Secretory carrier membrane protein SCAMP2 and phosphatidylinositol 4,5-bisphosphate interactions in the regulation of dense core vesicle exocytosis

Biochemistry

Volumn 46, Issue 38, 2007, Pages 10909-10920

  Liao, Haini ^a,b   Ellena, Jeff ^b   Liu, Lixia ^a   Szabo, Gabor ^a   Cafiso, David ^b   Castle, David ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCYTOSIS; MEMBRANE FUSION; NUCLEAR RELAXATION; OXYGEN ENHANCEMENT; TRYPTOPHAN;

BIOLOGICAL MEMBRANES; CELLS; HORMONES; LIPOSOMES; PARAMAGNETIC RESONANCE;

PROTEINS;

ALANINE; ARGININE; HUMAN GROWTH HORMONE; LIPOSOME; LYSINE; NORADRENALIN; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN DERIVATIVE; SECRETORY CARRIER MEMBRANE PROTEIN 2; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; EXOCYTOSIS; GENETIC TRANSFECTION; LIPID MEMBRANE; NONHUMAN; NORADRENALIN RELEASE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CALCIUM; CARRIER PROTEINS; CELL MEMBRANE; CLONING, MOLECULAR; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTROSTATICS; EXOCYTOSIS; HUMANS; MEMBRANE FUSION; MEMBRANE PROTEINS; MUTAGENESIS, SITE-DIRECTED; PC12 CELLS; PEPTIDES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; SECRETORY VESICLES; SPIN LABELS; SUBCELLULAR FRACTIONS; TRANSFECTION; UNILAMELLAR LIPOSOMES; VESICULAR TRANSPORT PROTEINS;

EID: 34648833644     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701121j     Document Type: Article

References (49)

1. Di Paolo, G., and De Camilli, P. (2006) Phosphoinositides in cell regulation and membrane dynamics, Nature 443, 651-657.
2. De Matteis, M. A., and Godi, A. (2004) Protein-lipid interactions in membrane trafficking at the Golgi complex, Biochim. Biophys. Acta 1666, 264-274.
3. McLaughlin, S., Wang, J., Gambhir, A., and Murray, D. (2002) PIP(2) and proteins: interactions, organization, and information flow, Annu. Rev. Biophys. Biomol. Struct. 31, 151-175.
4. Holz, R. W., Hlubek, M. D., Sorensen, S. D., Fisher, S. K., Balla, T., Ozaki, S., Prestwich, G. D., Stuenkel, E. L., and Bittner, M. A. (2000) A pleckstrin homology domain specific for phosphatidylinositol 4, 5-bisphosphate (PtdIns-4,5-P2) and fused to green fluorescent protein identifies plasma membrane PtdIns-4,5-P2 as being important in exocytosis, J. Biol. Chem. 275, 17878-17885.
5. Aikawa, Y., and Martin, T. F. (2003) ARF6 regulates a plasma membrane pool of phosphatidylinositol(4,5)bisphosphate required for regulated exocytosis, J. Cell Biol. 162, 647-659.
6. Hay, J. C., and Martin, T. F. (1993) Phosphatidylinositol transfer protein required for ATP-dependent priming of Ca(2+)-activated secretion, Nature 366, 572-575.
7. Hay, J. C., Fisette, P. L., Jenkins, G. H., Fukami, K., Takenawa, T., Anderson, R. A., and Martin, T. F. (1995) ATP-dependent inositide phosphorylation required for Ca(2+)-activated secretion, Nature 374, 173-177.
8. Milosevic, I., Sorensen, J. B., Lang, T., Krauss, M., Nagy, G., Haucke, V., Jahn, R., and Neher, E. (2005) Plasmalemmal phosphatidylinositol-4,5- bisphosphate level regulates the releasable vesicle pool size in chromaffin cells, J. Neurosci. 25, 2557-2565.
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. 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.
11. Gong, L. W., Di Paolo, G., Diaz, E., Cestra, G., Diaz, M. E., Lindau, M., De, Camilli, P., and Toomre, D. (2005) Phosphatidylinositol phosphate kinase type I gamma regulates dynamics of large dense-core vesicle fusion, Proc. Natl. Acad. Sci. U.S.A. 102, 5204-5209.
12. Laux, T., Fukami, K., Thelen, M., Golub, T., Frey, D., and Caroni, P. (2000) GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism, J. Cell Biol. 149, 1455-1472.
13. Aoyagi, K., Sugaya, T., Umeda, M., Yamamoto, S., Terakawa, S., and Takahashi, M. (2005) The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters, J. Biol. Chem. 280, 17346-17352.
14. Brand, S. H., and Castle, J. D. (1993) SCAMP 37, a new marker within the general cell surface recycling system, EMBO J. 12, 3753-3761.
15. Castle, A., and Castle, D. (2005) Ubiquitously expressed secretory carrier membrane proteins (SCAMPs) 1-4 mark different pathways and exhibit limited constitutive trafficking to and from the cell surface, J. Cell Sci. 118, 3769-3780.
16. Fernandez-Chacon, R., and Sudhof, T. C. (2000) Novel SCAMPs lacking NPF repeats: ubiquitous and synaptic vesicle-specific forms implicate SCAMPs in multiple membrane-trafficking functions, J. Neurosci. 20, 7941-7950.
17. Fernandez-Chacon, R., Alvarez de Toledo, G., Hammer, R. E., and Sudhof, T. C. (1999) Analysis of SCAMP1 function in secretory vesicle exocytosis by means of gene targeting in mice, J. Biol. Chem. 274, 32551-32554.
18. Guo, Z., Liu, L., Cafiso, D., and Castle, D. (2002) Perturbation of a very late step of regulated exocytosis by a secretory carrier membrane protein (SCAMP2)-derived peptide, J. Biol. Chem. 277, 35357-35363.
19. Liu, L., Guo, Z., Tieu, Q., Castle, A., and Castle, D. (2002) Role of secretory carrier membrane protein SCAMP2 in granule exocytosis, Mol. Biol. Cell 13, 4266-4278.
20. Liu, L., Liao, H., Castle, A., Zhang, J., Casanova, J., Szabo, G., and Castle, D. (2005) SCAMP2 interacts with Arf6 and phospholipase D1 and links their function to exocytotic fusion pore formation in PC12 cells, Mol. Biol. Cell 16, 4463-4472.
21. Caumont, A. S., Vitale, N., Gensse, M., Galas, M. C., Casanova, J. E., and Bader, M. F. (2000) Identification of a plasma membrane-associated guanine nucleotide exchange factor for ARF6 in chromaffin cells. Possible role in the regulated exocytotic pathway, J. Biol. Chem. 275, 15637-15644.
22. Vitale, N., Chasserot-Golaz, S., Bailly, Y., Morinaga, N., Frohman, M. A., and Bader, M. F. (2002) Calcium-regulated exocytosis of dense-core vesicles requires the activation of ADP-ribosylation factor (ARF)6 by ARF nucleotide binding site opener at the plasma membrane, J. Cell Biol. 159, 79-89.
23. Hubbard, C., Singleton, D., Rauch, M., Jayasinghe, S., Cafiso, D., and Castle, D. (2000) The secretory carrier membrane protein family: structure and membrane topology, Mol. Biol. Cell 11, 2933-2947.
24. Wang, J., Gambhir, A., Hangyas-Mihalyne, G., Murray, D., Golebiewska, U., and McLaughlin, S. (2002) Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions, J. Biol. Chem. 277, 34401-34412.
25. Ellena, J. F., Moulthrop, J., Wu, J., Rauch, M., Jaysinghne, S., Castle, J. D., and Cafiso, D. S. (2004) Membrane position of a basic aromatic peptide that sequesters phosphatidylinositol 4,5 bisphosphate determined by site-directed spin labeling and high-resolution NMR, Biophys. J. 87, 3221-3233.
26. Grassetti, D. R., and Murray, J. F., Jr. (1967) Determination of sulfhydryl groups with 2,2′- or 4,4′-dithiodipyridine, Arch. Biochem. Biophys. 119, 41-49.
27. Ellena, J. F., Obraztsov, V. V., Cumbea, V. L., Woods, C. M., and Cafiso, D. S. (2002) Perfluorooctyl bromide has limited membrane solubility and is located at the bilayer center. Locating small molecules in lipid bilayers through paramagnetic enhancements of NMR relaxation, J. Med. Chem. 45, 5534-5542.
28. Wang, C. T., Grishanin, R., Earles, C. A., Chang, P. Y., Martin, T. F., Chapman, E. R., and Jackson, M. B. (2001) Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles, Science 294, 1111-1115.
29. Chung, S. H., Joberty, G., Gelino, E. A., Macara, I. G., and Holz, R. W. (1999) Comparison of the effects on secretion in chromaffin and PC12 cells of Rab3 family members and mutants. Evidence that inhibitory effects are independent of direct interaction with Rabphilin3, J. Biol. Chem. 274, 18113-18120.
30. Wang, C. T., Bai, J., Chang, P. Y., Chapman, E. R., and Jackson, M. B. (2006) Synaptotagmin-Ca2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: fusion pore opening and fusion pore dilation, J. Physiol. 570, 295-307.
31. Colliver, T. L., Hess, E. J., Pothos, E. N., Sulzer, D., and Ewing, A. G. (2000) Quantitative and statistical analysis of the shape of amperometric spikes recorded from two populations of cells, J. Neurochem. 74, 1086-1097.
32. Bai, J., Wang, C. T., Richards, D. A., Jackson, M. B., and Chapman, E. R. (2004) Fusion pore dynamics are regulated by synaptotagmin*t-SNARE interactions, Neuron 41, 929-942.
33. Wimley, W. C., Creamer, T. P., and White, S. H. (1996) Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides, Biochemistry 35, 5109-5124.
34. Rauch, M. E., Ferguson, C. G., Prestwich, G. D., and Cafiso, D. S. (2002) Myristoylated alanine-rich C kinase substrate (MARCKS) sequesters spin-labeled phosphatidylinositol 4,5-bisphosphate in lipid bilayers, J. Biol. Chem. 277, 14068-14076.
35. Windrem, D. A., and Plachy, W. Z. (1980) The diffusion-solubility of oxygen in lipid bilayers, Biochim. Biophys. Acta 600, 655-665.
36. Wang, J., Arbuzova, A., Hangyas-Mihalyne, G., and McLaughlin, S. (2001) The effector domain of myristoylated alanine-rich C kinase substrate binds strongly to phosphatidylinositol 4,5-bisphosphate, J. Biol. Chem. 276, 5012-5019.
37. Travis, E. R., and Wightman, R. M. (1998) Spatio-temporal resolution of exocytosis from individual cells, Annu. Rev. Biophys. Biomol. Struct. 27, 77-103.
38. McLaughlin, S., and Murray, D. (2005) Plasma membrane phosphoinositide organization by protein electrostatics, Nature 438, 605-611.
39. Victor, K., J. Jacob, and D. S. Cafiso. 1999. Interactions controlling the membrane binding of basic protein domains: phenylalanine and the attachmentof the myristoylated alanine-rich C-kinase substrate protein to interfaces. Biochemistry 38, 12527-12536.
40. Ben-Tal, N., Honig, B., Peitzsch, R. M., Denisov, G., and McLaughlin, S. (1996) Binding of small basic peptides to membranes containing acidic lipids; theoretical models and experimental results, Biophys. J. 71, 561-575.
41. Wang, J., Gambhir, A., McLaughlin, S., and Murray, D. (2004) A computational model for the electrostatic sequestration of PI-(4,5)P2 by membrane absorbed basic peptides. Biophys. J. 86, 1969-1986.
42. Singleton, D. R., Wu, T. T., and Castle, J. D. (1997) Three mammalian SCAMPs (secretory carrier membrane proteins) are highly related products of distinct genes having similar subcellular distributions, J. Cell Sci. 110 (Part 17), 2099-2107.
43. Wu, T. T., and Castle, J. D. (1997) Evidence for colocalization and interaction between 37 and 39 kDa isoforms of secretory carrier membrane proteins (SCAMPs), J. Cell Sci. 110 (Part 13), 1533-1541.
44. Martin, T. F. (2003) Tuning exocytosis for speed: fast and slow modes, Biochim. Biophys. Acta 1641, 157-165.
45. Sorensen, J. B. (2004) Formation, stabilisation and fusion of the readily releasable pool of secretory vesicles, Pfluegers Arch. 448, 347-362.
46. Suh, B. C., and Hille, B. (2005) Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate, Curr. Opin. Neurobiol. 15, 370-378.
47. Hoshi, T., Zagotta, W. N., and Aldrich, R. W. (1990) Biophysical and molecular mechanisms of Shaker potassium channel inactivation, Science 250, 533-538.
48. Oliver, D., Lien, C. C., Soom, M., Baukrowitz, T., Jonas, P., and Fakler, B. (2004) Functional conversion between A-type and delayed rectifier K+ channels by membrane lipids, Science 304, 265-270.
49. Prescott, E. D., and Julius, D. (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity, Science 300, 1284-1288.