Identification of secretory granule phosphatidylinositol 4,5-bisphosphate-interacting proteins using an affinity pulldown strategy

Molecular and Cellular Proteomics

Volumn 6, Issue 7, 2007, Pages 1158-1169

  Osborne, Shona L ^a   Wallis, Tristan P ^a,b   Jimenez, Jose L ^c   Gorman, Jeffrey J ^a,b   Meunier, Frederic A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ADAPTIN; CALCIUM; CATECHOLAMINE; DIGITONIN; GRANUPHILIN; ISOPROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; POLYLYSINE; SPECTRIN; SYNAPTOTAGMIN; SYNAPTOTAGMIN I; SYNAPTOTAGMIN VII; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATECHOLAMINE RELEASE; CELL FRACTIONATION; CELL MEMBRANE PERMEABILITY; CELL STRAIN; CHROMAFFIN CELL; CHROMAFFIN GRANULE; CONTROLLED STUDY; EXOCYTOSIS; GENE MUTATION; IMMUNOCYTOCHEMISTRY; INHIBITION KINETICS; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NEUROSECRETORY CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RAT; SECRETORY GRANULE; WESTERN BLOTTING;

ADRENAL MEDULLA; AMINO ACID SEQUENCE; ANIMALS; CATECHOLAMINES; CATTLE; CELL FRACTIONATION; CHROMAFFIN GRANULES; EXOCYTOSIS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PC12 CELLS; PHOSPHATIDYLINOSITOL PHOSPHATES; POLYLYSINE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEOME; RATS; SECRETORY VESICLES; SYNAPTOTAGMIN II; SYNAPTOTAGMINS;

EID: 34547101964     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M600430-MCP200     Document Type: Article

References (66)

1. Cremona, O., and De Camilli, P. (2001) Phosphoinositides in membrane traffic at the synapse. J. Cell Sci. 114, 1041-1052
2. Wenk, M. R., and De Camilli, P. (2004) Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl. Acad. Sci. U. S. A. 101, 8262-8269
3. Osborne, S. L., Meunier, F. A., and Schiavo, G. (2001) Phosphoinositides as key regulators of synaptic function. Neuron 32, 9-12
4. 2 as being important in exocytosis. J. Biol. Chem. 275, 17878-17885
5. Bai, J., Tucker, W. C., and Chapman, E. R. (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
6. Schiavo, G., Gu, Q. M., Prestwich, G. D., Sollner, T. H., and Rothman, J. E. (1996) Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl. Acad. Sci. U. S. A. 93, 13327-13332
7. Tucker, W. C., Edwardson, J. M., Bai, J., Kim, H. J., Martin, T. F., and Chapman, E. R. (2003) Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells. J. Cell Biol. 162, 199-209
8. Loyet, K. M. (1998) Specific binding of phosphatidylinositol 4,5-bisphosphate to calcium-dependent activator protein for secretion (CAPS), a potential phosphoinositide effector protein for regulated exocytosis. J. Biol. Chem. 273, 8337-8343
9. Grishanin, R. N., Kowalchyk, J. A., Klenchin, V. A., Ann, K., Earles, C. A., Chapman, E. R., Gerona, R. R., and Martin, T. F. (2004) CAPS acts at a prefusion step in dense-core vesicle exocytosis as a PIP2 binding protein. Neuron 43, 551-562
10. 2+-dependent manner. In vitro characteristics and possible significance. J. Biol. Chem. 273, 10240-10248
11. Speidel, D., Bruederle, C. E., Enk, C., Voets, T., Varoqueaux, F., Reim, K., Becherer, U., Fornai, F., Ruggieri, S., Holighaus, Y., Weihe, E., Bruns, D., Brose, N., and Rettig, J. (2005) CAPS1 regulates catecholamine loading of large dense-core vesicles. Neuron 46, 75-88
12. Chapman, E. R., and Jahn, R. (1994) Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes. Autonomous function of a single C2-homologous domain. J. Biol. Chem. 269, 5735-5741
13. Andrews, N. W., and Chakrabarti, S. (2005) There's more to life than neurotransmission: the regulation of exocytosis by synaptotagmin VII. Trends Cell Biol. 15, 626-631
14. Rizo, J., Chen, X., and Arac, D. (2006) Unraveling the mechanisms of synaptotagmin and SNARE function in neurotransmitter release. Trends Cell Biol. 16, 339-350
15. Osborne, S. L., Herreros, J., Bastiaens, P. I. H., and Schiavo, G. (1999) Calcium-dependent oligomerization of synaptotagmins I and II. Synaptotagmins I and II are localized on the same synaptic vesicle and heterodimerize in the presence of calcium. J. Biol. Chem. 274, 59-66
16. Fukuda, M., and Mikoshiba, K. (2000) Calcium-dependent and -independent hetero-oligomerization in the synaptotagmin family. J. Biochem. (Tokyo) 128, 637-645
17. Wang, P., Chicka, M. C., Bhalla, A., Richards, D. A., and Chapman, E. R. (2005) Synaptotagmin VII is targeted to secretory organelles in PC12 cells, where it functions as a high-affinity calcium sensor. Mol. Cell. Biol. 25, 8693-8702
18. 2+ sensor in exocytosis. Neuron 30, 459-473
19. 2+-dependent exocytosis in PC12 cells. J. Biol. Chem. 279, 52677-52684
20. Chakrabarti, S., Kobayashi, K. S., Flavell, R. A., Marks, C. B., Miyake, K., Liston, D. R., Fowler, K. T., Gorelick, F. S., and Andrews, N. W. (2003) Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice. J. Cell Biol. 162, 543-549
21. Virmani, T., Han, W., Liu, X., Sudhof, T. C., and Kavalali, E. T. (2003) Synaptotagmin 7 splice variants differentially regulate synaptic vesicle recycling. EMBO J. 22, 5347-5357
22. 2+-dependent exocytosis of lysosomes in fibroblasts. J. Cell Biol. 148, 1141-1150
23. Caler, E. V., Chakrabarti, S., Fowler, K. T., Rao, S., and Andrews, N. W. (2001) The exocytosis-regulatory protein synaptotagmin VII mediates cell invasion by Trypanosoma cruzi. J. Exp. Med. 193, 1097-1104
24. 2+-regulated exocytosis of lysosomes. Cell 106, 157-169
25. Roy, D., Liston, D. R., Idone, V. J., Di, A., Nelson, D. J., Pujol, C., Bliska, J. B., Chakrabarti, S., and Andrews, N. W. (2004) A process for controlling intracellular bacterial infections induced by membrane injury. Science 304, 1515-1518
26. Shen, S. S., Tucker, W. C., Chapman, E. R., and Steinhardt, R. A. (2005) Molecular regulation of membrane resealing in 3T3 fibroblasts. J. Biol. Chem. 280, 1652-1660
27. Bon, S., Bader, M. F., Aunis, D., Massoulie, J., and Henry, J. P. (1990) Subcellular distribution of acetylcholinesterase forms in chromaffin cells. Do chromaffin granules contain a specific secretory acetylcholinesterase? Eur. J. Biochem. 190, 221-232
28. Meunier, F. A., Osborne, S. L., Hammond, G. R., Cooke, F. T., Parker, P. J., Domin, J., and Schiavo, G. (2005) PI3-kinase C2α is essential for ATP-dependent priming of neurosecretory granule exocytosis. Mol. Biol. Cell. 16, 4841-4851
29. Wang, D. S., Ching, T. T., St Pyrek, J., and Chen, C. S. (2000) Biotinylated phosphatidylinositol 3,4,5-trisphosphate as affinity ligand. Anal. Biochem. 280, 301-307
30. Coppola, T., Frantz, C., Perret-Menoud, V., Gattesco, S., Hirling, H., and Regazzi, R. (2002) Pancreatic beta-cell protein granuphilin binds Rab3 and Munc-18 and controls exocytosis. Mol. Biol. Cell 13, 1906-1915
31. Matthew, W. D., Tsavaler, L., and Reichardt, L. F. (1981) Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J. Cell Biol. 91, 257-269
32. Gorman, J. J., Wallis, T. P., Whelan, D. A., Shaw, J., and Both, G. W. (2005) LH3, a "homologue" of the mastadenoviral E1B 55-kDa protein is a structural protein of atadenoviruses. Virology 342, 159-166
33. Fernandez, I. (2001) Three-dimensional structure of the synaptotagmin 1 C2B-domain. Synaptotagmin 1 as a phospholipid binding machine. Neuron 32, 1057-1069
34. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385
35. Fukuda, M., and Mikoshiba, K. (2001) Mechanism of the calcium-dependent multimerization of synaptotagmin VII mediated by its first and second C2 domains. J. Biol. Chem. 276, 27670-27676
36. Rickman, C., Craxton, M., Osborne, S., and Davletov, B. (2004) Comparative analysis of tandem C2 domains from the mammalian synaptotagmin family. Biochem. J. 378, 681-686
37. Burgoyne, R. D. (1992) Investigation of the Intracellular Regulators and Components of the Exocytotic Pathway, Vol. 20, p. 433, Humana Press Inc., Totowa, NJ
38. 2+-activated secretion. Nature 374, 173-177
39. Wiedemann, C., Schafer, T., and Burger, M. M. (1996) Chromaffin granule-associated phosphatidylinositol 4-kinase activity is required for stimulated secretion. EMBO J. 15, 2094-2101
40. Rameh, L. E., Arvidsson, A., Carraway, K. L., III, Couvillon, A. D., Rathbun, G., Crompton, A., VanRenterghem, B., Czech, M. P., Ravichandran, K. S., Burakoff, S. J., Wang, D. S., Chen, C. S., and Cantley, L. C. (1997) A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J. Biol. Chem. 272, 22059-22066
41. Perrin, D., Langley, O. K., and Aunis, D. (1987) Anti-α-fodrin inhibits secretion from permeabilized chromaffin cells. Nature 326, 498-501
42. Gaidarov, I., Chen, Q., Falck, J. R., Reddy, K. K., and Keen, J. H. (1996) A functional phosphatidylinositol 3,4,5-trisphosphate/ phosphoinositide binding domain in the clathrin adaptor AP-2 α subunit. Implications for the endocytic pathway. J. Biol. Chem. 271, 20922-20929
43. Slepnev, V. I., and De Camilli, P. (2000) Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat. Rev. Neurosci. 1, 161-172
44. Murshid, A., Srivastava, A., Kumar, R., and Presley, J. F. (2006) Characterization of the localization and function of NECAP 1 in neurons. J. Neurochem. 98, 1746-1762
45. Fukuda, M., Kanno, E., Saegusa, C., Ogata, Y., and Kuroda, T. S. (2002) Slp4-a/granuphilin-a regulates dense-core vesicle exocytosis in PC12 cells. J. Biol. Chem. 277, 39673-39678
46. Fukuda, M., Ogata, Y., Saegusa, C., Kanno, E., and Mikoshiba, K. (2002) Alternative splicing isoforms of synaptotagmin VII in the mouse, rat and human. Biochem. J. 365, 173-180
47. Tagaya, M., Genma, T., Yamamoto, A., Kozaki, S., and Mizushima, S. (1996) SNAP-25 is present on chromaffin granules and acts as a SNAP receptor. FEBS Lett. 394, 83-86
48. Fukuda, M., Kojima, T., Aruga, J., Niinobe, M., and Mikoshiba, K. (1995) Functional diversity of C2 domains of synaptotagmin family. Mutational analysis of inositol high polyphosphate, binding domain. J. Biol. Chem. 270, 26523-26527
49. Ibata, K., Fukuda, M., and Mikoshiba, K. (1998) Inositol 1,3,4,5-tetrakisphosphate binding activities of neuronal and non-neuronal synaptotagmins. Identification of conserved amino acid substitutions that abolish inositol 1,3,4,5-tetrakisphosphate binding to synaptotagmins III, V, and X. J. Biol. Chem. 273, 12267-12273
50. 2+ affinities. EMBO J. 21, 270-280
51. Morciano, M., Burre, J., Corvey, C., Karas, M., Zimmermann, H., and Volknandt, W. (2005) Immunoisolation of two synaptic vesicle pools from synaptosomes: a proteomics analysis. J. Neurochem. 95, 1732-1745
52. Profit, A. A., Chen, J., Gu, Q. M., Chaudhary, A., Prasad, K., Lafer, E. M., and Prestwich, G. D. (1998) Probing the phosphoinositide binding site of the clathrin assembly protein AP-2 with photoaffinity labels. Arch. Biochem. Biophys. 357, 85-94
53. Wang, J., Takeuchi, T., Yokota, H., and Izumi, T. (1999) Novel rabphilin-3-like protein associates with insulin-containing granules in pancreatic beta cells. J. Biol. Chem. 274, 28542-28548
54. Fukuda, M. (2004) RNA interference-mediated silencing of synaptotagmin IX, but not synaptotagmin I, inhibits dense-core vesicle exocytosis in PC12 cells. Biochem. J. 380, 875-879
55. Voets, T., Moser, T., Lund, P. E., Chow, R. H., Geppert, M., Sudhof, T. C., and Neher, E. (2001) Intracellular calcium dependence of large densecore vesicle exocytosis in the absence of synaptotagmin I. Proc. Natl. Acad. Sci. U. S. A. 98, 11680-11685
56. Nagy, G., Kim, J. H., Pang, Z. P., Matti, U., Rettig, J., Sudhof, T. C., and Sorensen, J. B. (2006) Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J. Neurosci. 26, 632-643
57. Bai, J., and Chapman, E. R. (2004) The C2 domains of synaptotagmin-partners in exocytosis. Trends Biochem. Sci. 29, 143-151
58. Poskanzer, K. E., Fetter, R. D., and Davis, G. W. (2006) Discrete residues in the c(2)b domain of synaptotagmin I independently specify endocytic rate and synaptic vesicle size. Neuron 50, 49-62
59. Borden, C. R., Stevens, C. F., Sullivan, J. M., and Zhu, Y. (2005) Synaptotagmin mutants Y311N and K326/327A alter the calcium dependence of neurotransmission. Mol. Cell. Neurosci. 29, 462-470
60. Mackler, J. M., and Reist, N. E. (2001) Mutations in the second C2 domain of synaptotagmin disrupt synaptic transmission at Drosophila neuromuscular junctions. J. Comp. Neurol. 436, 4-16
61. 2+ binding to C2 domains of synaptotagmin 1. J. Biol. Chem. 281, 15845-15852
62. 2+-independent stage of synaptic vesicle priming in vivo. Mol. Biol. Cell. 17, 5211-5226
63. Rickman, C., Archer, D. A., Meunier, F. A., Craxton, M., Fukuda, M., Burgoyne, R. D., and Davletov, B. (2004) Synaptotagmin interaction with the syntaxin/SNAP-25 dimer is mediated by an evolutionarily conserved motif and is sensitive to inositol hexakisphosphate. J. Biol. Chem. 279, 12574-12579
64. 2+-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418, 340-344
65. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb-Viewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723
66. Patton, C., Thompson, S., and Epel, D. (2004) Some precautions using chelators to buffer metals in biological solutions. Cell Calcium 35, 427-431