The association of dynamin with synaptophysin regulates quantal size and duration of exocytotic events in chromaffin cells

Journal of Neuroscience

Volumn 30, Issue 32, 2010, Pages 10683-10691

  González Jamett, Arlek M ^a   Báez Matus, Ximena ^a   Hevia, Montserrat A ^a   Guerra, María José ^a   Olivares, María José ^a   Martínez, Agustín D ^a   Neely, Alan ^a   Cárdenas, Ana M ^a  

^a UNIVERSIDAD DE VALPARAÍSO   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CATECHOLAMINE; DYNAMIN; MONOCLONAL ANTIBODY; PEPTIDE; SYNAPTOPHYSIN; SYNAPTOBREVIN 2;

AMPEROMETRY; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATECHOLAMINE RELEASE; CELL FRACTIONATION; CELL SIZE; CHROMAFFIN CELL; CHROMAFFIN GRANULE; CONTROLLED STUDY; EXOCYTOSIS; INJECTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SPIKE WAVE; ANIMAL; CATTLE; CELL CULTURE; CHEMISTRY; DRUG EFFECT; ELECTROCHEMISTRY; GENETICS; IMMUNOLOGY; IMMUNOPRECIPITATION; METABOLISM; METHODOLOGY; MICROINJECTION; PHYSIOLOGY; PROTEIN BINDING; PROTEIN DOMAIN; ULTRASTRUCTURE;

ANIMALS; ANTIBODIES; CATTLE; CELLS, CULTURED; CHROMAFFIN CELLS; CHROMAFFIN GRANULES; DYNAMINS; ELECTROCHEMISTRY; EXOCYTOSIS; IMMUNOPRECIPITATION; MICROINJECTIONS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; SUBCELLULAR FRACTIONS; SYNAPTOPHYSIN; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 77956198113     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5210-09.2010     Document Type: Article

References (53)

1. Albillos A, Dernick G, Horstmann H, Almers W, Alvarez de Toledo G, Lindau M (1997) The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389:509-512.
2. Alder J, Lu B, Valtorta F, Greengard P, Poo MM (1992a) Calcium-dependent transmitter secretion reconstituted in Xenopus oocytes: requirement for synaptophysin. Science 257:657-661.
3. Alder J, Xie ZP, Valtorta F, Greengard P, Poo M (1992b) Antibodies to synaptophysin interfere with transmitter secretion at neuromuscular synapses. Neuron 9:759-768.
4. Alés E, Tabares L, Poyato JM, Valero V, Lindau M, Alvarez de Toledo G (1999) High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat Cell Biol 1:40-44.
5. Annaert WG, Llona I, Backer AC, Jacob WA, De Potter WP (1993) Catecholamines are present in a synaptic-like microvesicle-enriched fraction from bovine adrenal medulla. J Neurochem 60:1746-1754.
6. Ardiles AO, Maripillán J, Lagos VL, Toro R, Mora IG, Villarroel L, Alés E, Borges R, Cárdenas AM (2006) A rapid exocytosis mode in chromaffin cells with a neuronal phenotype. J Neurochem 99:29-41.
7. Ardiles AO, González-Jamett AM, Maripillán J, Naranjo D, Caviedes P, Cárdenas AM (2007) Calcium channel subtypes differentially regulate fusion pore stability and expansion. J Neurochem 103:1574-1581.
8. Barclay JW, Craig TJ, Fisher RJ, Ciufo LF, Evans GJ, Morgan A, Burgoyne RD (2003) Phosphorylation of Munc18 by protein kinase C regulates the kinetics of exocytosis. J Biol Chem 278:10538-10545.
9. Cameron PL, Südhof TC, Jahn R, De Camilli P (1991) Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis. J Cell Biol 115:151-164.
10. Cao H, Garcia F, McNiven MA (1998) Differential distribution of dynamin isoforms in mammalian cells. Mol Biol Cell 9:2595-2609.
11. Chen XK, Wang LC, Zhou Y, Cai Q, Prakriya M, Duan KL, Sheng ZH, Lingle C, Zhou Z (2005) Activation of GPCRs modulates quantal size in chromaffin cells through G(betagamma) and PKC. Nat Neurosci 8:1160-1168.
12. Chow RH, von Rüden L, Neher E (1992) Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356:60-63.
13. Colliver TL, Pyott SJ, Achalabun M, Ewing AG (2000) VMAT-Mediated changes in quantal size and vesicular volume. J Neurosci 20:5276-5282.
14. Daly C, Ziff EB (2002) Ca2+-dependent formation of a dynamin- synaptophysin complex: potential role in synaptic vesicle endocytosis. J Biol Chem 277:9010-9015.
15. Daly C, Sugimori M, Moreira JE, Ziff EB, Llinás R (2000) Synaptophysin regulates clathrin-independent endocytosis of synaptic vesicles. Proc Natl Acad Sci U S A 97:6120-6125.
16. Elferink LA, Peterson MR, Scheller RH (1993) A role for synaptotagmin (p65) in regulated exocytosis. Cell 72:153-159.
17. Elhamdani A, Palfrey HC, Artalejo CR (2001) Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells. Neuron 31:819-830.
18. Elhamdani A, Azizi F, Solomaha E, Palfrey HC, Artalejo CR (2006) Two mechanistically distinct forms of endocytosis in adrenal chromaffin cells: differential effects of SH3 domains and amphiphysin antagonism. FEBS Lett 580:3263-3269.
19. Fisher RJ, Pevsner J, Burgoyne RD (2001) Control of fusion pore dynamics during exocytosis by Munc18. Science 291:875-878.
20. Fournier S, Novas ML, Trifaró JM (1989) Subcellular distribution of 65,000 calmodulin-binding protein (p65) and synaptophysin (p38) in adrenal medulla. J Neurochem 53:1043-1049.
21. Fulop T, Doreian B, Smith C (2008) Dynamin I plays dual roles in the activity-dependent shift in exocytic mode in mouse adrenal chromaffin cells. Arch Biochem Biophys 477:146-154.
22. Galas MC, Chasserot-Golaz S, Dirrig-Grosch S, Bader MF (2000) Presence of dynamin-syntaxin complexes associated with secretory granules in adrenal chromaffin cells. J Neurochem 75:1511-1519.
23. Gincel D, Shoshan-Barmatz V (2002) The synaptic vesicle protein synaptophysin: purification and characterization of its channel activity. Biophys J 83:3223-3229.
24. Gong LW, Hafez I, Alvarez de Toledo G, Lindau M (2003) Secretory vesicles membrane area is regulated in tandem with quantal size in chromaffin cells. J Neurosci 23:7917-7921.
25. Graham ME, O'Callaghan DW, McMahon HT, Burgoyne RD (2002) Dynamin-dependent and dynamin-independent processes contribute to the regulation of single vesicle release kinetics and quantal size. Proc Natl Acad Sci U S A 99:7124-7129.
26. Jahn R, Schiebler W, Ouimet C, Greengard P (1985) A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci U S A 82:4137-4141.
27. Janz R, Südhof TC, Hammer RE, Unni V, Siegelbaum SA, Bolshakov VY (1999) Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I. Neuron 24:687-700.
28. Kawagoe KT, Zimmerman JB, Wightman RM (1993) Principles of voltammetry and microelectrode surface states. J Neurosci Methods 48:225-240.
29. Knaus P, Betz H (1990) Mapping of a dominant immunogenic region of synaptophysin, a major membrane protein of synaptic vesicles. FEBS Lett 261:358-360.
30. Leube RE, Kaiser P, Seiter A, Zimbelmann R, Franke WW, Rehm H, Knaus P, Prior P, Betz H, Reinke H, Beyreuther K, Wiedenmann B (1987) Synaptophysin: molecular organization and mRNA expression as determined from cloned cDNA. EMBO J 6:3261-3268.
31. Liang YJ, Wu DF, Yang LQ, Höllt V, Koch T (2007) Interaction of the muopioid receptor with synaptophysin influences receptor trafficking and signaling. Mol Pharmacol 71:123-131.
32. Lindau M, Alvarez de Toledo G (2003) The fusion pore. Biochim Biophys Acta 1641:167-173.
33. Linstedt AD, Kelly RB (1991) Synaptophysin is sorted from endocytotic markers in neuroendocrine PC12 cells but not transfected fibroblasts. Neuron 7:309-317.
34. McMahon HT, Bolshakov VY, Janz R, Hammer RE, Siegelbaum SA, Südhof TC (1996) Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release. Proc Natl Acad Sci U S A 93:4760-4764.
35. McNiven MA, Kim L, Krueger EW, Orth JD, Cao H, Wong TW (2000) Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151:187-198.
36. Mitter D, Reisinger C, Hinz B, Hollmann S, Yelamanchili SV, Treiber-Held S, Ohm TG, Herrmann A, Ahnert-Hilger G (2003) The synaptophysin/synaptobrevin interaction critically depends on the cholesterol content. J Neurochem 84:35-42.
37. Montiel C, Mendoza I, García CJ, Awad Y, García-Olivares J, Solís-Garrido LM, Lara H, García AG, Cárdenas AM (2003) Distinct protein kinases regulate SNAP-25 expression in chromaffin cells. J Neurosci Res 71:353-364.
38. Neco P, Fernández-Peruchena C, Navas S, Gutiérrez LM, de Toledo GA, Alés E (2008) Myosin II contributes to fusion pore expansion during exocytosis. J Biol Chem 283:10949-10957.
39. Obendorf D, Schwarzenbrunner U, Fischer-Colbrie R, Laslop A, Winkler H (1988) In adrenal medulla synaptophysin (protein p38) is present in chromaffin vesicles and in a special vesicle population. J Neurochem 51:1573-1580.
40. Okamoto PM, Gamby C, Wells D, Fallon J, Vallee RB (2001) Dynamin isoform-specific interaction with the shank/ProSAP scaffolding proteins of the postsynaptic density and actin cytoskeleton. J Biol Chem 276:48458-48465.
41. Régnier-Vigouroux A, Tooze SA, Huttner WB (1991) Newly synthesized synaptophysin is transported to synaptic-like microvesicles via constitutive secretory vesicles and the plasma membrane. EMBO J 10:3589-35601.
42. Schilling K, Gratzl M (1988) Quantification of p38/synaptophysin in highly purified adrenal medullary chromaffin vesicles. FEBS Lett 233:22-24.
43. Segura F, Brioso MA, Gómez JF, Machado JD, Borges R (2000) Automatic analysis for amperometrical recordings of exocytosis. J Neurosci Methods 103:151-156.
44. Smith AD, Winkler H (1967) A simple method for the isolation of adrenal chromaffin granules on a large scale. Biochem J 103:480-482.
45. Spiwoks-Becker I, Vollrath L, Seeliger MW, Jaissle G, Eshkind LG, Leube RE (2001) Synaptic vesicle alterations in rod photoreceptors of synaptophysin-deficient mice. Neuroscience 107:127-142.
46. Südhof TC, Lottspeich F, Greengard P, Mehl E, Jahn R (1987) A synaptic vesicle protein with a novel cytoplasmic domain and four transmembrane regions. Science 238:1142-1144.
47. Thomas L, Hartung K, Langosch D, Rehm H, Bamberg E, Franke WW, Betz H (1988) Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science 242:1050-1053.
48. Tixier-Vidal A, Faivre-Bauman A, Picart R, Wiedenmann B (1988) Immunoelectron microscopic localization of synaptophysin in a Golgi subcompartment of developing hypothalamic neurons. Neuroscience 26:847-861.
49. Valtorta F, Pennuto M, Bonanomi D, Benfenati F (2004) Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis? Bioessays 26:445-453.
50. Wang R, Hosaka M, Han L, Yokota-Hashimoto H, Suda M, Mitsushima D, Torii S, Takeuchi T (2006) Molecular probes for sensing the cholesterol composition of subcellular organelle membranes. Biochim Biophys Acta 1761:1169-1181.
51. Yin Y, Dayanithi G, Lemos JR (2002) Ca(2+)-regulated, neurosecretory granule channel involved in release from neurohypophysial terminals. J Physiol 539:409-418.
52. 2+ and glycolysis. Brain Res 780:86-94.
53. Zhou Z, Misler S, Chow RH (1996) Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys J 70:1543-1552.