The V-ATPase membrane domain is a sensor of granular ph that controls the exocytotic machinery

Journal of Cell Biology

Volumn 203, Issue 2, 2013, Pages 283-298

  Poëa Guyon, Sandrine ^a   Ammar, Mohamed Raafet ^b   Erard, Marie ^c   Amar, Muriel ^a   Moreau, Alexandre W ^d   Fossier, Philippe ^a   Gleize, Vincent ^a,e   Vitale, Nicolas ^b   Morel, Nicolas ^a  

^a CNRS   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITÉ PARIS SUD   (France)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CATECHOLAMINE; CELL MEMBRANE PROTEIN; NEUROTRANSMITTER;

ACIDITY; AMPEROMETRIC BIOSENSOR; AMPEROMETRY; ANIMAL CELL; ARTICLE; CATECHOLAMINE RELEASE; CELL FUSION; CELL KINETICS; CELL MEMBRANE DEPOLARIZATION; CELL PH; CELL VACUOLE; CHROMAFFIN CELL; CONTROLLED STUDY; DISSOCIATION CONSTANT; EMBRYO; ENZYME ACTIVITY; ENZYME INACTIVATION; EXOCYTOSIS; GRANULAR CELL; HUMAN; HUMAN CELL; ILLUMINATION; INTRACELLULAR MEMBRANE; MOUSE; NERVE CELL; NERVE CELL CULTURE; NEUROTRANSMITTER RELEASE; NONHUMAN; PC12 CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT; SECRETORY GRANULE; SECRETORY VESICLE; SENSOR; SPIKE; SYNAPTIC TRANSMISSION;

ANIMALS; CATECHOLAMINES; CATTLE; CHROMAFFIN CELLS; EXOCYTOSIS; HYDROGEN-ION CONCENTRATION; KINETICS; LIGHT; MEMBRANE FUSION; MICE; NEURONS; PC12 CELLS; PROTEIN STRUCTURE, TERTIARY; RATS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SECRETORY VESICLES; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TRANSFECTION; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84887531850     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201303104     Document Type: Article

References (67)

1. Adams, S.R., and R.Y. Tsien. 2008. Preparation of the membrane-permeant biarsenicals FlAsH-EDT2 and ReAsH-EDT2 for fluorescent labeling of tetracysteine-tagged proteins. Nat. Protoc. 3:1527-1534. http://dx.doi.org/10.1038/nprot.2008.144
2. Aikawa, Y., and T.F. Martin. 2003. ARF6 regulates a plasma membrane pool of phosphatidylinositol(4,5)bisphosphate required for regulated exocytosis. J. Cell Biol. 162:647-659. http://dx.doi.org/10.1083/jcb.200212142
3. Albillos, A., G. Dernick, H. Horstmann, W. Almers, G. Alvarez de Toledo, and M. Lindau. 1997. The exocytotic event in chromaffin cells revealed by patch amperometry. Nature. 389:509-512. http://dx.doi.org/10.1038/39081
4. Bader, M.F., and N. Vitale. 2009. Phospholipase D in calcium-regulated exocytosis: lessons from chromaffin cells. Biochim. Biophys. Acta. 1791:936-941. http://dx.doi.org/10.1016/j.bbalip.2009.02.016
5. Barg, S., P. Huang, L. Eliasson, D.J. Nelson, S. Obermüller, P. Rorsman, F. Thévenod, and E. Renström. 2001. Priming of insulin granules for exocytosis by granular Cl(-) uptake and acidification. J. Cell Sci. 114: 2145-2154.
6. Béglé, A., P. Tryoen-Tóth, J. de Barry, M.F. Bader, and N. Vitale. 2009. ARF6 regulates the synthesis of fusogenic lipids for calcium-regulated exocytosis in neuroendocrine cells. J. Biol. Chem. 284:4836-4845. http://dx.doi.org/10.1074/jbc. M806894200
7. Bowman, B.J., M.E. McCall, R. Baertsch, and E.J. Bowman. 2006. A model for the proteolipid ring and bafilomycin/concanamycin-binding site in the vacuolar ATPase of Neurospora crassa. J. Biol. Chem. 281:31885-31893. http://dx.doi.org/10.1074/jbc. M605532200
8. Bruns, D., D. Riedel, J. Klingauf, and R. Jahn. 2000. Quantal release of serotonin. Neuron. 28:205-220. http://dx.doi.org/10.1016/S0896-6273(00)00097-0
9. Camacho, M., J.D. Machado, M.S. Montesinos, M. Criado, and R. Borges. 2006. Intragranular pH rapidly modulates exocytosis in adrenal chromaffin cells. J. Neurochem. 96:324-334. http://dx.doi.org/10.1111/j.1471-4159.2005.03526.x
10. Cavelier, P., and D. Attwell. 2007. Neurotransmitter depletion by bafilomycin is promoted by vesicle turnover. Neurosci. Lett. 412:95-100. http://dx.doi.org/10.1016/j.neulet.2006.10.040
11. Chasserot-Golaz, S., N. Vitale, E. Umbrecht-Jenck, D. Knight, V. Gerke, and M.F. Bader. 2005. Annexin 2 promotes the formation of lipid microdomains required for calcium-regulated exocytosis of dense-core vesicles. Mol. Biol. Cell. 16:1108-1119. http://dx.doi.org/10.1091/mbc. E04-07-0627
12. Cousin, M.A., and D.G. Nicholls. 1997. Synaptic vesicle recycling in cultured cerebellar granule cells: role of vesicular acidification and refilling. J. Neurochem. 69:1927-1935. http://dx.doi.org/10.1046/j.1471-4159.1997.69051927.x
13. Di Giovanni, J., S. Boudkkazi, S. Mochida, A. Bialowas, N. Samari, C. Lévêque, F. Youssouf, A. Brechet, C. Iborra, Y. Maulet, et al. 2010. V-ATPase membrane sector associates with synaptobrevin to modulate neurotransmitter release. Neuron. 67:268-279. http://dx.doi.org/10.1016/j.neuron.2010.06.024
14. Edwards, R.H. 2007. The neurotransmitter cycle and quantal size. Neuron. 55:835-858. http://dx.doi.org/10.1016/j.neuron.2007.09.001
15. El Far, O., and M. Seagar. 2011. A role for V-ATPase subunits in synaptic vesicle fusion? J. Neurochem. 117:603-612.
16. Erard, M., A. Fredj, H. Pasquier, D.B. Beltolngar, Y. Bousmah, V. Derrien, P. Vincent, and F. Merola. 2013. Minimum set of mutations needed to optimize cyan fluorescent proteins for live cell imaging. Mol. Biosyst. 9:258-267. http://dx.doi.org/10.1039/c2mb25303h
17. Forgac, M. 2007. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8:917-929. http://dx.doi.org/10.1038/nrm2272
18. Füldner, H.H., and H. Stadler. 1982. 31P-NMR analysis of synaptic vesicles. Status of ATP and internal pH. Eur. J. Biochem. 121:519-524. http://dx.doi.org/10.1111/j.1432-1033.1982.tb05817.x
19. Galli, T., P.S. McPherson, and P. De Camilli. 1996. The V0 sector of the VATPase, synaptobrevin, and synaptophysin are associated on synaptic vesicles in a Triton X-100-resistant, freeze-thawing sensitive, complex. J. Biol. Chem. 271:2193-2198. http://dx.doi.org/10.1074/jbc.271.4.2193
20. Goslin, K., H. Asmussen, and G. Banker. 1998. Rat hippocampal neurons in lowdensity culture. In Culturing Nerve Cells. Second edition. G. Banker and K. Goslin, editors. MIT Press, Cambridge, MA. 339-370.
21. Hicks, B.W., and S.M. Parsons. 1992. Characterization of the P-type and V-type ATPases of cholinergic synaptic vesicles and coupling of nucleotide hydrolysis to acetylcholine transport. J. Neurochem. 58:1211-1220. http://dx.doi.org/10.1111/j.1471-4159.1992.tb11331.x
22. Hiesinger, P.R., A. Fayyazuddin, S.Q. Mehta, T. Rosenmund, K.L. Schulze, R.G. Zhai, P. Verstreken, Y. Cao, Y. Zhou, J. Kunz, and H.J. Bellen. 2005. The v-ATPase V0 subunit a1 is required for a late step in synaptic vesicle exocytosis in Drosophila. Cell. 121:607-620. http://dx.doi.org/10.1016/j.cell.2005.03.012
23. Hong, S.J. 2001. Reduction of quantal size and inhibition of neuromuscular transmission by bafilomycin A. Neuropharmacology. 41:609-617. http://dx.doi.org/10.1016/S0028-3908(01)00104-6
24. Hosokawa, H., P.V. Dip, M. Merkulova, A. Bakulina, Z. Zhuang, A. Khatri, X. Jian, S.M. Keating, S.A. Bueler, J.L. Rubinstein, et al. 2013. The Ntermini of a-subunit isoforms are involved in signaling between vacuolar H+-ATPase (V-ATPase) and cytohesin-2. J. Biol. Chem. 288:5896-5913. http://dx.doi.org/10.1074/jbc. M112.409169
25. Hurtado-Lorenzo, A., M. Skinner, J. El Annan, M. Futai, G.H. Sun-Wada, S. Bourgoin, J. Casanova, A. Wildeman, S. Bechoua, D.A. Ausiello, et al. 2006. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat. Cell Biol. 8:124-136. http://dx.doi.org/10.1038/ncb1348
26. Israël, M., N. Morel, B. Lesbats, S. Birman, and R. Manaranche. 1986. Purification of a presynaptic membrane protein that mediates a calciumdependent translocation of acetylcholine. Proc. Natl. Acad. Sci. USA. 83:9226-9230. http://dx.doi.org/10.1073/pnas.83.23.9226
27. Jacobson, K., Z. Rajfur, E. Vitriol, and K. Hahn. 2008. Chromophore-assisted laser inactivation in cell biology. Trends Cell Biol. 18:443-450. http://dx.doi.org/10.1016/j.tcb.2008.07.001
28. Jahn, R., and D. Fasshauer. 2012. Molecular machines governing exocytosis of synaptic vesicles. Nature. 490:201-207. http://dx.doi.org/10.1038/nature11320
29. Johnson, R.G., and A. Scarpa. 1976. Internal pH of isolated chromaffin vesicles. J. Biol. Chem. 251:2189-2191.
30. Kuijpers, G.A., L.M. Rosario, and R.L. Ornberg. 1989. Role of intracellular pH in secretion from adrenal medulla chromaffin cells. J. Biol. Chem. 264:698-705.
31. Liégeois, S., A. Benedetto, J.M. Garnier, Y. Schwab, and M. Labouesse. 2006. The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol. 173:949-961. http://dx.doi.org/10.1083/jcb.200511072
32. Lindgren, C.A., D.G. Emery, and P.G. Haydon. 1997. Intracellular acidification reversibly reduces endocytosis at the neuromuscular junction. J. Neurosci. 17:3074-3084.
33. Marek, K.W., and G.W. Davis. 2002. Transgenically encoded protein photoinactivation (FlAsH-FALI): acute inactivation of synaptotagmin I. Neuron. 36:805-813. http://dx.doi.org/10.1016/S0896-6273(02)01068-1
34. Martin, B.R., B.N. Giepmans, S.R. Adams, and R.Y. Tsien. 2005. Mammalian cell-based optimization of the biarsenical-binding tetracysteine motif for improved fluorescence and affinity. Nat. Biotechnol. 23:1308-1314. http://dx.doi.org/10.1038/nbt1136
35. Michaelson, D.M., and I. Angel. 1980. Determination of delta pH in cholinergic synaptic vesicles: its effect on storage and release of acetylcholine. Life Sci. 27:39-44. http://dx.doi.org/10.1016/0024-3205(80)90017-X
36. Morel, N. 2003. Neurotransmitter release: the dark side of the vacuolar-H+ATPase. Biol. Cell. 95:453-457. http://dx.doi.org/10.1016/S0248-4900(03)00075-3
37. Morel, N., V. Gérard, and G. Shiff. 1998. Vacuolar H+-ATPase domains are transported separately in axons and assemble in Torpedo nerve endings. J. Neurochem. 71:1702-1708. http://dx.doi.org/10.1046/j.1471-4159.1998.71041702.x
38. Morel, N., Y. Dunant, and M. Israël. 2001. Neurotransmitter release through the V0 sector of V-ATPase. J. Neurochem. 79:485-488. http://dx.doi.org/10.1046/j.1471-4159.2001.00611.x
39. Morel, N., J.C. Dedieu, and J.M. Philippe. 2003. Specific sorting of the a1 isoform of the V-H+ATPase a subunit to nerve terminals where it associates with both synaptic vesicles and the presynapticplasma membrane. J. Cell Sci. 116:4751-4762. http://dx.doi.org/10.1242/jcs.00791
40. Oot, R.A., and S. Wilkens. 2012. Subunit interactions at the V1-Vo interface in yeast vacuolar ATPase. J. Biol. Chem. 287:13396-13406. http://dx.doi.org/10.1074/jbc. M112.343962
41. Oot, R.A., L.S. Huang, E.A. Berry, and S. Wilkens. 2012. Crystal structure of the yeast vacuolar ATPase heterotrimeric EGC(head) peripheral stalk complex. Structure. 20:1881-1892. http://dx.doi.org/10.1016/j.str.2012.08.020
42. Peri, F., and C. Nüsslein-Volhard. 2008. Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell. 133:916-927. http://dx.doi.org/10.1016/j.cell.2008.04.037
43. Peters, C., M.J. Bayer, S. Bühler, J.S. Andersen, M. Mann, and A. Mayer. 2001. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature. 409:581-588. http://dx.doi.org/10.1038/35054500
44. Poëa-Guyon, S., M. Amar, P. Fossier, and N. Morel. 2006. Alternative splicing controls neuronal expression of v-ATPase subunit a1 and sorting to nerve terminals. J. Biol. Chem. 281:17164-17172. http://dx.doi.org/10.1074/jbc. M600927200
45. Poëa-Guyon, S., H. Pasquier, F. Mérola, N. Morel, and M. Erard. 2013. The enhanced cyan fluorescent protein: a sensitive pH sensor for fluorescence lifetime imaging. Anal. Bioanal. Chem. 405:3983-3987. http://dx.doi.org/10.1007/s00216-013-6860-y
46. Pollard, H.B., H. Shindo, C.E. Creutz, C.J. Pazoles, and J.S. Cohen. 1979. Internal pH and state of ATP in adrenergic chromaffin granules determined by 31P nuclear magnetic resonance spectroscopy. J. Biol. Chem. 254:1170-1177.
47. Rizo, J., and C. Rosenmund. 2008. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15:665-674. http://dx.doi.org/10.1038/nsmb.1450
48. Saw, N.M., S.Y. Kang, L. Parsaud, G.A. Han, T. Jiang, K. Grzegorczyk, M. Surkont, G.H. Sun-Wada, Y. Wada, L. Li, and S. Sugita. 2011. Vacuolar H(+)-ATPase subunits Voa1 and Voa2 cooperatively regulate secretory vesicle acidification, transmitter uptake, and storage. Mol. Biol. Cell. 22:3394-3409. http://dx.doi.org/10.1091/mbc. E11-02-0155
49. Segura, F., M.A. Brioso, J.F. Gómez, J.D. Machado, and R. Borges. 2000. Automatic analysis for amperometrical recordings of exocytosis. J. Neurosci. Methods. 103:151-156. http://dx.doi.org/10.1016/S0165-0270(00)00309-5
50. Shao, E., and M. Forgac. 2004. Involvement of the nonhomologous region of subunit A of the yeast V-ATPase in coupling and in vivo dissociation. J. Biol. Chem. 279:48663-48670. http://dx.doi.org/10.1074/jbc. M408278200
51. Smardon, A.M., and P.M. Kane. 2007. RAVE is essential for the efficient assembly of the C subunit with the vacuolar H(+)-ATPase. J. Biol. Chem. 282:26185-26194. http://dx.doi.org/10.1074/jbc. M703627200
52. Stewart, A.G., and D. Stock. 2012. Priming a molecular motor for disassembly. Structure. 20:1799-1800. http://dx.doi.org/10.1016/j.str.2012.10.003
53. Strasser, B., J. Iwaszkiewicz, O. Michielin, and A. Mayer. 2011. The V-ATPase proteolipid cylinder promotes the lipid-mixing stage of SNARE-dependent fusion of yeast vacuoles. EMBO J. 30:4126-4141. http://dx.doi.org/10.1038/emboj.2011.335
54. Tabares, L., E. Alés, M. Lindau, and G. Alvarez de Toledo. 2001. Exocytosis of catecholamine (CA)-containing and CA-free granules in chromaffin cells. J. Biol. Chem. 276:39974-39979. http://dx.doi.org/10.1074/jbc. M106498200
55. Takamori, S., M. Holt, K. Stenius, E.A. Lemke, M. Grønborg, D. Riedel, H. Urlaub, S. Schenck, B. Brügger, P. Ringler, et al. 2006. Molecular anatomy of a trafficking organelle. Cell. 127:831-846. http://dx.doi.org/10.1016/j.cell.2006.10.030
56. Taupenot, L., K.L. Harper, and D.T. O'Connor. 2005. Role of H+-ATPasemediated acidification in sorting and release of the regulated secretory protein chromogranin A: evidence for a vesiculogenic function. J. Biol. Chem. 280:3885-3897. http://dx.doi.org/10.1074/jbc. M408197200
57. Thomas, P., J.G. Wong, A.K. Lee, and W. Almers. 1993. A low affinity Ca2+ receptor controls the final steps in peptide secretion from pituitary melanotrophs. Neuron. 11:93-104. http://dx.doi.org/10.1016/0896-6273(93)90274-U
58. Toei, M., R. Saum, and M. Forgac. 2010. Regulation and isoform function of the V-ATPases. Biochemistry. 49:4715-4723. http://dx.doi.org/10.1021/bi100397s
59. Tour, O., R.M. Meijer, D.A. Zacharias, S.R. Adams, and R.Y. Tsien. 2003. Genetically targeted chromophore-assisted light inactivation. Nat. Biotechnol. 21:1505-1508. http://dx.doi.org/10.1038/nbt914
60. Ungermann, C., W. Wickner, and Z. Xu. 1999. Vacuole acidification is required for trans-SNARE pairing, LMA1 release, and homotypic fusion. Proc. Natl. Acad. Sci. USA. 96:11194-11199. http://dx.doi.org/10.1073/pnas.96.20.11194
61. Vitale, N., H. Mukai, B. Rouot, D. Thiersé, D. Aunis, and M.F. Bader. 1993. Exocytosis in chromaffin cells. Possible involvement of the heterotrimeric GTP-binding protein G(o). J. Biol. Chem. 268:14715-14723.
62. Vitale, N., A.S. Caumont, S. Chasserot-Golaz, G. Du, S. Wu, V.A. Sciorra, A.J. Morris, M.A. Frohman, and M.F. Bader. 2001. Phospholipase D1: a key factor for the exocytotic machinery in neuroendocrine cells. EMBO J. 20:2424-2434. http://dx.doi.org/10.1093/emboj/20.10.2424
63. Vitale, N., S. Chasserot-Golaz, Y. Bailly, N. Morinaga, M.A. Frohman, and M.F. Bader. 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. http://dx.doi.org/10.1083/jcb.200203027
64. Wickner, W., and R. Schekman. 2008. Membrane fusion. Nat. Struct. Mol. Biol. 15:658-664. http://dx.doi.org/10.1038/nsmb.1451
65. Williamson, W.R., D. Wang, A.S. Haberman, and P.R. Hiesinger. 2010. A dual function of V0-ATPase a1 provides an endolysosomal degradation mechanism in Drosophila melanogaster photoreceptors. J. Cell Biol. 189:885-899. http://dx.doi.org/10.1083/jcb.201003062
66. Xie, X.S., D. Padron, X. Liao, J. Wang, M.G. Roth, and J.K. De Brabander. 2004. Salicylihalamide A inhibits the V0 sector of the V-ATPase through a mechanism distinct from bafilomycin A1. J. Biol. Chem. 279:19755-19763. http://dx.doi.org/10.1074/jbc. M313796200
67. Yan, P., Y. Xiong, B. Chen, S. Negash, T.C. Squier, and M.U. Mayer. 2006. Fluorophore-assisted light inactivation of calmodulin involves singletoxygen mediated cross-linking and methionine oxidation. Biochemistry. 45:4736-4748. http://dx.doi.org/10.1021/bi052395a