Molecular Anatomy of a Trafficking Organelle

Cell

Volumn 127, Issue 4, 2006, Pages 831-846

  Takamori, Shigeo ^a   Holt, Matthew ^a   Stenius, Katinka ^b   Lemke, Edward A ^a   Grønborg, Mads ^a   Riedel, Dietmar ^a   Urlaub, Henning ^a   Schenck, Stephan ^a   Brügger, Britta ^c   Ringler, Philippe ^d   Müller, Shirley A ^d   Rammner, Burkhard ^e   Gräter, Frauke ^a   Hub, Jochen S ^a   De Groot, Bert L ^a   Mieskes, Gottfried ^a   Moriyama, Yoshinori ^f   Klingauf, Jürgen ^a   Grubmüller, Helmut ^a   Heuser, John ^g   Wieland, Felix ^c   Jahn, Reinhard ^a   more..

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF BASEL   (Switzerland)

^e Scimotion   (Germany)

^f OKAYAMA UNIVERSITY   (Japan)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; LIPID; PROTEIN;

ARTICLE; CALCULATION; CELL ORGANELLE; DENSITY; LIPID COMPOSITION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; SYNAPSE VESICLE; TRANSPORT VESICLE;

EUKARYOTA;

EID: 33750805030     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.10.030     Document Type: Article

References (63)

1. Ahnert-Hilger G., Höltje M., Pahner I., Winter S., and Brunk I. Regulation of vesicular neurotransmitter transporters. Rev. Physiol. Biochem. Pharmacol. 150 (2003) 140-160
2. Antonin W., Riedel D., and Fischer von Mollard G. The SNARE Vti1a-beta is localized to small synaptic vesicles and participates in a novel SNARE complex. J. Neurosci. 20 (2000) 5724-5732
3. Benfenati F., Greengard P., Brunner J., and Bähler M. Electrostatic and hydrophobic interactions of synapsin I and synapsin I fragments with phospholipid bilayers. J. Cell Biol. 108 (1989) 1851-1862
4. Bennett M.K., Calakos N., Kreiner T., and Scheller R.H. Synaptic vesicle membrane proteins interact to form a multimeric complex. J. Cell Biol. 116 (1992) 761-775
5. Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., and Hermans J. Interaction models for water in relation to protein hydration. In: Pullman B. (Ed). Intermolecular Forces (1981), D. Riedel Publishing Company, Dordrecht, The Netherlands 331-342
6. Blondeau F., Ritter B., Allaire P.D., Wasiak S., Girard M., Hussain N.K., Angers A., Legendre-Guillemin V., Roy L., Boismenu D., et al. Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. USA 101 (2004) 3833-3838
7. Bock J.B., Matern H.T., Peden A.A., and Scheller R.H. A genomic perspective on membrane compartment organization. Nature 409 (2001) 839-841
8. Bonifacino J.S., and Glick B.S. The mechanisms of vesicle budding and fusion. Cell 116 (2004) 153-166
9. Bradford M.M. A rapid and sensitve method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
10. Brisson A., and Unwin P.N. Tubular crystals of acetylcholine receptor. J. Cell Biol. 99 (1984) 1202-1211
11. Brügger B., Erben G., Sandhoff R., Wieland F.T., and Lehmann W.D. Quantitative analysis of biological membrane lipids at the low picomole level by nano electrospray ionization tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 94 (1997) 2339-2344
12. Brügger B., Sandhoff R., Wegehingel S., Gorgas K., Malsam J., Helms J.B., Lehmann W.D., Nickel W., and Wieland F.T. Evidence for segregation of sphingomyelin and cholesterol during formation of COPI-coated vesicles. J. Cell Biol. 151 (2000) 507-518
13. Chapman E.R., and Jahn R. Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes. Autonomous function of a single C2-homologous domain. J. Biol. Chem. 269 (1994) 5735-5741
14. Daniels R.W., Collins C.A., Chen K., Gelfand M.V., Featherstone D.E., and DiAntonio A. A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle. Neuron 49 (2006) 11-16
15. de Hoop M.J., Huber L.A., Stenmark H., Williamson E., Zerial M., Parton R.G., and Dotti C.G. The involvement of the small GTP-binding protein Rab5a in neuronal endocytosis. Neuron 13 (1994) 11-22
16. Elias J.E., Haas W., Faherty B.K., and Gygi S.P. Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2 (2005) 667-675
17. Engel A. Molecular weight determination by scanning transmission electron microscopy. Ultramicroscopy 3 (1978) 273-281
18. Fischer von Mollard G., Stahl B., Khokhlatchev A., Südhof T.C., and Jahn R. Rab3C is a synaptic vesicle protein that dissociates from synaptic vesicles after stimulation of exocytosis. J. Biol. Chem. 269 (1994) 10971-10974
19. Fischer von Mollard G., Stahl B., Walch-Solimena C., Takei K., Daniels L., Khoklatchev A., De Camilli P., Südhof T.C., and Jahn R. Localization of Rab5 to synaptic vesicles identifies endosomal intermediate in synaptic vesicle recycling pathway. Eur. J. Cell Biol. 65 (1994) 319-326
20. Fremeau Jr. R.T., Troyer M.D., Pahner I., Nygaard G.O., Tran C.H., Reimer R.J., Bellocchio E.E., Fortin D., Storm-Mathisen J., and Edwards R.H. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31 (2001) 247-260
21. Goelz S.E., Nestler E.J., Chehrazi B., and Greengard P. Distribution of protein I in mammalian brain as determined by a detergent-based radioimmunoassay. Proc. Natl. Acad. Sci. USA 78 (1981) 2130-2134
22. Harlow M.L., Ress D., Stoschek A., Marshall R.M., and McMahan U.J. The architecture of active zone material at the frog's neuromuscular junction. Nature 409 (2001) 479-484
23. Harris K.M., and Sultan P. Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology 34 (1995) 1387-1395
24. Hartinger J., Stenius K., Hogemann D., and Jahn R. 16-BAC/SDS-PAGE: A two-dimensional gel electrophoresis system suitable for the separation of integral membrane proteins. Anal. Biochem. 240 (1996) 126-133
25. Heuser J. Protocol for 3-D visualization of molecules on mica via the quick-freeze, deep-etch technique. J. Electron Microsc. Tech. 13 (1989) 244-263
26. Holt M., Varoqueaux F., Wiederhold K., Takamori S., Urlaub H., Fasshauer D., and Jahn R. Identification of SNAP-47, a novel Qbc-snare with ubiquitous expression. J. Biol. Chem. 281 (2006) 17076-17083
27. Huttner W.B., Schiebler W., Greengard P., and De Camilli P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96 (1983) 1374-1388
28. Jahn R., and Südhof T.C. Synaptic vesicles and exocytosis. Annu. Rev. Neurosci. 17 (1994) 219-246
29. Jahn R., Schiebler W., and Greengard P. A quantitative dot-immunobinding assay for proteins using nitrocellulose membrane filters. Proc. Natl. Acad. Sci. USA 81 (1984) 1684-1687
30. Janz R., Hofmann K., and Sudhof T.C. SVOP, an evolutionarily conserved synaptic vesicle protein, suggests novel transport functions of synaptic vesicles. J. Neurosci. 18 (1998) 9269-9281
31. 2+-regulated versus constitutive exocytosis. J. Neurosci. 23 (2003) 10531-10539
32. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
33. Lin R.C., and Scheller R.H. Mechanisms of synaptic vesicle exocytosis. Annu. Rev. Cell Dev. Biol. 16 (2000) 19-49
34. Littleton J.T., Chapman E.R., Kreber R., Garment M.B., Carlson S.D., and Ganetzky B. Temperature-sensitive paralytic mutations demonstrate that synaptic exocytosis requires SNARE complex assembly and disassembly. Neuron 21 (1998) 401-413
35. Magde D., Elson E., and Webb W.W. Thermodynamic fluctuations in a reacting System - Measurement by Fluorescence Correlation Spectroscopy. Phys. Rev. Lett. 29 (1972) 705-708
36. Maycox P.R., Link E., Reetz A., Morris S.A., and Jahn R. Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118 (1992) 1379-1388
37. Morciano M., Burre J., Corvey C., Karas M., Zimmermann H., and Volknandt W. Immunoisolation of two synaptic vesicle pools from synaptosomes: a proteomics analysis. J. Neurochem. 95 (2005) 1732-1745
38. Moriyama Y., and Nelson N. Cold inactivation of vacuolar proton-ATPases. J. Biol. Chem. 264 (1989) 3577-3582
39. Muller J.D., Chen Y., and Gratton E. Fluorescence correlation spectroscopy. Methods Enzymol. 361 (2003) 69-92
40. Müller S.A., Goldie K.N., Bürki R., Häring R., and Engel A. Factors influencing the precision of quantitative scanning transmission electron microscopy. Ultramicroscopy 46 (1992) 317-334
41. Nagle J.F., and Tristram-Nagle S. Structure of lipid bilayers. Biochim. Biophys. Acta 1469 (2000) 159-195
42. Nagy A., Baker R.R., Morris S.J., and Whittaker V.P. The preparation and characterization of synaptic vesicles of high purity. Brain Res. 109 (1976) 285-309
43. Navone F., Jahn R., Di Gioia G., Stukenbrok H., Greengard P., and De Camilli P. Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J. Cell Biol. 103 (1986) 2511-2527
44. Peters R. Optical single transporter recording: transport kinetics in microarrays of membrane patches. Annu. Rev. Biophys. Biomol. Struct. 32 (2003) 47-67
45. Peterson G.L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83 (1977) 346-356
46. Pfeffer S., and Aivazian D. Targeting Rab GTPases to distinct membrane compartments. Nat. Rev. Mol. Cell Biol. 5 (2004) 886-896
47. Pothos E.N., Larsen K.E., Krantz D.E., Liu Y., Haycock J.W., Setlik W., Gershon M.D., Edwards R.H., and Sulzer D. Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J. Neurosci. 20 (2000) 7297-7306
48. Reigada D., Diez-Perez I., Gorostiza P., Verdaguer A., Gomez de Aranda I., Pineda O., Vilarrasa J., Marsal J., Blasi J., Aleu J., and Solsona C. Control of neurotransmitter release by an internal gel matrix in synaptic vesicles. Proc. Natl. Acad. Sci. USA 100 (2003) 3485-3490
49. Ritchie K., Shan X.Y., Kondo J., Iwasawa K., Fujiwara T., and Kusumi A. Detection of non-brownian diffusion in the cell membrane in single molecule tracking. Biophys. J. 88 (2005) 2266-2277
50. Schlüter O.M., Khvotchev M., Jahn R., and Südhof T.C. Localization versus function of Rab3 proteins. Evidence for a common regulatory role in controlling fusion. J. Biol. Chem. 277 (2002) 40919-40929
51. Schuette C.G., Hatsuzawa K., Margittai M., Stein A., Riedel D., Küster P., König M., Seidel C., and Jahn R. Determinants of liposome fusion mediated by synaptic SNARE proteins. Proc. Natl. Acad. Sci. USA 101 (2004) 2858-2863
52. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68 (1996) 850-858
53. Singer S.J., and Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science 175 (1972) 720-731
54. Stadler H., and Tsukita S. Synaptic vesicles contain an ATP-dependent proton pump and show 'knob-like' protrusions on their surface. EMBO J. 3 (1984) 3333-3337
55. Stobrawa S.M., Breiderhoff T., Takamori S., Engel D., Schweizer M., Zdebik A.A., Bosl M.R., Ruether K., Jahn H., Draguhn A., et al. Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29 (2001) 185-196
56. Südhof T.C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27 (2004) 509-547
57. Takamori S., Rhee J.S., Rosenmund C., and Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407 (2000) 189-194
58. Takamori S., Riedel D., and Jahn R. Immunoisolation of GABA-specific synaptic vesicles defines a functionally distinct subset of synaptic vesicles. J. Neurosci. 20 (2000) 4904-4911
59. Takamori S., Rhee J.S., Rosenmund C., and Jahn R. Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J. Neurosci. 21 (2001) RC182
60. Walch-Solimena C., Blasi J., Edelmann L., Chapman E.R., Fischer von Mollard G., and Jahn R. The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J. Cell Biol. 128 (1995) 637-645
61. Wilkens S., Zhang Z., and Zheng Y. A structural model of the vacuolar ATPase from transmission electron microscopy. Micron 36 (2005) 109-126
62. Williams J. How does a vesicle know it is full?. Neuron 18 (1997) 683-686
63. Wojcik S.M., Rhee J.S., Herzog E., Sigler A., Jahn R., Takamori S., Brose N., and Rosenmund C. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc. Natl. Acad. Sci. USA 101 (2004) 7158-7163