Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi

Emperador-Melero J, Huson V, van Weering J, Bollmann C, Fischer von Mollard G, Toonen RF, Verhage M (2018)
NATURE COMMUNICATIONS 9(1): 3421.

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Autor*in
Emperador-Melero, Javier; Huson, Vincent; van Weering, Jan; Bollmann, Christian; Fischer von Mollard, GabrieleUniBi ; Toonen, Ruud F.; Verhage, Matthijs
Abstract / Bemerkung
The SNAREs Vti1a/1b are implicated in regulated secretion, but their role relative to canonical exocytic SNAREs remains elusive. Here, we show that synaptic vesicle and dense-core vesicle (DCV) secretion is indeed severely impaired in Vti1a/b-deficient neurons. The synaptic levels of proteins that mediate secretion were reduced, down to 50% for the exocytic SNARE SNAP25. The delivery of SNAP25 and DCV-cargo into axons was decreased and these molecules accumulated in the Golgi. These defects were rescued by either Vti1a or Vti1b expression. Distended Golgi cisternae and clear vacuoles were observed in Vti1a/b-deficient neurons. The normal non-homogeneous distribution of DCV-cargo inside the Golgi was lost. Cargo trafficking out of, but not into the Golgi, was impaired. Finally, retrograde Cholera Toxin trafficking, but not Sortilin/Sorcs1 distribution, was compromised. We conclude that Vti1a/b support regulated secretion by sorting secretory cargo and synaptic secretion machinery components at the Golgi.
Erscheinungsjahr
2018
Zeitschriftentitel
NATURE COMMUNICATIONS
Band
9
Ausgabe
1
Art.-Nr.
3421
ISSN
2041-1723
Page URI
https://pub.uni-bielefeld.de/record/2931110

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Emperador-Melero J, Huson V, van Weering J, et al. Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi. NATURE COMMUNICATIONS. 2018;9(1): 3421.
Emperador-Melero, J., Huson, V., van Weering, J., Bollmann, C., Fischer von Mollard, G., Toonen, R. F., & Verhage, M. (2018). Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi. NATURE COMMUNICATIONS, 9(1), 3421. doi:10.1038/s41467-018-05699-z
Emperador-Melero, Javier, Huson, Vincent, van Weering, Jan, Bollmann, Christian, Fischer von Mollard, Gabriele, Toonen, Ruud F., and Verhage, Matthijs. 2018. “Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi”. NATURE COMMUNICATIONS 9 (1): 3421.
Emperador-Melero, J., Huson, V., van Weering, J., Bollmann, C., Fischer von Mollard, G., Toonen, R. F., and Verhage, M. (2018). Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi. NATURE COMMUNICATIONS 9:3421.
Emperador-Melero, J., et al., 2018. Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi. NATURE COMMUNICATIONS, 9(1): 3421.
J. Emperador-Melero, et al., “Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi”, NATURE COMMUNICATIONS, vol. 9, 2018, : 3421.
Emperador-Melero, J., Huson, V., van Weering, J., Bollmann, C., Fischer von Mollard, G., Toonen, R.F., Verhage, M.: Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi. NATURE COMMUNICATIONS. 9, : 3421 (2018).
Emperador-Melero, Javier, Huson, Vincent, van Weering, Jan, Bollmann, Christian, Fischer von Mollard, Gabriele, Toonen, Ruud F., and Verhage, Matthijs. “Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi”. NATURE COMMUNICATIONS 9.1 (2018): 3421.

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Synaptotagmin 17 controls neurite outgrowth and synaptic physiology via distinct cellular pathways.
Ruhl DA, Bomba-Warczak E, Watson ET, Bradberry MM, Peterson TA, Basu T, Frelka A, Evans CS, Briguglio JS, Basta T, Stowell MHB, Savas JN, Roopra A, Pearce RA, Piper RC, Chapman ER., Nat Commun 10(1), 2019
PMID: 31387992

75 References

Daten bereitgestellt von Europe PubMed Central.

The BAR domain protein Arfaptin-1 controls secretory granule biogenesis at the trans-Golgi network.
Gehart H, Goginashvili A, Beck R, Morvan J, Erbs E, Formentini I, De Matteis MA, Schwab Y, Wieland FT, Ricci R., Dev. Cell 23(4), 2012
PMID: 22981988
Two Rab2 interactors regulate dense-core vesicle maturation.
Ailion M, Hannemann M, Dalton S, Pappas A, Watanabe S, Hegermann J, Liu Q, Han HF, Gu M, Goulding MQ, Sasidharan N, Schuske K, Hullett P, Eimer S, Jorgensen EM., Neuron 82(1), 2014
PMID: 24698274
Early Golgi Abnormalities and Neurodegeneration upon Loss of Presynaptic Proteins Munc18-1, Syntaxin-1, or SNAP-25.
Santos TC, Wierda K, Broeke JH, Toonen RF, Verhage M., J. Neurosci. 37(17), 2017
PMID: 28348137
Deletion of the SNARE vti1b in mice results in the loss of a single SNARE partner, syntaxin 8.
Atlashkin V, Kreykenbohm V, Eskelinen EL, Wenzel D, Fayyazi A, Fischer von Mollard G., Mol. Cell. Biol. 23(15), 2003
PMID: 12861006
Synchronization of secretory protein traffic in populations of cells.
Boncompain G, Divoux S, Gareil N, de Forges H, Lescure A, Latreche L, Mercanti V, Jollivet F, Raposo G, Perez F., Nat. Methods 9(5), 2012
PMID: 22406856
Dense-core secretory granule biogenesis.
Kim T, Gondre-Lewis MC, Arnaoutova I, Loh YP., Physiology (Bethesda) 21(), 2006
PMID: 16565478
Neuropeptide delivery to synapses by long-range vesicle circulation and sporadic capture.
Wong MY, Zhou C, Shakiryanova D, Lloyd TE, Deitcher DL, Levitan ES., Cell 148(5), 2012
PMID: 22385966
COG Complex Complexities: Detailed Characterization of a Complete Set of HEK293T Cells Lacking Individual COG Subunits.
Bailey Blackburn J, Pokrovskaya I, Fisher P, Ungar D, Lupashin VV., Front Cell Dev Biol 4(), 2016
PMID: 27066481
Homotypic fusion of early endosomes: SNAREs do not determine fusion specificity.
Brandhorst D, Zwilling D, Rizzoli SO, Lippert U, Lang T, Jahn R., Proc. Natl. Acad. Sci. U.S.A. 103(8), 2006
PMID: 16469845
Endosomal sorting of readily releasable synaptic vesicles.
Hoopmann P, Punge A, Barysch SV, Westphal V, Buckers J, Opazo F, Bethani I, Lauterbach MA, Hell SW, Rizzoli SO., Proc. Natl. Acad. Sci. U.S.A. 107(44), 2010
PMID: 20956291
The BAR domain protein PICK1 controls vesicle number and size in adrenal chromaffin cells.
Pinheiro PS, Jansen AM, de Wit H, Tawfik B, Madsen KL, Verhage M, Gether U, Sorensen JB., J. Neurosci. 34(32), 2014
PMID: 25100601
Sortilin controls intracellular sorting of brain-derived neurotrophic factor to the regulated secretory pathway.
Chen ZY, Ieraci A, Teng H, Dall H, Meng CX, Herrera DG, Nykjaer A, Hempstead BL, Lee FS., J. Neurosci. 25(26), 2005
PMID: 15987945
Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses.
Granseth B, Odermatt B, Royle SJ, Lagnado L., Neuron 51(6), 2006
PMID: 16982422
Vesicular trafficking of semaphorin 3A is activity-dependent and differs between axons and dendrites.
de Wit J, Toonen RF, Verhaagen J, Verhage M., Traffic 7(8), 2006
PMID: 16734664
Selective molecular impairment of spontaneous neurotransmission modulates synaptic efficacy.
Crawford DC, Ramirez DM, Trauterman B, Monteggia LM, Kavalali ET., Nat Commun 8(), 2017
PMID: 28186166
Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events.
Pryor PR, Mullock BM, Bright NA, Lindsay MR, Gray SR, Richardson SC, Stewart A, James DE, Piper RC, Luzio JP., EMBO Rep. 5(6), 2004
PMID: 15133481
Additive effects on the energy barrier for synaptic vesicle fusion cause supralinear effects on the vesicle fusion rate.
Schotten S, Meijer M, Walter AM, Huson V, Mamer L, Kalogreades L, ter Veer M, Ruiter M, Brose N, Rosenmund C, Sorensen JB, Verhage M, Cornelisse LN., Elife 4(), 2015
PMID: 25871846
Seven novel mammalian SNARE proteins localize to distinct membrane compartments.
Advani RJ, Bae HR, Bock JB, Chao DS, Doung YC, Prekeris R, Yoo JS, Scheller RH., J. Biol. Chem. 273(17), 1998
PMID: 9553086
Protein scaffolds in the coupling of synaptic exocytosis and endocytosis.
Haucke V, Neher E, Sigrist SJ., Nat. Rev. Neurosci. 12(3), 2011
PMID: 21304549
Opposing functions of two sub-domains of the SNARE-complex in neurotransmission.
Weber JP, Reim K, Sorensen JB., EMBO J. 29(15), 2010
PMID: 20562829
ADF/cofilin regulates secretory cargo sorting at the TGN via the Ca2+ ATPase SPCA1.
von Blume J, Alleaume AM, Cantero-Recasens G, Curwin A, Carreras-Sureda A, Zimmermann T, van Galen J, Wakana Y, Valverde MA, Malhotra V., Dev. Cell 20(5), 2011
PMID: 21571222
SNAP-25 gene family members differentially support secretory vesicle fusion.
Arora S, Saarloos I, Kooistra R, van de Bospoort R, Verhage M, Toonen RF., J. Cell. Sci. 130(11), 2017
PMID: 28404788
Munc18-1 expression levels control synapse recovery by regulating readily releasable pool size.
Toonen RF, Wierda K, Sons MS, de Wit H, Cornelisse LN, Brussaard A, Plomp JJ, Verhage M., Proc. Natl. Acad. Sci. U.S.A. 103(48), 2006
PMID: 17110441
Endosomal accumulation of APP in wobbler motor neurons reflects impaired vesicle trafficking: implications for human motor neuron disease.
Palmisano R, Golfi P, Heimann P, Shaw C, Troakes C, Schmitt-John T, Bartsch JW., BMC Neurosci 12(), 2011
PMID: 21385376
HID-1 controls formation of large dense core vesicles by influencing cargo sorting and trans-Golgi network acidification.
Hummer BH, de Leeuw NF, Burns C, Chen L, Joens MS, Hosford B, Fitzpatrick JAJ, Asensio CS., Mol. Biol. Cell 28(26), 2017
PMID: 29074564
Activity-dependent phosphorylation of Ser187 is required for SNAP-25-negative modulation of neuronal voltage-gated calcium channels.
Pozzi D, Condliffe S, Bozzi Y, Chikhladze M, Grumelli C, Proux-Gillardeaux V, Takahashi M, Franceschetti S, Verderio C, Matteoli M., Proc. Natl. Acad. Sci. U.S.A. 105(1), 2007
PMID: 18162553
Automated analysis of neuronal morphology, synapse number and synaptic recruitment.
Schmitz SK, Hjorth JJ, Joemai RM, Wijntjes R, Eijgenraam S, de Bruijn P, Georgiou C, de Jong AP, van Ooyen A, Verhage M, Cornelisse LN, Toonen RF, Veldkamp WJ, Veldkamp W., J. Neurosci. Methods 195(2), 2010
PMID: 21167201
Differential Maturation of the Two Regulated Secretory Pathways in Human iPSC-Derived Neurons.
Emperador Melero J, Nadadhur AG, Schut D, Weering JV, Heine VM, Toonen RF, Verhage M., Stem Cell Reports 8(3), 2017
PMID: 28238793
Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development.
Kunwar AJ, Rickmann M, Backofen B, Browski SM, Rosenbusch J, Schoning S, Fleischmann T, Krieglstein K, Fischer von Mollard G., Proc. Natl. Acad. Sci. U.S.A. 108(6), 2011
PMID: 21262811
Metabolic turnover of synaptic proteins: kinetics, interdependencies and implications for synaptic maintenance.
Cohen LD, Zuchman R, Sorokina O, Muller A, Dieterich DC, Armstrong JD, Ziv T, Ziv NE., PLoS ONE 8(5), 2013
PMID: 23658807
A SNARE-adaptor interaction is a new mode of cargo recognition in clathrin-coated vesicles.
Miller SE, Collins BM, McCoy AJ, Robinson MS, Owen DJ., Nature 450(7169), 2007
PMID: 18033301
Propeptide cleavage conditions sortilin/neurotensin receptor-3 for ligand binding.
Munck Petersen C, Nielsen MS, Jacobsen C, Tauris J, Jacobsen L, Gliemann J, Moestrup SK, Madsen P., EMBO J. 18(3), 1999
PMID: 9927419
The SNARE protein vti1a functions in dense-core vesicle biogenesis.
Walter AM, Kurps J, de Wit H, Schoning S, Toft-Bertelsen TL, Lauks J, Ziomkiewicz I, Weiss AN, Schulz A, Fischer von Mollard G, Verhage M, Sorensen JB., EMBO J. 33(15), 2014
PMID: 24902738
Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs.
Fasshauer D, Sutton RB, Brunger AT, Jahn R., Proc. Natl. Acad. Sci. U.S.A. 95(26), 1998
PMID: 9861047
Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission.
Ramirez DM, Khvotchev M, Trauterman B, Kavalali ET., Neuron 73(1), 2012
PMID: 22243751
Recruitment of arfaptins to the trans-Golgi network by PI(4)P and their involvement in cargo export.
Cruz-Garcia D, Ortega-Bellido M, Scarpa M, Villeneuve J, Jovic M, Porzner M, Balla T, Seufferlein T, Malhotra V., EMBO J. 32(12), 2013
PMID: 23695357
Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform.
Mallard F, Tang BL, Galli T, Tenza D, Saint-Pol A, Yue X, Antony C, Hong W, Goud B, Johannes L., J. Cell Biol. 156(4), 2002
PMID: 11839770
SNAREs Controlling Vesicular Release of BDNF and Development of Callosal Axons.
Shimojo M, Courchet J, Pieraut S, Torabi-Rander N, Sando R 3rd, Polleux F, Maximov A., Cell Rep 11(7), 2015
PMID: 25959820
SORCS1 is necessary for normal insulin secretory granule biogenesis in metabolically stressed β cells.
Kebede MA, Oler AT, Gregg T, Balloon AJ, Johnson A, Mitok K, Rabaglia M, Schueler K, Stapleton D, Thorstenson C, Wrighton L, Floyd BJ, Richards O, Raines S, Eliceiri K, Seidah NG, Rhodes C, Keller MP, Coon JL, Audhya A, Attie AD., J. Clin. Invest. 124(10), 2014
PMID: 25157818
Neurotrophin secretion: current facts and future prospects.
Lessmann V, Gottmann K, Malcangio M., Prog. Neurobiol. 69(5), 2003
PMID: 12787574
A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function.
Antonin W, Holroyd C, Fasshauer D, Pabst S, Von Mollard GF, Jahn R., EMBO J. 19(23), 2000
PMID: 11101518
VPS54 and the wobbler mouse.
Schmitt-John T., Front Neurosci 9(), 2015
PMID: 26539077
Molecular anatomy of a trafficking organelle.
Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P, Muller SA, Rammner B, Grater F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmuller H, Heuser J, Wieland F, Jahn R., Cell 127(4), 2006
PMID: 17110340
Organization of SNAREs within the Golgi stack.
Malsam J, Sollner TH., Cold Spring Harb Perspect Biol 3(10), 2011
PMID: 21768609
Post-Golgi anterograde transport requires GARP-dependent endosome-to-TGN retrograde transport.
Hirata T, Fujita M, Nakamura S, Gotoh K, Motooka D, Murakami Y, Maeda Y, Kinoshita T., Mol. Biol. Cell 26(17), 2015
PMID: 26157166
Subunit structure of a mammalian ER/Golgi SNARE complex.
Xu D, Joglekar AP, Williams AL, Hay JC., J. Biol. Chem. 275(50), 2000
PMID: 11035026
Retrograde traffic out of the yeast vacuole to the TGN occurs via the prevacuolar/endosomal compartment.
Bryant NJ, Piper RC, Weisman LS, Stevens TH., J. Cell Biol. 142(3), 1998
PMID: 9700156
Homotypic fusion of immature secretory granules during maturation requires syntaxin 6.
Wendler F, Page L, Urbe S, Tooze SA., Mol. Biol. Cell 12(6), 2001
PMID: 11408578
Cab45 is required for Ca(2+)-dependent secretory cargo sorting at the trans-Golgi network.
von Blume J, Alleaume AM, Kienzle C, Carreras-Sureda A, Valverde M, Malhotra V., J. Cell Biol. 199(7), 2012
PMID: 23266954
GS28, a 28-kilodalton Golgi SNARE that participates in ER-Golgi transport.
Subramaniam VN, Peter F, Philp R, Wong SH, Hong W., Science 272(5265), 1996
PMID: 8638159
Golgi function and dysfunction in the first COG4-deficient CDG type II patient.
Reynders E, Foulquier F, Leao Teles E, Quelhas D, Morelle W, Rabouille C, Annaert W, Matthijs G., Hum. Mol. Genet. 18(17), 2009
PMID: 19494034
Flux of signalling endosomes undergoing axonal retrograde transport is encoded by presynaptic activity and TrkB.
Wang T, Martin S, Nguyen TH, Harper CB, Gormal RS, Martinez-Marmol R, Karunanithi S, Coulson EJ, Glass NR, Cooper-White JJ, van Swinderen B, Meunier FA., Nat Commun 7(), 2016
PMID: 27687129
Neuropeptide transmission in brain circuits.
van den Pol AN., Neuron 76(1), 2012
PMID: 23040809
Membrane fusion: grappling with SNARE and SM proteins.
Sudhof TC, Rothman JE., Science 323(5913), 2009
PMID: 19164740
Molecular machines governing exocytosis of synaptic vesicles.
Jahn R, Fasshauer D., Nature 490(7419), 2012
PMID: 23060190
The SNAREs vti1a and vti1b have distinct localization and SNARE complex partners.
Kreykenbohm V, Wenzel D, Antonin W, Atlachkine V, von Mollard GF., Eur. J. Cell Biol. 81(5), 2002
PMID: 12067063
Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis.
Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, Lopez-Bendito G, Molnar Z, Becher MW, Valenzuela CF, Partridge LD, Wilson MC., Nat. Neurosci. 5(1), 2002
PMID: 11753414
Munc13 controls the location and efficiency of dense-core vesicle release in neurons.
van de Bospoort R, Farina M, Schmitz SK, de Jong A, de Wit H, Verhage M, Toonen RF., J. Cell Biol. 199(6), 2012
PMID: 23229896
Self-assembly of VPS41 promotes sorting required for biogenesis of the regulated secretory pathway.
Asensio CS, Sirkis DW, Maas JW Jr, Egami K, To TL, Brodsky FM, Shu X, Cheng Y, Edwards RH., Dev. Cell 27(4), 2013
PMID: 24210660
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