Measurements of the acidification kinetics of single synaptopHluorin vesicles

Biophysical Journal

Volumn 101, Issue 7, 2011, Pages 1580-1589

  Budzinski, Kristi L ^a   Zeigler, Maxwell ^a   Fujimoto, Bryant S ^a   Bajjalieh, Sandra M ^b   Chiu, Daniel T ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CHLORIDE; GLUTAMIC ACID DERIVATIVE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTON; SYNAPTOPHIUORIN;

ANIMAL; ARTICLE; BRAIN; CHEMISTRY; CYTOLOGY; ENDOCYTOSIS; GENETICS; KINETICS; METABOLISM; MOUSE; PERMEABILITY; PH; SPECTROFLUOROMETRY; SYNAPSE VESICLE; TRANSGENE;

ANIMALS; BRAIN; CHLORIDES; ENDOCYTOSIS; GLUTAMATES; GREEN FLUORESCENT PROTEINS; HYDROGEN-ION CONCENTRATION; KINETICS; MICE; NEUROTRANSMITTER AGENTS; PERMEABILITY; PROTONS; RECOMBINANT FUSION PROTEINS; SPECTROMETRY, FLUORESCENCE; SYNAPTIC VESICLES; TRANSGENES;

MUS;

EID: 80053371760     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.08.032     Document Type: Article

References (39)

1. S. Naito, and T. Ueda Characterization of glutamate uptake into synaptic vesicles J. Neurochem. 44 1985 99 109 (Pubitemid 15190740)
2. +-ATPase in rat brain synaptic vesicles. Coupling to L-glutamate transport J. Biol. Chem. 264 1989 8281 8288 (Pubitemid 19137318)
3. H. Wolosker, D.O. de Souza, and L. de Meis Regulation of glutamate transport into synaptic vesicles by chloride and proton gradient J. Biol. Chem. 271 1996 11726 11731 (Pubitemid 26157241)
4. V.P. Whittaker, I.A. Michaelson, and R.J. Kirkland The separation of synaptic vesicles from nerve-ending particles (synaptosomes) Biochem. J. 90 1964 293 303
5. S. Clerc, and Y. Barenholz A quantitative model for using acridine orange as a transmembrane pH gradient probe Anal. Biochem. 259 1998 104 111 (Pubitemid 28247057)
6. G. Miesenböck, D.A. De Angelis, and J.E. Rothman Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins Nature 394 1998 192 195 (Pubitemid 28325974)
7. P.P. Atluri, and T.A. Ryan The kinetics of synaptic vesicle reacidification at hippocampal nerve terminals J. Neurosci. 26 2006 2313 2320 (Pubitemid 44699040)
8. S.P. Gandhi, and C.F. Stevens Three modes of synaptic vesicular recycling revealed by single-vesicle imaging Nature 423 2003 607 613 (Pubitemid 36713215)
9. L. He, and L.G. Wu The debate on the kiss-and-run fusion at synapses Trends Neurosci. 30 2007 447 455 (Pubitemid 47376946)
10. Z.Y. Li, and J. Burrone V.N. Murthy Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin Proc. Natl. Acad. Sci. USA 102 2005 6131 6136 (Pubitemid 40594267)
11. V.K.S. Hsiao, and J.R. Waldeisen T.J. Huang Aminopropyltriethoxysilane (APTES)-functionalized nanoporous polymeric gratings: fabrication and application in biosensing J. Mater. Chem. 17 2007 4896 4901 (Pubitemid 350176535)
12. E.K. Matthews, and J.J. Nordmann The synaptic vesicle: calcium ion binding to the vesicle membrane and its modification by drug action Mol. Pharmacol. 12 1976 778 788
13. S. Jayaraman, and P. Haggie A.S. Verkman Mechanism and cellular applications of a green fluorescent protein-based halide sensor J. Biol. Chem. 275 2000 6047 6050 (Pubitemid 30129883)
14. S. Takamori, and M. Holt R. Jahn Molecular anatomy of a trafficking organelle Cell 127 2006 831 846 (Pubitemid 44716256)
15. S.A. Mutch, and P. Kensel-Hammes D.T. Chiu Protein quantification at the single vesicle level reveals that a subset of synaptic vesicle proteins are trafficked with high precision J. Neurosci. 31 2011 1461 1470
16. L.B. Shi, and K. Fushimi A.S. Verkman Heterogeneity in ATP-dependent acidification in endocytic vesicles from kidney proximal tubule. Measurement of pH in individual endocytic vesicles in a cell-free system Biophys. J. 59 1991 1208 1217
17. F.Y. Wan, Y.N. Wang, and G.J. Zhang Influence of the physical states of membrane surface area and center area on lysosomal proton permeability Arch. Biochem. Biophys. 404 2002 285 292
18. S. Paula, and A.G. Volkov D.W. Deamer Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness Biophys. J. 70 1996 339 348 (Pubitemid 26021472)
19. C.L. Kuyper, and J.S. Kuo D.T. Chiu Proton permeation into single vesicles occurs via a sequential two-step mechanism and is heterogeneous J. Am. Chem. Soc. 128 2006 3233 3240
20. 3- exchangers Am. J. Physiol. 255 1988 C857 C869
21. L. Maresová, and B. Hosková H. Sychrová New applications of pHluorin - measuring intracellular pH of prototrophic yeasts and determining changes in the buffering capacity of strains with affected potassium homeostasis Yeast 27 2010 317 325
22. R.W. Van Dyke, and J.D. Belcher Acidification of three types of liver endocytic vesicles: similarities and differences Am. J. Physiol. 266 1994 C81 C94
23. M. Grabe, and G. Oster Regulation of organelle acidity J. Gen. Physiol. 117 2001 329 344
24. S. Roseth, E.M. Fykse, and F. Fonnum Uptake of L-glutamate into synaptic vesicles: competitive inhibition by dyes with biphenyl and amino- and sulphonic acid-substituted naphthyl groups Biochem. Pharmacol. 56 1998 1243 1249 (Pubitemid 28512676)
25. S. Schenck, and S.M. Wojcik S. Takamori A chloride conductance in VGLUT1 underlies maximal glutamate loading into synaptic vesicles Nat. Neurosci. 12 2009 156 162
26. R.W. Van Dyke Proton pump-generated electrochemical gradients in rat liver multivesicular bodies. Quantitation and effects of chloride J. Biol. Chem. 263 1988 2603 2611 (Pubitemid 18062898)
27. J.S. Tabb, and P.E. Kish T. Ueda Glutamate transport into synaptic vesicles. Roles of membrane potential, pH gradient, and intravesicular pH J. Biol. Chem. 267 1992 15412 15418
28. M. Grabe, H.Y. Wang, and G. Oster The mechanochemistry of V-ATPase proton pumps Biophys. J. 78 2000 2798 2813 (Pubitemid 30396915)
29. N. Nelson, A. Sacher, and H. Nelson The significance of molecular slips in transport systems Nat. Rev. Mol. Cell Biol. 3 2002 876 881 (Pubitemid 35285278)
30. P.R. Maycox, and T. Deckwerth R. Jahn Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes J. Biol. Chem. 263 1988 15423 15428
31. S. Roseth, E.M. Fykse, and F. Fonnum Uptake of L-glutamate into rat brain synaptic vesicles: effect of inhibitors that bind specifically to the glutamate transporter J. Neurochem. 65 1995 96 103
32. Y. Moriyama, and N. Nelson Internal anion binding site and membrane potential dominate the regulation of proton pumping by the chromaffin granule ATPase Biochem. Biophys. Res. Commun. 149 1987 140 144
33. J. Hartinger, and R. Jahn An anion binding site that regulates the glutamate transporter of synaptic vesicles J. Biol. Chem. 268 1993 23122 23127 (Pubitemid 23328022)
34. R.H. Edwards The neurotransmitter cycle and quantal size Neuron 55 2007 835 858 (Pubitemid 47391194)
35. G.D. Price, and L.O. Trussell Estimate of the chloride concentration in a central glutamatergic terminal: a gramicidin perforated-patch study on the calyx of Held J. Neurosci. 26 2006 11432 11436 (Pubitemid 44772173)
36. I. Mellman The importance of being acid: the role of acidification in intracellular membrane traffic J. Exp. Biol. 172 1992 39 45
37. G.-H. Sun-Wada, Y. Wada, and M. Futai Diverse and essential roles of mammalian vacuolar-type proton pump ATPase: toward the physiological understanding of inside acidic compartments Biochim. Biophys. Acta Bioenergetics 1658 2004 106 114 (Pubitemid 39013240)
38. V. Marshansky The V-ATPase a2-subunit as a putative endosomal pH-sensor Biochem. Soc. Trans. 35 2007 1092 1099 (Pubitemid 350206437)
39. K.L. Budzinski, and R.W. Allen D.T. Chiu Large structural change in isolated synaptic vesicles upon loading with neurotransmitter Biophys. J. 97 2009 2577 2584