Optineurin links Hace1-dependent Rac ubiquitylation to integrin-mediated mechanotransduction to control bacterial invasion and cell division.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
13 10 2022
13 10 2022
Historique:
received:
24
09
2021
accepted:
30
09
2022
entrez:
13
10
2022
pubmed:
14
10
2022
medline:
18
10
2022
Statut:
epublish
Résumé
Extracellular matrix (ECM) elasticity is perceived by cells via focal adhesion structures, which transduce mechanical cues into chemical signalling to conform cell behavior. Although the contribution of ECM compliance to the control of cell migration or division is extensively studied, little is reported regarding infectious processes. We study this phenomenon with the extraintestinal Escherichia coli pathogen UTI89. We show that UTI89 takes advantage, via its CNF1 toxin, of integrin mechanoactivation to trigger its invasion into cells. We identify the HACE1 E3 ligase-interacting protein Optineurin (OPTN) as a protein regulated by ECM stiffness. Functional analysis establishes a role of OPTN in bacterial invasion and integrin mechanical coupling and for stimulation of HACE1 E3 ligase activity towards the Rac1 GTPase. Consistent with a role of OPTN in cell mechanics, OPTN knockdown cells display defective integrin-mediated traction force buildup, associated with limited cellular invasion by UTI89. Nevertheless, OPTN knockdown cells display strong mechanochemical adhesion signalling, enhanced Rac1 activation and increased cyclin D1 translation, together with enhanced cell proliferation independent of ECM stiffness. Together, our data ascribe a new function to OPTN in mechanobiology.
Identifiants
pubmed: 36229487
doi: 10.1038/s41467-022-33803-x
pii: 10.1038/s41467-022-33803-x
pmc: PMC9561704
doi:
Substances chimiques
Integrins
0
Cyclin D1
136601-57-5
Ubiquitin-Protein Ligases
EC 2.3.2.27
rac1 GTP-Binding Protein
EC 3.6.5.2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6059Informations de copyright
© 2022. The Author(s).
Références
Nat Rev Mol Cell Biol. 2008 Sep;9(9):690-701
pubmed: 18719708
Physiol Rev. 2013 Jan;93(1):269-309
pubmed: 23303910
Cell. 2009 Nov 25;139(5):891-906
pubmed: 19931152
Traffic. 2011 May;12(5):579-90
pubmed: 21291504
Science. 2005 Nov 18;310(5751):1139-43
pubmed: 16293750
Urology. 2018 Mar;113:235-240
pubmed: 29197522
Annu Rev Physiol. 2018 Feb 10;80:353-387
pubmed: 29433414
J Cell Biol. 2013 Jan 7;200(1):9-19
pubmed: 23295347
Nature. 2010 Nov 25;468(7323):533-8
pubmed: 21107423
J Cell Sci. 2019 Apr 3;132(7):
pubmed: 30837291
Trends Cell Biol. 2007 May;17(5):246-50
pubmed: 17363257
Nat Med. 2007 Sep;13(9):1060-9
pubmed: 17694067
Proc Natl Acad Sci U S A. 2011 Jun 7;108(23):9466-71
pubmed: 21593411
Biophys J. 2008 Jan 1;94(1):207-20
pubmed: 17827246
Methods Enzymol. 2006;406:447-56
pubmed: 16472677
J Cell Sci. 2008 Dec 1;121(Pt 23):3853-7
pubmed: 19020303
EMBO Rep. 2011 Mar;12(3):259-66
pubmed: 21311561
Nat Cell Biol. 2011 Jun;13(6):722-7
pubmed: 21572419
J Cell Sci. 2009 Jan 15;122(Pt 2):199-206
pubmed: 19118212
Nature. 1997 Jun 12;387(6634):729-33
pubmed: 9192901
Cell. 2011 Jul 8;146(1):148-63
pubmed: 21729786
Cell Motil Cytoskeleton. 2009 Aug;66(8):606-17
pubmed: 19459187
Nat Cell Biol. 2013 Apr;15(4):395-405
pubmed: 23455479
Cell. 2017 Nov 30;171(6):1397-1410.e14
pubmed: 29107331
Cancer Res. 2020 Jul 15;80(14):3009-3022
pubmed: 32366477
Exp Cell Res. 2013 Sep 10;319(15):2329-36
pubmed: 23648569
Biophys J. 1996 Jan;70(1):556-67
pubmed: 8770233
Nature. 2002 Dec 12;420(6916):629-35
pubmed: 12478284
Nucleic Acids Res. 2004 Jan 1;32(Database issue):D452-5
pubmed: 14681455
Curr Protoc Cell Biol. 2010 Jun;Chapter 10:Unit 10.16
pubmed: 20521229
Trends Cell Biol. 2018 May;28(5):356-367
pubmed: 29496292
PLoS Pathog. 2007 Jul;3(7):e100
pubmed: 17630833
Oncogene. 2013 Mar 28;32(13):1735-42
pubmed: 22614015
Nat Rev Microbiol. 2021 Jan;19(1):37-54
pubmed: 32826992
J Cell Biol. 2010 Mar 22;188(6):877-90
pubmed: 20308429
Nat Rev Microbiol. 2020 Apr;18(4):211-226
pubmed: 32071440
Pathog Dis. 2015 Dec;73(9):ftv091
pubmed: 26454272
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
Nat Biotechnol. 2013 Jul;31(7):638-46
pubmed: 23792630
Cell Rep. 2016 Mar 22;14(11):2668-82
pubmed: 26972014
Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18243-8
pubmed: 19805036
Science. 2004 Feb 6;303(5659):839-42
pubmed: 14764880
J Cell Sci. 2008 Sep 1;121(Pt 17):2795-804
pubmed: 18682496
J Cell Biol. 2012 Feb 6;196(3):363-74
pubmed: 22291038
Sci Rep. 2017 Jul 11;7(1):5117
pubmed: 28698636
J Biol Chem. 2000 Jul 28;275(30):22780-9
pubmed: 10807909
Nat Rev Mol Cell Biol. 2014 Dec;15(12):786-801
pubmed: 25415508
Cell Microbiol. 2002 Jan;4(1):19-28
pubmed: 11856170
Mol Microbiol. 1993 Sep;9(6):1247-54
pubmed: 7934938
Cell Rep. 2020 Aug 18;32(7):108050
pubmed: 32814053
Nature. 2017 Jun 22;546(7659):528-532
pubmed: 28614296
Nature. 2014 Jul 17;511(7509):319-25
pubmed: 25030168
J Cell Sci. 2011 Mar 1;124(Pt 5):679-83
pubmed: 21321325
J Cell Sci. 2012 Jul 1;125(Pt 13):3025-38
pubmed: 22797926
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
Genome Res. 2003 Nov;13(11):2498-504
pubmed: 14597658
Mol Biol Cell. 2018 Jul 1;29(13):1571-1589
pubmed: 29718765
Nat Cell Biol. 2019 Jan;21(1):25-31
pubmed: 30602766
Nat Cell Biol. 2011 Apr;13(4):383-93
pubmed: 21423176
Curr Opin Microbiol. 2005 Feb;8(1):10-5
pubmed: 15694851
J Immunol. 2014 Apr 1;192(7):3390-8
pubmed: 24585879
Nat Commun. 2016 Mar 07;7:10738
pubmed: 26948702
Nature. 2011 Sep 18;478(7368):260-3
pubmed: 21926999
Nat Protoc. 2018 Mar;13(3):530-550
pubmed: 29446774
Proc Natl Acad Sci U S A. 2018 Mar 13;115(11):2646-2651
pubmed: 29487208
J Cell Sci. 2011 Dec 1;124(Pt 23):3923-7
pubmed: 22194302
Small GTPases. 2012 Apr-Jun;3(2):102-6
pubmed: 22790197
J Cell Physiol. 2009 Aug;220(2):292-6
pubmed: 19415697
Cancer Biol Ther. 2002 May-Jun;1(3):226-31
pubmed: 12432268
J Cell Sci. 2010 Jul 15;123(Pt 14):2491-501
pubmed: 20592186
Nat Rev Mol Cell Biol. 2016 Aug;17(8):496-510
pubmed: 27301673
Nature. 2010 Jul 8;466(7303):263-6
pubmed: 20613844
PLoS Pathog. 2015 Mar 17;11(3):e1004732
pubmed: 25781937
Dev Cell. 2011 Nov 15;21(5):959-65
pubmed: 22036506
Cell. 2006 Dec 1;127(5):1015-26
pubmed: 17129785
Cell Cycle. 2011 May 15;10(10):1571-81
pubmed: 21478669
Curr Biol. 2009 Sep 29;19(18):1511-8
pubmed: 19765988
Nat Cell Biol. 2019 Nov;21(11):1357-1369
pubmed: 31659275
Mol Cell Proteomics. 2014 Sep;13(9):2513-26
pubmed: 24942700
Nat Commun. 2013;4:2180
pubmed: 23864022
J Cell Sci. 2014 Apr 1;127(Pt 7):1394-405
pubmed: 24481817
Cancer Cell. 2014 Jul 14;26(1):106-20
pubmed: 25026213
Curr Top Microbiol Immunol. 2017;399:155-174
pubmed: 27744507
J Cell Sci. 2010 May 1;123(Pt 9):1385-8
pubmed: 20410370
Nat Microbiol. 2021 Mar;6(3):401-412
pubmed: 33432150
Cancer Cell. 2005 Sep;8(3):241-54
pubmed: 16169468
Methods Cell Biol. 2015;125:289-308
pubmed: 25640435
Proc Natl Acad Sci U S A. 2010 Sep 21;107(38):16518-23
pubmed: 20823257
Clin Imaging. 2011 Jul-Aug;35(4):284-7
pubmed: 21724121
Cell. 2002 Nov 15;111(4):553-64
pubmed: 12437928
Rev Infect Dis. 1987 Sep-Oct;9 Suppl 5:S450-5
pubmed: 2825322
Cell. 2002 Jun 28;109(7):913-23
pubmed: 12110187
Sci Signal. 2014 Jun 17;7(330):ra57
pubmed: 24939893
Exp Cell Res. 2016 Apr 10;343(1):35-41
pubmed: 26518118
Elife. 2018 Jan 18;7:
pubmed: 29345620
Cell Tissue Res. 2014 Nov;358(2):567-83
pubmed: 25096716
Proc Natl Acad Sci U S A. 2014 Sep 9;111(36):13075-80
pubmed: 25157134
J Cell Biol. 2003 Oct 27;163(2):409-19
pubmed: 14581461
Nat Cell Biol. 2005 Sep;7(9):901-8
pubmed: 16113676
Cell Microbiol. 2020 May;22(5):e13196
pubmed: 32083802
Biochim Biophys Acta. 2016 Mar;1858(3):538-45
pubmed: 26299820
Nature. 2013 Apr 11;496(7444):233-7
pubmed: 23542589
Nat Rev Mol Cell Biol. 2019 Aug;20(8):457-473
pubmed: 31182865
Cell Host Microbe. 2008 Oct 16;4(4):314-23
pubmed: 18854236
J Cell Biol. 2013 Aug 5;202(3):545-61
pubmed: 23918940
Nat Cell Biol. 2008 Sep;10(9):1039-50
pubmed: 19160484
Curr Biol. 2016 Jan 11;26(1):27-37
pubmed: 26725196
Nat Commun. 2014 Dec 10;5:5749
pubmed: 25494455
Nat Cell Biol. 2016 May;18(5):540-8
pubmed: 27065098