Synaptophysin chaperones the assembly of 12 SNAREpins under each ready-release vesicle.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
07 Nov 2023
Historique:
medline: 1 11 2023
pubmed: 30 10 2023
entrez: 30 10 2023
Statut: ppublish

Résumé

The synaptic vesicle protein Synaptophysin (Syp) has long been known to form a complex with the Vesicle associated soluble N-ethylmaleimide sensitive fusion protein attachment receptor (v-SNARE) Vesicle associated membrane protein (VAMP), but a more specific molecular function or mechanism of action in exocytosis has been lacking because gene knockouts have minimal effects. Utilizing fully defined reconstitution and single-molecule measurements, we now report that Syp functions as a chaperone that determines the number of SNAREpins assembling between a ready-release vesicle and its target membrane bilayer. Specifically, Syp directs the assembly of 12 ± 1 SNAREpins under each docked vesicle, even in the face of an excess of SNARE proteins. The SNAREpins assemble in successive waves of 6 ± 1 and 5 ± 2 SNAREpins, respectively, tightly linked to oligomerization of and binding to the vesicle Ca

Identifiants

pubmed: 37903271
doi: 10.1073/pnas.2311484120
pmc: PMC10636311
doi:

Substances chimiques

Synaptophysin 0
Synaptotagmins 134193-27-4
SNARE Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2311484120

Commentaires et corrections

Type : UpdateOf

Références

J Struct Biol. 2015 Nov;192(2):216-21
pubmed: 26278980
Biophys J. 2016 Mar 8;110(5):1110-24
pubmed: 26958888
J Colloid Interface Sci. 2002 Feb 1;246(1):40-7
pubmed: 16290382
Nat Struct Mol Biol. 2015 Jul;22(7):547-54
pubmed: 26030875
Proc Natl Acad Sci U S A. 2019 Feb 12;116(7):2435-2442
pubmed: 30700546
Elife. 2018 Nov 09;7:
pubmed: 30412051
Proc Natl Acad Sci U S A. 2021 Feb 2;118(5):
pubmed: 33468631
Biophys J. 2017 Jun 6;112(11):2348-2356
pubmed: 28591607
J Biol Chem. 2002 Jul 19;277(29):26517-23
pubmed: 12004067
FEBS Lett. 2019 Jan;593(2):154-162
pubmed: 30570144
Proc Natl Acad Sci U S A. 2021 Jan 26;118(4):
pubmed: 33468652
Proc Natl Acad Sci U S A. 2017 Feb 7;114(6):1238-1241
pubmed: 28115718
Small. 2022 Dec;18(51):e2205567
pubmed: 36328714
J Neurosci. 1999 Mar 15;19(6):1922-31
pubmed: 10066245
Neuron. 2011 Jun 9;70(5):847-54
pubmed: 21658579
J Neurosci. 2011 Sep 28;31(39):14032-6
pubmed: 21957264
FEBS Lett. 2023 Sep;597(18):2233-2249
pubmed: 37643878
Sci Adv. 2022 Jun 24;8(25):eabo5272
pubmed: 35731863
J Am Chem Soc. 2014 Mar 5;136(9):3456-64
pubmed: 24533674
J Am Soc Mass Spectrom. 2019 Jan;30(1):149-160
pubmed: 29949059
Elife. 2022 Apr 20;11:
pubmed: 35442188
FEBS Lett. 2021 Feb;595(3):297-309
pubmed: 33222163
Sci Rep. 2015 Sep 03;5:13659
pubmed: 26333660
EMBO J. 1995 Jan 16;14(2):224-31
pubmed: 7835333
Proc Natl Acad Sci U S A. 2018 Aug 7;115(32):E7624-E7631
pubmed: 30038018
Eur J Biochem. 1997 Oct 15;249(2):540-6
pubmed: 9370365
FEBS Lett. 2019 Jan;593(2):144-153
pubmed: 30561792
Protein Sci. 2017 Jul;26(7):1252-1265
pubmed: 28097727
Science. 2014 May 30;344(6187):1023-8
pubmed: 24876496
Nat Cell Biol. 2000 Jan;2(1):42-9
pubmed: 10620806
Chem Phys Lipids. 2013 Jul-Aug;172-173:67-77
pubmed: 23701821
Neuron. 2002 Jan 31;33(3):397-409
pubmed: 11832227
Elife. 2015 Apr 02;4:
pubmed: 25831964
Proc Natl Acad Sci U S A. 2014 Jul 15;111(28):10317-22
pubmed: 24982161
Nat Commun. 2014 Sep 17;5:4955
pubmed: 25229806
Proc Natl Acad Sci U S A. 2022 Feb 15;119(7):
pubmed: 35135883
Langmuir. 2018 May 22;34(20):5849-5859
pubmed: 29694054
Elife. 2020 May 13;9:
pubmed: 32401194
Elife. 2019 May 15;8:
pubmed: 31090538
Cell. 1995 Oct 6;83(1):111-9
pubmed: 7553862
Cell. 1993 Nov 5;75(3):409-18
pubmed: 8221884
Science. 2013 Jan 25;339(6118):421-5
pubmed: 23258414
J Biol Chem. 1994 Oct 7;269(40):24534-7
pubmed: 7929121
J Biol Chem. 2002 Mar 8;277(10):7838-48
pubmed: 11751907
Structure. 2007 Jun;15(6):707-14
pubmed: 17562317
Proc Natl Acad Sci U S A. 2014 Sep 23;111(38):13966-71
pubmed: 25201968
Proc Natl Acad Sci U S A. 1988 Jun;85(12):4538-42
pubmed: 3380805
Nat Struct Mol Biol. 2011 May;18(5):542-9
pubmed: 21499244
J Cell Biol. 2002 Jul 22;158(2):273-82
pubmed: 12119360
Nat Protoc. 2013 May;8(5):998-1009
pubmed: 23619891
Nat Commun. 2019 Jan 8;10(1):69
pubmed: 30622273
Cell. 1988 Jul 15;54(2):221-7
pubmed: 3390865
Nat Methods. 2023 Jun;20(6):891-897
pubmed: 37106230
J Struct Biol. 2005 Oct;152(1):36-51
pubmed: 16182563
Front Synaptic Neurosci. 2021 Sep 20;13:740318
pubmed: 34616284
Science. 2012 Sep 14;337(6100):1340-3
pubmed: 22903523
Science. 2006 Aug 4;313(5787):676-80
pubmed: 16794037
Cell. 2006 Nov 17;127(4):831-46
pubmed: 17110340
J Cell Biol. 2002 Sep 2;158(5):929-40
pubmed: 12213837
Science. 1988 Nov 18;242(4881):1050-3
pubmed: 2461586
FEBS Lett. 2017 Nov;591(21):3459-3480
pubmed: 28983915
Nature. 1993 Mar 25;362(6418):318-24
pubmed: 8455717
Cell. 1998 Mar 20;92(6):759-72
pubmed: 9529252
Langmuir. 2009 May 19;25(10):5767-72
pubmed: 19358596
Biophys J. 2023 Jun 6;122(11):1962-1973
pubmed: 36168290
Nat Methods. 2017 Apr;14(4):331-332
pubmed: 28250466
Proc Natl Acad Sci U S A. 2016 Nov 22;113(47):E7590-E7599
pubmed: 27821736
Nat Struct Mol Biol. 2011 Jul 24;18(8):927-33
pubmed: 21785414
EMBO J. 2020 Aug 17;39(16):e103631
pubmed: 32643828
Nat Neurosci. 2018 Jan;21(1):41-49
pubmed: 29230050
Cell Rep. 2020 Jul 21;32(3):107926
pubmed: 32698012
Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5141-6
pubmed: 19251653

Auteurs

Manindra Bera (M)

Nanobiology Institute, Yale University School of Medicine, New Haven, CT 06520.
Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06520.

Abhijith Radhakrishnan (A)

Nanobiology Institute, Yale University School of Medicine, New Haven, CT 06520.
Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06520.

Jeff Coleman (J)

Nanobiology Institute, Yale University School of Medicine, New Haven, CT 06520.
Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06520.

R Venkat K Sundaram (RV)

Nanobiology Institute, Yale University School of Medicine, New Haven, CT 06520.
Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06520.

Sathish Ramakrishnan (S)

Nanobiology Institute, Yale University School of Medicine, New Haven, CT 06520.
Department of Pathology, Yale University School of Medicine, New Haven, CT 06520.

Frederic Pincet (F)

Nanobiology Institute, Yale University School of Medicine, New Haven, CT 06520.
Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06520.
Laboratoire de Physique Statistique, Ecole Normale Supérieure, Paris Sciences et Lettres Research University, CNRS, Sorbonne Université, Université de Paris Cité, 75005 Paris, France.

James E Rothman (JE)

Nanobiology Institute, Yale University School of Medicine, New Haven, CT 06520.
Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06520.

Articles similaires

Humans Stomach Neoplasms Computational Biology Prognosis Synaptotagmins

Specialized contact sites regulate the fusion of chlamydial inclusion membranes.

Christine Linton, Jordan Wesolowski, Anna Lobley et al.
1.00
Chlamydia trachomatis Inclusion Bodies Membrane Fusion HeLa Cells Humans

Classifications MeSH