schlicker C, Leonov A, Zweckstetter M, Sheldrick GM, Becker S (2007) The C2A-C2B linker defines the high affinity Ca(2+) binding mode of rabphilin-3A. J Biol Chem 282: 5015-5025 (Pubitemid 47100949)
48. Ubach J, Zhang X, Shao X, Südhof TC, Rizo J (1998) Ca2+ binding to synaptotagmin: how many Ca2+ ions bind to the tip of a C2-domain? EMBO J 17: 3921-3930
49. 49. Ochoa WF, Corbalán-Garcia S, Eritja R, Rodriguez-Alfaro JA, Gómez-Fernández JC, Fita. I, Verdaguer N (2002) Additional binding sites for anionic phospholipids and calcium ions in the crystal structures of complexes of the C2 domain of protein kinase c alpha. J Mol Biol 320: 277-291 (Pubitemid 34722218)
50. 50. Sakaguchi G, Orita. S, Maeda M, Igarashi H, Takai Y (1995) Molecular cloning of an isoform of Doc2 having two C2-like domains. Biochem. Biophys Res Commun 217: 1053-1061 (Pubitemid 26019759)
51. 2+-dependent exocytosis from PC12 cells. J Biol Chem 271: 7257-7260
52. 2+-dependent exocytotic machinery. J Biol Chem 272: 16081-16084
53. 53. 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: 11418-11422 (Pubitemid 28450143)
54. 54. Duncan RR, Betz A, Shipston MJ, Brose N, Chow RH (1999) Transient, phorbol ester-induced DOC2-Munc13 interactions in vivo. J Biol Chem 274: 27347-27350 (Pubitemid 129527774)
55. 55. Abdullah LH, Bundy JT, Ehre C, Davis CW (2003) Mucin secretion and. PKC isoforms in SPOC1 goblet cells: differential activation by purinergic agonist and PMA. Am J Physiol Lung Cell Mol Physiol 285: L149-L160 (Pubitemid 36736478)
56. 56. 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 (Pubitemid 30462117)
57. 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
58. 58. Basu J, Betz A, Brose N, Rosenmund. C (2007) Munc13-1 C1 domain activation lowers the energy barrier for synaptic vesicle fusion. J Neurosci 27: 1200-1210 (Pubitemid 46203329)
59. 59. Hon T, Takai Y, Takaliashi T (1999) Presynaptic mechanism for phorbol ester-induced synaptic potentiation. J Neurosci 19: 7262-7267 (Pubitemid 29404582)
60. Wakade TD, Bhave SV, Bhave AS, Malhotra RK, Wakade AR. (1991) Depolarizing stimuli and neurotransmitters utilize separate pathways to activate protein kinase C in sympathetic neurons. J Biol Chem 266: 6424-6428
61. 61. Oancea E, Meyer T (1998) Protein kinase C as a molecular machine for decoding calcium, and diacylglycerol signals. Cell 95: 307-318 (Pubitemid 28507320)
62. 2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron 28: 537-545
63. Toonen RF (2003) Role of Munc18-1 in synaptic vesicle and large dense-core vesicle secretion. Biochem Soc Trans 31: 848-850
64. Rizo J, Rosenmund C (2008) Synaptic vesicle fusion. Nat Struct Mol Biol 15: 665-674
65. Jewell JL, Oh E, Bennett SM, Meroueh SO, Thurmond DC (2008) The tyrosine phosphorylation of Munc18c induces a switch in binding specificity from syntaxin 4 to Doc2beta. J Biol Chem 283: 21734-21746
66. Chapman ER (2008) How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77: 615-641
67. 67. Fukuda M, Kanno E (2005) Analysis of the role of Rab27 effector Slp4-a/Granuphilin-a in dense-core vesicle exocytosis. Methods Enzymol 403: 445-457 (Pubitemid 43216930)
68. 68. Fukuda M, Saegusa C, Mikoshiba K (2001) Novel splicing isoforms of synaptotagmin-like proteins 2 and 3: identification of the Slp homology domain. Biochem Biophys Res Commun 283: 513-519 (Pubitemid 32924721)
69. Krivov GG, Shapovalov MV, Dunbrack RL Jr (2009) Improved prediction of protein side-chain conformations with SCWRL4. Proteins 77(4): 778-795
70. 70. Rohl CA, Strauss CE, Misura KM, Baker D (2004) Protein structure prediction using Rosetta. Methods Enzymol 383: 66-93 (Pubitemid 38401787)
71. Lovell SC, Davis IW, Arendall WB III, de Bakker PIW, Word JM, Prisant MG, Richardson JS, Richardson DC (2003) Structure validation by C-alpha geometry: phi, psi, and C-beta deviation. Proteins 50: 437-450
72. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB 3rd, Snoeyink J, Richardson JS, Richardson DC (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-W383