Nonredundant function of secretory carrier membrane protein isoforms in dense core vesicle exocytosis

American Journal of Physiology - Cell Physiology

Volumn 294, Issue 3, 2008, Pages

  Liao, Haini ^a   Zhang, Jie ^a   Shestopal, Svetlana ^a   Szabo, Gabor ^a   Castle, Anna ^a   Castle, David ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Amperometry; Membrane fusion; Neuroendocrine secretion

Indexed keywords

ISOPROTEIN; MEMBRANE PROTEIN; NORADRENALIN; PROTEIN SCAMP; PROTEIN SCAMP 1; PROTEIN SCAMP 2; PROTEIN SCAMP 3; PROTEIN SCAMP 4; PROTEIN SCAMP 5; RNA; UNCLASSIFIED DRUG;

AMPEROMETRY; ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CELL MEMBRANE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DENSE CORE VESICLE; EXOCYTOSIS; MAMMAL CELL; MEMBRANE FUSION; NEUROSECRETORY CELL; NONHUMAN; NORADRENALIN UPTAKE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; SECRETORY VESICLE;

ANIMALS; CALCIUM SIGNALING; CARRIER PROTEINS; CELL MEMBRANE; EXOCYTOSIS; KINETICS; MEMBRANE FUSION; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MODELS, NEUROLOGICAL; NEURONS; NOREPINEPHRINE; PC12 CELLS; PROTEIN ISOFORMS; RATS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SECRETORY VESICLES; TRANSFECTION; TRITIUM;

MAMMALIA; MYCTEROPERCA PHENAX;

EID: 41549135609     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00493.2007     Document Type: Article

References (43)

1. Abraham C, Hutter H, Palfreyman MT, Spatkowski G, Weimer RM, Windoffer R, Jorgensen EM, Leube RE. Synaptic tetraspan vesicle membrane proteins are conserved but not needed for synaptogenesis and neuronal function in Caenorhabditis elegans. Proc Natl Acad Sci USA 103: 8227-8232, 2006.
2. Bai J, Tucker WC, Chapman ER. 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, 2004.
3. Bai J, Wang CT, Richards DA, Jackson MB, Chapman ER. Fusion pore dynamics are regulated by synaptotagmin*t-SNARE interactions. Neuron 41: 929-942, 2004.
4. Brand SH, Laurie SM, Mixon MB, Castle JD. Secretory carrier membrane proteins 31-35 define a common protein composition among secretory carrier membranes. J Biol Chem 266: 18949-18957, 1991.
5. Castle A, Castle D. 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, 2005.
6. Caumont AS, Galas MC, Vitale N, Aunis D, Bader MF. Regulated exocytosis in chromaffin cells. Translocation of ARF6 stimulates a plasma membrane-associated phospholipase D. J Biol Chem 273: 1373-1379, 1998.
7. Ellena JF, Moulthrop J, Wu J, Rauch M, Jaysinghne S, Castle JD, Cafiso DS. 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, 2004.
8. Fernandez-Chacon R, Achiriloaie M, Janz R, Albanesi JP, Sudhof TC. SCAMP1 function in endocytosis. J Biol Chem 275: 12752-12756, 2000.
9. Fernandez-Chacon R, Alvarez de Toledo G, Hammer RE, Sudhof TC. Analysis of SCAMP1 function in secretory vesicle exocytosis by means of gene targeting in mice. J Biol Chem 274: 32551-32554, 1999.
10. Fernandez-Chacon R, Sudhof TC. Novel SCAMPs lacking NPF repeats: ubiquitous and synaptic vesicle-specific forms implicate SCAMPs in multiple membrane-trafficking functions. J Neurosci 20: 7941-7950, 2000.
11. Finnegan JM, Pihel K, Cahill PS, Huang L, Zerby SE, Ewing AG, Kennedy RT, Wightman RM. Vesicular quantal size measured by amperometry at chromaffin, mast, pheochromocytoma, and pancreatic beta-cells. J Neurochem 66: 1914-1923, 1996.
12. 2+-dependent activator protein for secretion 1 is critical for constitutive and regulated exocytosis but not for loading of transmitters into dense core vesicles. J Biol Chem 282: 21392-21403, 2007.
13. Gong LW, Di Paolo G, Diaz E, Cestra G, Diaz ME, Lindau M, De Camilli P, Toomre D. Phosphatidylinositol phosphate kinase type I gamma regulates dynamics of large dense-core vesicle fusion. Proc Natl Acad Sci USA 102: 5204-5209, 2005.
14. Guo Z, Liu L, Cafiso D, Castle D. Perturbation of a very late step of regulated exocytosis by a secretory carrier membrane protein (SCAMP2)-derived peptide. J Biol Chem 277: 35357-35363, 2002.
15. Haller M, Heinemann C, Chow RH, Heidelberger R, Neher E. Comparison of secretory responses as measured by membrane capacitance and by amperometry. Biophys J 74: 2100-2113, 1998.
16. Hubbard C, Singleton D, Rauch M, Jayasinghe S, Cafiso D, Castle D. The secretory carrier membrane protein family: structure and membrane topology. Mol Biol Cell 11: 2933-2947, 2000.
17. Jankowski JA, Schroeder TJ, Ciolkowski EL, Wightman RM. Temporal characteristics of quantal secretion of catecholamines from adrenal medullary cells. J Biol Chem 268: 14694-14700, 1993.
18. Kishimoto T, Liu TT, Hatakeyama H, Nemoto T, Takahashi N, Kasai H. Sequential compound exocytosis of large dense-core vesicles in PC12 cells studied with TEPIQ (two-photon extracellular polar-tracer imaging-based quantification) analysis. J Physiol 568: 905-915, 2005.
19. Klenchin VA, Martin TF. Priming in exocytosis: attaining fusion-competence after vesicle docking. Biochimie 82: 399-407, 2000.
20. Lang T, Bruns D, Wenzel D, Riedel D, Holroyd P, Thiele C, Jahn R. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J 20: 2202-2213, 2001.
21. Liao H, Ellena J, Liu L, Szabo G, Cafiso D, Castle D. Secretory carrier membrane protein SCAMP2 and phosphatidylinositol 4,5-bisphosphate interactions in the regulation of dense core vesicle exocytosis. Biochemistry 46: 10909-10920, 2007.
22. + exchanger NHE7. J Cell Sci 118: 1885-1897, 2005.
23. Liu L, Guo Z, Tieu Q, Castle A, Castle D. Role of secretory carrier membrane protein SCAMP2 in granule exocytosis. Mol Biol Cell 13: 4266-4278, 2002.
24. Liu L, Liao H, Castle A, Zhang J, Casanova J, Szabo G, Castle D. 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, 2005.
25. Martin TF. Tuning exocytosis for speed: fast and slow modes. Biochim Biophys Acta 1641: 157-165, 2003.
26. 2+-activated exocytosis in a cell-free system. J Biol Chem 272: 14447-14453, 1997.
27. Muller HK, Wiborg O, Haase J. Subcellular redistribution of the serotonin transporter by secretory carrier membrane protein 2. J Biol Chem 281: 28901-28909, 2006.
28. Nemoto T, Kimura R, Ito K, Tachikawa A, Miyashita Y, Iino M, Kasai H. Sequential-replenishment mechanism of exocytosis in pancreatic acini. Nat Cell Biol 3: 253-258, 2001.
29. Ninomiya Y, Kishimoto T, Yamazawa T, Ikeda H, Miyashita Y, Kasai H. Kinetic diversity in the fusion of exocytotic vesicles. EMBO J 16: 929-934, 1997.
30. Sbalzarini IF, Koumoutsakos P. Feature point tracking and trajectory analysis for video imaging in cell biology. J Struct Biol 151: 182-195, 2005.
31. Singleton DR, Wu TT, Castle JD. Three mammalian SCAMPs (secretory carrier membrane proteins) are highly related products of distinct genes having similar subcellular distributions. J Cell Sci 110: 2099-2107, 1997.
32. Sorensen JB. Formation, stabilisation and fusion of the readily releasable pool of secretory vesicles. Pflügers Arch 448: 347-362, 2004.
33. Speidel D, Bruederle CE, Enk C, Voets T, Varoqueaux F, Reim K, Becherer U, Fornai F, Ruggieri S, Holighaus Y, Weihe E, Bruns D, Brose N, Rettig J. CAPS1 regulates catecholamine loading of large dense-core vesicles. Neuron 46: 75-88, 2005.
34. Taraska JW, Almers W. Bilayers merge even when exocytosis is transient. Proc Natl Acad Sci USA 101: 8780-8785, 2004.
35. Toonen RF, Kochubey O, de Wit H, Gulyas-Kovacs A, Konijnenburg B, Sorensen JB, Klingauf J, Verhage M. Dissecting docking and tethering of secretory vesicles at the target membrane. EMBO J 25: 3725-3737, 2006.
36. Travis ER, Wightman RM. Spatio-temporal resolution of exocytosis from individual cells. Annu Rev Biophys Biomol Struct 27: 77-103, 1998.
37. Vitale N, Caumont AS, Chasserot-Golaz S, Du G, Wu S, Sciorra VA, Morris AJ, Frohman MA, Bader MF. Phospholipase D1: a key factor for the exocytotic machinery in neuroendocrine cells. EMBO J 20: 2424-2434, 2001.
38. Vitale N, Chasserot-Golaz S, Bailly Y, Morinaga N, Frohman MA, Bader MF. 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, 2002.
39. 2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: fusion pore opening and fusion pore dilation. J Physiol 570: 295-307, 2006.
40. Wang CT, Grishanin R, Earles CA, Chang PY, Martin TF, Chapman ER, Jackson MB. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294: 1111-1115, 2001.
41. Wang CT, Lu JC, Bai J, Chang PY, Martin TF, Chapman ER, Jackson MB. Different domains of synaptotagmin control the choice between kiss-and-run and full fusion. Nature 424: 943-947, 2003.
42. Wu TT, Castle JD. Evidence for colocalization and interaction between 37 and 39 kDa isoforms of secretory carrier membrane proteins (SCAMPs). J Cell Sci 110: 1533-1541, 1997.
43. Zhou Z, Misler S, Chow RH. Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys J 70: 1543-1552, 1996.