Regulation of the mammalian-brain V-ATPase through ultraslow mode-switching.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
received:
13
01
2022
accepted:
21
10
2022
entrez:
23
11
2022
pubmed:
24
11
2022
medline:
26
11
2022
Statut:
ppublish
Résumé
Vacuolar-type adenosine triphosphatases (V-ATPases)
Identifiants
pubmed: 36418452
doi: 10.1038/s41586-022-05472-9
pii: 10.1038/s41586-022-05472-9
doi:
Substances chimiques
Adenosine Triphosphate
8L70Q75FXE
Protons
0
Vacuolar Proton-Translocating ATPases
EC 3.6.1.-
Neurotransmitter Agents
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
827-834Subventions
Organisme : NIA NIH HHS
ID : R01 AG057342
Pays : United States
Organisme : European Research Council
Pays : International
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Vasanthakumar, T. & Rubinstein, J. L. Structure and roles of V-type ATPases. Trends Biochem. Sci. 45, 295–307 (2020).
doi: 10.1016/j.tibs.2019.12.007
Ueno, H., Suzuki, K. & Murata, T. Structure and dynamics of rotary V1 motor. Cell. Mol. Life Sci. 75, 1789–1802 (2018).
doi: 10.1007/s00018-018-2758-3
Forgac, M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8, 917–929 (2007).
doi: 10.1038/nrm2272
Spikes, T. E., Montgomery, M. G. & Walker, J. E. Structure of the dimeric ATP synthase from bovine mitochondria. Proc. Natl Acad. Sci. USA 117, 23519–23526 (2020).
doi: 10.1073/pnas.2013998117
Okuno, D., Iino, R. & Noji, H. Rotation and structure of FoF1-ATP synthase. J. Biochem. 149, 655–664 (2011).
doi: 10.1093/jb/mvr049
Takamori, S. et al. Molecular anatomy of a trafficking organelle. Cell 127, 831–846 (2006).
doi: 10.1016/j.cell.2006.10.030
Mutch, S. A. et al. Protein quantification at the single vesicle level reveals that a subset of synaptic vesicle proteins are trafficked with high precision. J. Neurosci. 31, 1461–1470 (2011).
doi: 10.1523/JNEUROSCI.3805-10.2011
Furuike, S. et al. Resolving stepping rotation in Thermus thermophilus H
doi: 10.1038/ncomms1215
Abbas, Y. M., Wu, D., Bueler, S. A., Robinson, C. V. & Rubinstein, J. L. Structure of V-ATPase from the mammalian brain. Science 367, 1240–1246 (2020).
doi: 10.1126/science.aaz2924
Rost, B. R. et al. Optogenetic acidification of synaptic vesicles and lysosomes. Nat. Neurosci. 18, 1845–1852 (2015).
doi: 10.1038/nn.4161
Farsi, Z. et al. Single-vesicle imaging reveals different transport mechanisms between glutamatergic and GABAergic vesicles. Science 351, 981–984 (2016).
doi: 10.1126/science.aad8142
Grabe, M., Wang, H. & Oster, G. The Mechanochemistry of V-ATPase proton pumps. Biophys. J. 78, 2798–2813 (2000).
doi: 10.1016/S0006-3495(00)76823-8
Gowrisankaran, S. & Milosevic, I. Regulation of synaptic vesicle acidification at the neuronal synapse. IUBMB Life 72, 568–576 (2020).
doi: 10.1002/iub.2235
Dilworth, M. V., Findlay, H. E. & Booth, P. J. Detergent-free purification and reconstitution of functional human serotonin transporter (SERT) using diisobutylene maleic acid (DIBMA) copolymer. Biochim. Biophys. Acta Biomembr. 1863, 183602 (2021).
doi: 10.1016/j.bbamem.2021.183602
Ahmed, S., Holt, M., Riedel, D. & Jahn, R. Small-scale isolation of synaptic vesicles from mammalian brain. Nat. Protoc. 8, 998–1009 (2013).
doi: 10.1038/nprot.2013.053
Budzinski, K. L., Zeigler, M., Fujimoto, B. S., Bajjalieh, S. M. & Chiu, D. T. Measurements of the acidification kinetics of single SynaptopHluorin vesicles. Biophys. J. 101, 1580–1589 (2011).
doi: 10.1016/j.bpj.2011.08.032
Hernandez, J. M. et al. Membrane fusion intermediates via directional and full assembly of the SNARE complex. Science 336, 1581–1584 (2012).
doi: 10.1126/science.1221976
Preobraschenski, J., Zander, J.-F., Suzuki, T., Ahnert-Hilger, G. & Jahn, R. Vesicular glutamate transporters use flexible anion and cation binding sites for efficient accumulation of neurotransmitter. Neuron 84, 1287–1301 (2014).
doi: 10.1016/j.neuron.2014.11.008
Castorph, S. et al. Synaptic vesicles studied by dynamic light scattering. Eur. Phys. J. E 34, 63 (2011).
doi: 10.1140/epje/i2011-11063-2
Veshaguri, S. et al. Direct observation of proton pumping by a eukaryotic P-type ATPase. Science 351, 1469–1473 (2016).
doi: 10.1126/science.aad6429
Stamou, D., Duschl, C., Delamarche, E. & Vogel, H. Self-assembled microarrays of attoliter molecular vessels. Angew. Chem. Int. Ed. 42, 5580–5583 (2003).
doi: 10.1002/anie.200351866
Bendix, P. M., Pedersen, M. S. & Stamou, D. Quantification of nano-scale intermembrane contact areas by using fluorescence resonance energy transfer. Proc. Natl Acad. Sci. USA 106, 12341–12346 (2009).
doi: 10.1073/pnas.0903052106
Mathiasen, S. et al. Nanoscale high-content analysis using compositional heterogeneities of single proteoliposomes. Nat. Methods 11, 931–934 (2014).
doi: 10.1038/nmeth.3062
Fitzgerald, G. A. et al. Quantifying secondary transport at single-molecule resolution. Nature 575, 528–534 (2019).
doi: 10.1038/s41586-019-1747-5
Singh, A. et al. Protons in small spaces: discrete simulations of vesicle acidification. PLoS Comput. Biol. 15, e1007539 (2019).
doi: 10.1371/journal.pcbi.1007539
Taoufiq, Z. et al. Hidden proteome of synaptic vesicles in the mammalian brain. Proc. Natl Acad. Sci. USA 117, 33586–33596 (2020).
doi: 10.1073/pnas.2011870117
Zhao, J., Benlekbir, S. & Rubinstein, J. L. Electron cryomicroscopy observation of rotational states in a eukaryotic V-ATPase. Nature 521, 241–245 (2015).
doi: 10.1038/nature14365
Drory, O. & Nelson, N. The emerging structure of vacuolar ATPases. Physiology 21, 317–325 (2006).
doi: 10.1152/physiol.00017.2006
Kettner, C., Bertl, A., Obermeyer, G., Slayman, C. & Bihler, H. Electrophysiological analysis of the yeast V-type proton pump: variable coupling ratio and proton shunt. Biophys. J. 85, 3730–3738 (2003).
doi: 10.1016/S0006-3495(03)74789-4
Kishikawa, J., Nakanishi, A., Furuike, S., Tamakoshi, M. & Yokoyama, K. Molecular basis of ADP inhibition of vacuolar (V)-type ATPase/synthase. J. Biol. Chem. 289, 403–412 (2014).
doi: 10.1074/jbc.M113.523498
Uner, N. E. et al. Single-molecule analysis of inhibitory pausing states of V1-ATPase. J. Biol. Chem. 287, 28327–28335 (2012).
doi: 10.1074/jbc.M112.381194
Davies, J. M., Hunt, I. & Sanders, D. Vacuolar H
doi: 10.1073/pnas.91.18.8547
Accardi, A. Structure and gating of CLC channels and exchangers: structure and gating of CLC channels and exchangers. J. Physiol. 593, 4129–4138 (2015).
doi: 10.1113/JP270575
Schenck, S., Wojcik, S. M., Brose, N. & Takamori, S. A chloride conductance in VGLUT1 underlies maximal glutamate loading into synaptic vesicles. Nat. Neurosci. 12, 156–162 (2009).
doi: 10.1038/nn.2248
Maycox, P. R., Deckwerth, T., Hell, J. W. & Jahn, R. Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes. J. Biol. Chem. 263, 15423–15428 (1988).
doi: 10.1016/S0021-9258(19)37605-7
Minagawa, Y. et al. Basic properties of rotary dynamics of the molecular motor Enterococcus hirae V1-ATPase. J. Biol. Chem. 288, 32700–32707 (2013).
doi: 10.1074/jbc.M113.506329
Imamura, H. et al. Evidence for rotation of V1-ATPase. Proc. Natl Acad. Sci. USA 100, 2312–2315 (2003).
doi: 10.1073/pnas.0436796100
Grabe, M. & Oster, G. Regulation of organelle acidity. J. Gen. Physiol. 117, 329–344 (2001).
doi: 10.1085/jgp.117.4.329
Nakanishi, A., Kishikawa, J., Tamakoshi, M., Mitsuoka, K. & Yokoyama, K. Cryo EM structure of intact rotary H
doi: 10.1038/s41467-017-02553-6
Yasuda, R., Noji, H., Yoshida, M., Kinosita, K. & Itoh, H. Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase. Nature 410, 898–904 (2001).
doi: 10.1038/35073513
Noji, H., Yoshida, M. & Kinosita, K. Direct observation of the rotation of F
Adachi, K. et al. Coupling of rotation and catalysis in F1-ATPase revealed by single-molecule imaging and manipulation. Cell 130, 309–321 (2007).
doi: 10.1016/j.cell.2007.05.020
Watanabe, R. et al. Arrayed lipid bilayer chambers allow single-molecule analysis of membrane transporter activity. Nat. Commun. 5, 4519 (2014).
doi: 10.1038/ncomms5519
Soga, N. et al. Monodisperse liposomes with femtoliter volume enable quantitative digital bioassays of membrane transporters and cell-free gene expression. ACS Nano 14, 11700–11711 (2020).
doi: 10.1021/acsnano.0c04354
Phan, N. T. N., Li, X. & Ewing, A. G. Measuring synaptic vesicles using cellular electrochemistry and nanoscale molecular imaging. Nat. Rev. Chem. 1, 0048 (2017).
doi: 10.1038/s41570-017-0048
Maxson, M. E. et al. Detection and quantification of the vacuolar H
doi: 10.1083/jcb.202107174
Lu, H. P., Xun, L. & Xie, X. S. Single-molecule enzymatic dynamics. Science 282, 1877–1882 (1998).
doi: 10.1126/science.282.5395.1877
Ciftci, D. et al. Single-molecule transport kinetics of a glutamate transporter homolog shows static disorder. Sci. Adv. 6, eaaz1949 (2020).
doi: 10.1126/sciadv.aaz1949
Akyuz, N., Altman, R. B., Blanchard, S. C. & Boudker, O. Transport dynamics in a glutamate transporter homologue. Nature 502, 114–118 (2013).
doi: 10.1038/nature12265
Erkens, G. B., Hänelt, I., Goudsmits, J. M. H., Slotboom, D. J. & van Oijen, A. M. Unsynchronised subunit motion in single trimeric sodium-coupled aspartate transporters. Nature 502, 119–123 (2013).
doi: 10.1038/nature12538
Akyuz, N. et al. Transport domain unlocking sets the uptake rate of an aspartate transporter. Nature 518, 68–73 (2015).
doi: 10.1038/nature14158
Dyla, M. et al. Dynamics of P-type ATPase transport revealed by single-molecule FRET. Nature 551, 346–351 (2017).
doi: 10.1038/nature24296
Rundlet, E. J. et al. Structural basis of early translocation events on the ribosome. Nature 595, 741–745 (2021).
doi: 10.1038/s41586-021-03713-x
Chung, S. H. & Kennedy, R. A. Forward-backward non-linear filtering technique for extracting small biological signals from noise. J. Neurosci. Methods 40, 71–86 (1991).
doi: 10.1016/0165-0270(91)90118-J
Kemmer, G. C. et al. Lipid-conjugated fluorescent pH sensors for monitoring pH changes in reconstituted membrane systems. Analyst 140, 6313–6320 (2015).
doi: 10.1039/C5AN01180A
Pobbati, A. V. N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science 313, 673–676 (2006).
doi: 10.1126/science.1129486
Stein, A., Radhakrishnan, A., Riedel, D., Fasshauer, D. & Jahn, R. Synaptotagmin activates membrane fusion through a Ca2
doi: 10.1038/nsmb1305
Rigaud, J.-L., Lévy, D. & Düzgünes, N. (ed.) in Methods in Enzymology Vol. 372, 65–86 (Elsevier, 2003).
Rigaud, J.-L., Pitard, B. & Levy, D. Reconstitution of membrane proteins into liposomes: application to energy-transducing membrane proteins. Biochim. Biophys. Acta Bioenerg. 1231, 223–246 (1995).
doi: 10.1016/0005-2728(95)00091-V
van den Bogaart, G. et al. One SNARE complex is sufficient for membrane fusion. Nat. Struct. Mol. Biol. 17, 358–364 (2010).
doi: 10.1038/nsmb.1748
Huttner, W. B., Schiebler, W., Greengard, P. & 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, 1374–1388 (1983).
doi: 10.1083/jcb.96.5.1374
Nagy, A., Baker, R. R., Morris, S. J. & Whittaker, V. P. The preparation and characterization of synaptic vesicles of high purity. Brain Res. 109, 285–309 (1976).
doi: 10.1016/0006-8993(76)90531-X
Upmanyu, N. et al. Colocalization of different neurotransmitter transporters on synaptic vesicles is sparse except for VGLUT1 and ZnT3. Neuron 110, 1483–1497 (2022).
doi: 10.1016/j.neuron.2022.02.008
Takamori, S., Riedel, D. & Jahn, R. Immunoisolation of GABA-specific synaptic vesicles defines a functionally distinct subset of synaptic vesicles. J. Neurosci. 20, 4904–4911 (2000).
doi: 10.1523/JNEUROSCI.20-13-04904.2000
Preobraschenski, J. et al. Dual and direction-selective mechanisms of phosphate transport by the vesicular glutamate transporter. Cell Rep. 23, 535–545 (2018).
doi: 10.1016/j.celrep.2018.03.055