Coordinated Ras and Rac Activity Shapes Macropinocytic Cups and Enables Phagocytosis of Geometrically Diverse Bacteria.

Bacteria Cell Cycle Proteins Dictyostelium / cytology Phagocytosis Pinocytosis rac GTP-Binding Proteins / metabolism ras Proteins / metabolism
Dictyostelium Rac Ras macropinocytosis phagocytosis small GTPase

Journal

Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782

Informations de publication

Date de publication:
03 08 2020
Historique:
received: 25 10 2019
revised: 20 04 2020
accepted: 14 05 2020
pubmed: 13 6 2020
medline: 20 8 2021
entrez: 13 6 2020
Statut: ppublish

Résumé

Engulfment of extracellular material by phagocytosis or macropinocytosis depends on the ability of cells to generate specialized cup-shaped protrusions. To effectively capture and internalize their targets, these cups are organized into a ring or ruffle of actin-driven protrusion encircling a non-protrusive interior domain. These functional domains depend on the combined activities of multiple Ras and Rho family small GTPases, but how their activities are integrated and differentially regulated over space and time is unknown. Here, we show that the amoeba Dictyostelium discoideum coordinates Ras and Rac activity using the multidomain protein RGBARG (RCC1, RhoGEF, BAR, and RasGAP-containing protein). We find RGBARG uses a tripartite mechanism of Ras, Rac, and phospholipid interactions to localize at the protruding edge and interface with the interior of both macropinocytic and phagocytic cups. There, we propose RGBARG shapes the protrusion by expanding Rac activation at the rim while suppressing expansion of the active Ras interior domain. Consequently, cells lacking RGBARG form enlarged, flat interior domains unable to generate large macropinosomes. During phagocytosis, we find that disruption of RGBARG causes a geometry-specific defect in engulfing rod-shaped bacteria and ellipsoidal beads. This demonstrates the importance of coordinating small GTPase activities during engulfment of more complex shapes and thus the full physiological range of microbes, and how this is achieved in a model professional phagocyte.

Identifiants

DOI: 10.1016/j.cub.2020.05.049 PMID: 32531280 PMC: PMC7416115
pubmed: 32531280
pii: S0960-9822(20)30736-3
doi: 10.1016/j.cub.2020.05.049
pmc: PMC7416115
pii:
doi:

Substances chimiques

Cell Cycle Proteins 0
rac GTP-Binding Proteins EC 3.6.5.2
ras Proteins 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

2912-2926.e5

Subventions

Organisme : Medical Research Council
ID : MR/N013840/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_U105115237
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0700091
Pays : United Kingdom
Organisme : Wellcome Trust
ID : GR077544AIA
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/J014443/1
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Cell Microbiol. 2006 Jan;8(1):139-48
pubmed: 16367873
J Cell Sci. 2000 Feb;113 ( Pt 4):709-19
pubmed: 10652263
J Cell Biol. 2001 Oct 1;155(1):19-25
pubmed: 11581283
Nature. 2002 Aug 15;418(6899):790-3
pubmed: 12181570
Mol Biol Cell. 2002 Oct;13(10):3508-20
pubmed: 12388753
Plasmid. 2009 Mar;61(2):110-8
pubmed: 19063918
J Cell Sci. 2004 Dec 15;117(Pt 26):6497-509
pubmed: 15572406
J Cell Biol. 1996 Dec;135(5):1249-60
pubmed: 8947549
Elife. 2016 Dec 13;5:
pubmed: 27960076
Proc Natl Acad Sci U S A. 2016 Nov 22;113(47):E7464-E7473
pubmed: 27821733
EMBO J. 2004 Oct 27;23(21):4177-89
pubmed: 15470506
Pharm Res. 2009 Jan;26(1):244-9
pubmed: 18548338
J Vis Exp. 2018 Sep 10;(139):
pubmed: 30247467
Elife. 2015 Mar 27;4:
pubmed: 25815683
J Biol Chem. 1999 Jan 15;274(3):1240-7
pubmed: 9880492
J Cell Biol. 2014 Feb 17;204(4):497-505
pubmed: 24535823
Proc Natl Acad Sci U S A. 2019 Jan 22;116(4):1289-1298
pubmed: 30622175
J Cell Sci. 2000 Jun;113 ( Pt 12):2253-65
pubmed: 10825297
J Exp Med. 1995 Aug 1;182(2):389-400
pubmed: 7629501
Philos Trans R Soc Lond B Biol Sci. 2019 Feb 4;374(1765):20180158
pubmed: 30967007
Mol Biol Cell. 2004 Aug;15(8):3509-19
pubmed: 15169870
Mol Biol Cell. 2000 Oct;11(10):3453-67
pubmed: 11029048
J Cell Sci. 2019 Jan 24;132(2):
pubmed: 30617109
PLoS Pathog. 2019 Feb 7;15(2):e1007551
pubmed: 30730983
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Cell Microbiol. 2007 Nov;9(11):2716-33
pubmed: 17587329
J Cell Sci. 2018 Mar 21;131(6):
pubmed: 29440238
Cell. 1995 Apr 7;81(1):53-62
pubmed: 7536630
J Cell Sci. 1997 Jan;110 ( Pt 2):105-12
pubmed: 9044041
EMBO J. 1998 Nov 2;17(21):6219-29
pubmed: 9799231
Methods Mol Biol. 2006;346:423-38
pubmed: 16957305
J Cell Sci. 2000 Apr;113 ( Pt 8):1427-34
pubmed: 10725225
Genome Biol. 2008 Apr 22;9(4):R75
pubmed: 18430225
Scand J Immunol. 1977;6(8):797-807
pubmed: 561436
Immunity. 1995 Dec;3(6):783-91
pubmed: 8777723
Science. 2004 Jan 23;303(5657):495-9
pubmed: 14645856
Curr Biol. 1998 Dec 17-31;8(25):1347-56
pubmed: 9889097
Nat Commun. 2015 Oct 14;6:8623
pubmed: 26465210
J Exp Med. 1975 Nov 1;142(5):1263-82
pubmed: 1194852
Trends Cell Biol. 2006 Oct;16(10):493-8
pubmed: 16949824
Nat Rev Mol Cell Biol. 2008 Aug;9(8):639-49
pubmed: 18612320
Eukaryot Cell. 2006 Oct;5(10):1648-63
pubmed: 16950926
J Exp Med. 1997 Nov 3;186(9):1487-94
pubmed: 9348306
Curr Biol. 2000 Jul 13;10(14):839-48
pubmed: 10899002
Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):4930-4
pubmed: 16549762
Methods Mol Biol. 2013;983:59-92
pubmed: 23494302
Science. 1998 Nov 27;282(5394):1717-21
pubmed: 9831565
J Cell Biol. 2018 Nov 5;217(11):3873-3885
pubmed: 30150290
PLoS One. 2018 May 30;13(5):e0196809
pubmed: 29847546
J Cell Biol. 2001 Jun 25;153(7):1369-80
pubmed: 11425868
Philos Trans R Soc Lond B Biol Sci. 2019 Feb 4;374(1765):20180146
pubmed: 30967000
J Cell Sci. 2013 Sep 15;126(Pt 18):4296-307
pubmed: 23843627
Sci Rep. 2013;3:2385
pubmed: 23924974
Nature. 2013 May 30;497(7451):633-7
pubmed: 23665962
Biotechniques. 2001 Nov;31(5):1140-2, 1144, 1146-9
pubmed: 11730020
BMC Syst Biol. 2010 Nov 08;4:149
pubmed: 21059234
Cell. 2007 Jun 1;129(5):865-77
pubmed: 17540168
J Cell Sci. 2016 Jul 15;129(14):2697-705
pubmed: 27352861
J Cell Sci. 2017 Sep 15;130(18):3158-3172
pubmed: 28778987
Traffic. 2006 Sep;7(9):1194-212
pubmed: 17004322
FEBS J. 2017 Nov;284(22):3778-3790
pubmed: 28544479
Eur J Cell Biol. 2006 Sep;85(9-10):947-59
pubmed: 16762450
Science. 1986 Sep 5;233(4768):1061-8
pubmed: 3090687
Methods Mol Biol. 2013;983:383-402
pubmed: 23494319
Biochem J. 1970 Sep;119(2):171-4
pubmed: 5530748
Exp Cell Res. 2007 Apr 15;313(7):1496-507
pubmed: 17368443

Auteurs

Catherine M Buckley (CM)

Department of Biomedical Sciences, University of Sheffield, Sheffield S10 2TT, UK.

Henderikus Pots (H)

Department of Cell Biochemistry, University of Groningen, Groningen 9747 AG, Netherlands.

Aurelie Gueho (A)

Department of Biochemistry, Faculty of Sciences, Sciences II, University of Geneva, CH-1211-Geneva-4, Switzerland.

James H Vines (JH)

Department of Biomedical Sciences, University of Sheffield, Sheffield S10 2TT, UK.

Christopher J Munn (CJ)

Department of Biomedical Sciences, University of Sheffield, Sheffield S10 2TT, UK.

Ben A Phillips (BA)

Department of Biomedical Sciences, University of Sheffield, Sheffield S10 2TT, UK.

Bernd Gilsbach (B)

German Centre for Neurodegenerative Diseases, Tübingen 72076, Germany.

David Traynor (D)

MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK.

Anton Nikolaev (A)

Department of Biomedical Sciences, University of Sheffield, Sheffield S10 2TT, UK.

Thierry Soldati (T)

Department of Biochemistry, Faculty of Sciences, Sciences II, University of Geneva, CH-1211-Geneva-4, Switzerland.

Andrew J Parnell (AJ)

Department of Physics and Astronomy, University of Sheffield, Sheffield S3 7RH, UK.

Arjan Kortholt (A)

Department of Cell Biochemistry, University of Groningen, Groningen 9747 AG, Netherlands.

Jason S King (JS)

Department of Biomedical Sciences, University of Sheffield, Sheffield S10 2TT, UK. Electronic address: jason.king@sheffield.ac.uk.

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Classifications MeSH

Recherchemedicale.com › Bactéries › Coordinated Ras and Rac Activity Shapes...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines du cycle cellulaire › Coordinated Ras and Rac Activity Shapes...
Recherchemedicale.com › Eucaryotes › Amoebozoa › Mycetozoa › Dictyosteliida › Dictyostelium › Coordinated Ras and Rac Activity Shapes...
Recherchemedicale.com › Phénomènes du système immunitaire › Phagocytose › Coordinated Ras and Rac Activity Shapes...
Recherchemedicale.com › Phénomènes physiologiques cellulaires › Endocytose › Pinocytose › Coordinated Ras and Rac Activity Shapes...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Protéines G › Protéines G monomériques › Protéines G rho › Protéines G rac › Coordinated Ras and Rac Activity Shapes...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Protéines G › Protéines G monomériques › Protéines G ras › Coordinated Ras and Rac Activity Shapes...