Spatiotemporal Coordination of Rac1 and Cdc42 at the Whole Cell Level during Cell Ruffling.
FRET-based biosensors
Rho family GTPases
cytoskeletal regulation
morphodynamics
multiscale modeling
Journal
Cells
ISSN: 2073-4409
Titre abrégé: Cells
Pays: Switzerland
ID NLM: 101600052
Informations de publication
Date de publication:
15 06 2023
15 06 2023
Historique:
received:
31
03
2023
revised:
06
06
2023
accepted:
09
06
2023
medline:
29
6
2023
pubmed:
28
6
2023
entrez:
28
6
2023
Statut:
epublish
Résumé
Rho-GTPases are central regulators within a complex signaling network that controls cytoskeletal organization and cell movement. The network includes multiple GTPases, such as the most studied Rac1, Cdc42, and RhoA, along with their numerous effectors that provide mutual regulation through feedback loops. Here we investigate the temporal and spatial relationship between Rac1 and Cdc42 during membrane ruffling, using a simulation model that couples GTPase signaling with cell morphodynamics and captures the GTPase behavior observed with FRET-based biosensors. We show that membrane velocity is regulated by the kinetic rate of GTPase activation rather than the concentration of active GTPase. Our model captures both uniform and polarized ruffling. We also show that cell-type specific time delays between Rac1 and Cdc42 activation can be reproduced with a single signaling motif, in which the delay is controlled by feedback from Cdc42 to Rac1. The resolution of our simulation output matches those of time-lapsed recordings of cell dynamics and GTPase activity. Our data-driven modeling approach allows us to validate simulation results with quantitative precision using the same pipeline for the analysis of simulated and experimental data.
Identifiants
pubmed: 37371108
pii: cells12121638
doi: 10.3390/cells12121638
pmc: PMC10297213
pii:
doi:
Substances chimiques
CDC42 protein, human
EC 3.6.5.2
rac1 GTP-Binding Protein
EC 3.6.5.2
RAC1 protein, human
0
rho GTP-Binding Proteins
EC 3.6.5.2
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM136892
Pays : United States
Organisme : NIH HHS
ID : R01GM136892
Pays : United States
Commentaires et corrections
Type : UpdateOf
Références
Nat Cell Biol. 2005 Mar;7(3):270-7
pubmed: 15723051
Kybernetik. 1972 Dec;12(1):30-9
pubmed: 4663624
Cell Syst. 2015 Jul 29;1(1):37-50
pubmed: 26273703
Front Cell Dev Biol. 2021 Aug 20;9:685825
pubmed: 34490242
Curr Opin Cell Biol. 2012 Apr;24(2):245-53
pubmed: 22154943
Physiol Rev. 2013 Jan;93(1):269-309
pubmed: 23303910
Science. 1998 Jan 23;279(5350):509-14
pubmed: 9438836
J Cell Sci. 2012 May 15;125(Pt 10):2381-92
pubmed: 22344265
Sci Rep. 2015 Dec 04;5:17527
pubmed: 26634649
Nat Commun. 2018 Nov 16;9(1):4816
pubmed: 30446664
J Cell Sci. 2004 Mar 15;117(Pt 8):1291-300
pubmed: 15020669
Biochem Soc Trans. 2021 Jun 30;49(3):1425-1442
pubmed: 34196668
Curr Opin Cell Biol. 2008 Feb;20(1):35-40
pubmed: 18207721
Bioessays. 2000 Aug;22(8):753-60
pubmed: 10918306
Interface Focus. 2012 Aug 6;2(4):407-16
pubmed: 23919125
Elife. 2020 Jul 24;9:
pubmed: 32705984
Nat Chem Biol. 2017 Sep;13(9):994-1001
pubmed: 28759015
Small GTPases. 2015;6(2):71-80
pubmed: 25942647
Philos Trans R Soc Lond B Biol Sci. 2018 May 26;373(1747):
pubmed: 29632261
Proc Natl Acad Sci U S A. 2013 Jan 22;110(4):1339-44
pubmed: 23297209
Phys Biol. 2012 Aug;9(4):046005
pubmed: 22785332
Mol Biol Cell. 2004 Aug;15(8):3509-19
pubmed: 15169870
Biophys J. 2008 May 1;94(9):3684-97
pubmed: 18212014
Cells. 2019 Jul 21;8(7):
pubmed: 31330900
Oncogene. 2004 Dec 16;23(58):9369-80
pubmed: 15516977
Cell Rep. 2021 May 25;35(8):109157
pubmed: 34038718
Nature. 2002 Dec 12;420(6916):629-35
pubmed: 12478284
Oncogene. 2023 Mar;42(11):833-847
pubmed: 36693952
Nat Commun. 2018 Nov 7;9(1):4673
pubmed: 30405112
Thromb Haemost. 2010 Jan;103(1):40-55
pubmed: 20062930
Mol Biol Cell. 2017 Feb 1;28(3):370-380
pubmed: 28137950
Mol Cell Biol. 1995 Apr;15(4):1942-52
pubmed: 7891688
Philos Trans R Soc Lond B Biol Sci. 2013 Sep 23;368(1629):20130003
pubmed: 24062577
Mol Biol Cell. 2011 Jul 1;22(13):2212-20
pubmed: 21551075
J Theor Biol. 2004 Nov 7;231(1):49-67
pubmed: 15363929
EMBO J. 2011 Oct 05;30(19):3875-7
pubmed: 21975373
Curr Top Dev Biol. 2008;81:1-63
pubmed: 18023723
J R Soc Interface. 2021 Apr;18(177):20201047
pubmed: 33849339
Sci Rep. 2021 Sep 30;11(1):19512
pubmed: 34593939
FEBS Lett. 2008 Apr 30;582(10):1437-43
pubmed: 18381072
Nat Chem Biol. 2020 Aug;16(8):826-833
pubmed: 32424303
Front Cell Dev Biol. 2020 Apr 08;8:201
pubmed: 32322580
Science. 2010 Sep 24;329(5999):1616-20
pubmed: 20929839
Small GTPases. 2016 Oct;7(4):207-221
pubmed: 27628050
Nat Rev Mol Cell Biol. 2016 Aug;17(8):496-510
pubmed: 27301673
Nat Phys. 2022 Sep;18(9):1112-1121
pubmed: 37220497
J Cell Biol. 2003 Jun 9;161(5):845-51
pubmed: 12796474
Cell Signal. 2011 Aug;23(8):1291-8
pubmed: 21419846
Science. 2012 Apr 13;336(6078):175-9
pubmed: 22499937
J Cell Biol. 2018 Feb 5;217(2):447-457
pubmed: 29233866
J Math Biol. 2021 Mar 4;82(4):28
pubmed: 33660145
Dev Cell. 2020 Sep 14;54(5):608-623.e5
pubmed: 32877650
Small GTPases. 2012 Jan-Mar;3(1):45-52
pubmed: 22714417
Phys Rev E. 2020 Feb;101(2-1):022414
pubmed: 32168714
Mol Biol Cell. 2013 Feb;24(3):421-32
pubmed: 23264464
Small GTPases. 2014;5:e28997
pubmed: 25054920
Biophys J. 2006 Feb 15;90(4):1439-52
pubmed: 16326902
Cells. 2021 Jul 20;10(7):
pubmed: 34359999
Comput Phys Commun. 2007 Jun;176(11-12):670-681
pubmed: 18084624
Trends Cell Biol. 2011 Dec;21(12):718-26
pubmed: 21924908
PLoS Comput Biol. 2018 Apr 12;14(4):e1006095
pubmed: 29649212
Nature. 2009 Sep 3;461(7260):99-103
pubmed: 19693013
Mol Syst Biol. 2019 Mar 11;15(3):e8585
pubmed: 30858181
J Cell Sci. 2010 Jun 1;123(Pt 11):1841-50
pubmed: 20484664
J Am Chem Soc. 2016 Mar 2;138(8):2571-5
pubmed: 26863024
Mol Cell Biol. 2005 Jun;25(11):4602-14
pubmed: 15899863
Curr Opin Cell Biol. 2011 Feb;23(1):14-21
pubmed: 21093245