Structure and Function of a Bacterial Gap Junction Analog.
cell-cell connections
cyanobacteria
electron cryotomography
fluorescence recovery after photobleaching
membrane trafficking
multicellularity
septal junctions
subtomogram averaging
Journal
Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066
Informations de publication
Date de publication:
11 07 2019
11 07 2019
Historique:
received:
29
10
2018
revised:
04
03
2019
accepted:
29
05
2019
entrez:
13
7
2019
pubmed:
13
7
2019
medline:
9
4
2020
Statut:
ppublish
Résumé
Multicellular lifestyle requires cell-cell connections. In multicellular cyanobacteria, septal junctions enable molecular exchange between sister cells and are required for cellular differentiation. The structure of septal junctions is poorly understood, and it is unknown whether they are capable of controlling intercellular communication. Here, we resolved the in situ architecture of septal junctions by electron cryotomography of cryo-focused ion beam-milled cyanobacterial filaments. Septal junctions consisted of a tube traversing the septal peptidoglycan. Each tube end comprised a FraD-containing plug, which was covered by a cytoplasmic cap. Fluorescence recovery after photobleaching showed that intercellular communication was blocked upon stress. Gating was accompanied by a reversible conformational change of the septal junction cap. We provide the mechanistic framework for a cell junction that predates eukaryotic gap junctions by a billion years. The conservation of a gated dynamic mechanism across different domains of life emphasizes the importance of controlling molecular exchange in multicellular organisms.
Identifiants
pubmed: 31299201
pii: S0092-8674(19)30626-9
doi: 10.1016/j.cell.2019.05.055
pmc: PMC6630896
pii:
doi:
Substances chimiques
Bacterial Proteins
0
Membrane Proteins
0
Carbonyl Cyanide m-Chlorophenyl Hydrazone
555-60-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
374-384.e15Subventions
Organisme : European Research Council
ID : 679209
Pays : International
Informations de copyright
Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved.
Références
Cell. 2017 Mar 9;168(6):1065-1074.e10
pubmed: 28283062
Mol Microbiol. 2011 Feb;79(4):1077-88
pubmed: 21299655
Ultramicroscopy. 2018 Jul;190:1-11
pubmed: 29655973
Science. 2006 Aug 18;313(5789):944-8
pubmed: 16917055
Bio Protoc. 2015 Sep 5;5(17):
pubmed: 27294174
Mol Microbiol. 2010 Mar;75(5):1159-70
pubmed: 20487302
mBio. 2017 Jan 3;8(1):
pubmed: 28049144
Cell. 1999 Jun 11;97(6):743-54
pubmed: 10380926
Arch Mikrobiol. 1955;22(1):45-77
pubmed: 13249505
Proc Natl Acad Sci U S A. 2014 Mar 11;111(10):3823-8
pubmed: 24550502
Proc Natl Acad Sci U S A. 1984 Mar;81(5):1561-5
pubmed: 6324204
J Exp Bot. 2014 Dec;65(22):6337-58
pubmed: 25262225
Biochim Biophys Acta. 2013 Jan;1828(1):51-68
pubmed: 22342665
J Bacteriol. 1994 Apr;176(8):2282-92
pubmed: 8157596
Nat Methods. 2007 Mar;4(3):215-7
pubmed: 17277781
Nat Rev Microbiol. 2010 Jan;8(1):39-50
pubmed: 19966815
Nature. 1980 Feb 7;283(5747):545-9
pubmed: 7354837
Dev Cell. 2017 Oct 23;43(2):124-140
pubmed: 29065305
Mol Microbiol. 2018 Apr;108(2):187-203
pubmed: 29437253
mBio. 2015 Mar 17;6(2):e02109
pubmed: 25784700
J Struct Biol. 2017 Feb;197(2):73-82
pubmed: 27444390
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Life (Basel). 2018 Dec 20;9(1):
pubmed: 30577420
J Bacteriol. 2012 Oct;194(19):5218-27
pubmed: 22821973
Science. 2016 Mar 11;351(6278):aad2001
pubmed: 26965631
Nat Rev Neurosci. 2005 Mar;6(3):191-200
pubmed: 15738956
FASEB J. 2013 Jun;27(6):2293-300
pubmed: 23444428
J Bacteriol. 1983 Aug;155(2):628-33
pubmed: 6135688
Methods Mol Biol. 2017;1615:353-375
pubmed: 28667625
Microbiology (Reading). 2007 Feb;153(Pt 2):601-607
pubmed: 17259632
Front Cell Infect Microbiol. 2017 Sep 05;7:386
pubmed: 28929086
Trends Microbiol. 2016 Feb;24(2):79-82
pubmed: 26748968
Proc Natl Acad Sci U S A. 2013 Jan 29;110(5):1791-6
pubmed: 23319632
Biochemistry (Mosc). 2001 Jun;66(6):640-5
pubmed: 11421813
J Bacteriol. 1995 Mar;177(6):1520-6
pubmed: 7883709
Microsc Microanal. 2008 Oct;14(5):375-9
pubmed: 18793481
Methods Enzymol. 1988;167:747-54
pubmed: 3148842
J Struct Biol. 2007 Jan;157(1):138-47
pubmed: 16904341
J Bacteriol. 2007 May;189(10):3884-90
pubmed: 17369306
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Bacteriol. 1977 Mar;129(3):1545-55
pubmed: 14927
Proc Natl Acad Sci U S A. 2015 Aug 11;112(32):E4458-64
pubmed: 26216997
Cell Microbiol. 2011 Nov;13(11):1744-54
pubmed: 21819512
Mol Microbiol. 2011 Oct;82(1):87-98
pubmed: 21819458
Mol Microbiol. 2015 May;96(3):566-80
pubmed: 25644579
J Membr Biol. 1983;73(1):69-89
pubmed: 6306241
EMBO J. 2008 May 7;27(9):1299-308
pubmed: 18388860
Proc Natl Acad Sci U S A. 1968 Feb;59(2):484-90
pubmed: 5238978
Mol Microbiol. 2016 Sep;101(6):968-81
pubmed: 27273832
J Bacteriol. 1995 May;177(9):2387-95
pubmed: 7730269
Science. 1971 Apr 30;172(3982):492-4
pubmed: 5550507
J Struct Biol. 2005 Oct;152(1):36-51
pubmed: 16182563
Mol Microbiol. 2011 Mar;79(6):1655-69
pubmed: 21244533
J Microsc. 2008 May;230(Pt 2):212-7
pubmed: 18445149
mBio. 2015 Jun 30;6(4):e00376
pubmed: 26126850
FEMS Microbiol Rev. 2016 Nov 1;40(6):831-854
pubmed: 28204529
FASEB J. 2014 Jul;28(7):3016-22
pubmed: 24675362
Trends Microbiol. 2006 Oct;14(10):439-43
pubmed: 16934472
J Struct Biol. 2010 Nov;172(2):169-79
pubmed: 20178848
Nat Protoc. 2006;1(6):2813-9
pubmed: 17406539
Cell Tissue Res. 2013 Apr;352(1):21-31
pubmed: 22940728
Plant Physiol. 2007 Mar;143(3):1385-97
pubmed: 17237189
J Struct Biol. 1996 Jan-Feb;116(1):71-6
pubmed: 8742726