Seeing is believing: tools to study the role of Rho GTPases during cytokinesis

References

• Basant A, Glotzer M. Spatiotemporal regulation of RhoA during Cytokinesis. Curr. Biol. 2018;28(9):R570–R580.
   PubMed Web of Science ®Google Scholar
• Chircop M. Rho GTPases as regulators of mitosis and cytokinesis in mammalian cells. Small GTPases. 2014;5(2):e29770.
   PubMedGoogle Scholar
• Green RA, Paluch E, Oegema K. Cytokinesis in animal cells. Annu Rev Cell Dev Biol. 2012;28(1):29–58.
   PubMedGoogle Scholar
• Leite J, Osorio DS, Sobral AF, et al. Network contractility during Cytokinesis-from molecular to global views. Biomolecules. 2019;9(5):194.
   PubMed Web of Science ®Google Scholar
• Somers WG, Saint R. A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. Dev Cell. 2003;4(1):29–39.
   PubMed Web of Science ®Google Scholar
• Yüce O, Piekny A, Glotzer M. An Ect2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol. 2005;170(4):571–582.
   PubMed Web of Science ®Google Scholar
• Nishimura Y, Yonemura S. Centralspindlin regulates Ect2 and RhoA accumulation at the equatorial cortex during cytokinesis. J Cell Sci. 2006;119(1):104–114.
   PubMed Web of Science ®Google Scholar
• Zanin E, Desai A, Poser I, et al. A conserved RhoGAP limits M phase contractility and coordinates with microtubule asters to confine RhoA during cytokinesis. Dev Cell. 2013;26(5):496–510.
   PubMed Web of Science ®Google Scholar
• Kosako H, Yoshida T, Matsumura F, et al. Rho-kinase/ROCK is involved in cytokinesis through the phosphorylation of myosin light chain and not ezrin/radixin/moesin proteins at the cleavage furrow. Oncogene. 2000;19(52):6059–6064.
   PubMed Web of Science ®Google Scholar
• Rose R, Weyand M, Lammers M, et al. Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature. 2005;435(7041):513–518.
   PubMed Web of Science ®Google Scholar
• Glotzer M. Cytokinesis in Metazoa and Fungi. Cold Spring Harb Perspect Biol. 2017;9(10):a022343.
   PubMed Web of Science ®Google Scholar
• Frenette P, Haines E, Loloyan M, et al. An anillin-Ect2 complex stabilizes central spindle microtubules at the cortex during cytokinesis. PloS One. 2012;7(4):e34888.
   PubMed Web of Science ®Google Scholar
• Mishima M, Kaitna S, Glotzer M. Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell. 2002;2(1):41–54.
   PubMed Web of Science ®Google Scholar
• Glotzer M. Cytokinesis: centralspindlin moonlights as a membrane anchor. Curr Biol. 2013;23(4):R145–R147.
   PubMed Web of Science ®Google Scholar
• Lekomtsev S, Su KC, Pye VE, et al. Centralspindlin links the mitotic spindle to the plasma membrane during cytokinesis. Nature. 2012;492(7428):276–279.
   PubMed Web of Science ®Google Scholar
• Su KC, Takaki T, Petronczki M. Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev. Cell. 2011;21(6):1104–1115.
   PubMed Web of Science ®Google Scholar
• Kotýnková K, Su KC, West SC, et al. Plasma membrane association but not midzone recruitment of RhoGEF ECT2 is essential for cytokinesis. Cell Rep. 2016;17(10):2672–2686.
   PubMed Web of Science ®Google Scholar
• Petronczki M, Glotzer M, Kraut N, et al. Polo-like kinase 1 triggers the initiation of cytokinesis in human cells by promoting recruitment of the RhoGEF Ect2 to the central spindle. Dev Cell. 2007;12(5):713–725.
   PubMed Web of Science ®Google Scholar
• Wolfe BA, Takaki T, Petronczki M, et al. Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol. 2009;7(5):e1000110.
   PubMed Web of Science ®Google Scholar
• Gómez-Cavazos JS, Lee K-Y, Lara-González P, et al. A Non-canonical BRCT-Phosphopeptide recognition mechanism underlies RhoA activation in cytokinesis. Curr Biol. 2020;30(16):3101–3115.e3111.
   PubMed Web of Science ®Google Scholar
• Basant A, Lekomtsev S, Tse YC, et al. aurora b kinase promotes cytokinesis by inducing centralspindlin oligomers that associate with the plasma membrane. Dev. Cell. 2015;33(2):204–215.
   PubMed Web of Science ®Google Scholar
• Adriaans IE, Basant A, Ponsioen B, et al. PLK1 plays dual roles in centralspindlin regulation during cytokinesis. J Cell Biol. 2019;218(4):1250–1264.
   PubMed Web of Science ®Google Scholar
• Chen M, Pan H, Sun L, et al. Structure and regulation of human epithelial cell transforming 2 protein. Proc. Natl. Acad. Sci. U. S. A. 2020;117(2):1027–1035.
   PubMed Web of Science ®Google Scholar
• Zhang D, Glotzer M. The RhoGAP activity of CYK-4/MgcRacGAP functions non-canonically by promoting RhoA activation during cytokinesis. Elife. 2015;4. DOI:10.7554/eLife.08898
   Web of Science ®Google Scholar
• Budnar S, Husain KB, Gomez GA, et al. Anillin PRromotes cell contractility by cyclic resetting of RhoA residence kinetics. Dev Cell. 2019;49(6):894–906.e812.
   PubMed Web of Science ®Google Scholar
• Field CM, Alberts BM. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol. 1995;131(1):165–178.
   PubMed Web of Science ®Google Scholar
• Piekny AJ, Maddox AS. The myriad roles of Anillin during cytokinesis. Semin Cell Dev Biol. 2010;21:881–891.
   Google Scholar
• Piekny AJ, Glotzer M. Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr Biol. 2008;18(1):30–36.
   PubMed Web of Science ®Google Scholar
• Sun L, Guan R, Lee IJ, et al. Mechanistic insights into the anchorage of the contractile ring by anillin and Mid1. Dev Cell. 2015;33(4):413–426.
   PubMed Web of Science ®Google Scholar
• Bell KR, Werner ME, Doshi A, et al. Novel cytokinetic ring components drive negative feedback in cortical contractility. Mol Biol Cell. 2020;31(15):1623–1636.
   PubMed Web of Science ®Google Scholar
• Birkenfeld J, Nalbant P, Bohl BP, et al. GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev Cell. 2007;12(5):699–712.
   PubMed Web of Science ®Google Scholar
• Martz MK, Grabocka E, Beeharry N, et al. Leukemia-associated RhoGEF (LARG) is a novel RhoGEF in cytokinesis and required for the proper completion of abscission. Mol Biol Cell. 2013;24(18):2785–2794.
   PubMed Web of Science ®Google Scholar
• Su L, Agati JM, Parsons SJ. p190RhoGAP is cell cycle regulated and affects cytokinesis. J Cell Biol. 2003;163(3):571–582.
   PubMed Web of Science ®Google Scholar
• Su L, Pertz O, Mikawa M, et al. p190RhoGAP negatively regulates Rho activity at the cleavage furrow of mitotic cells. Exp Cell Res. 2009;315(8):1347–1359.
   PubMed Web of Science ®Google Scholar
• Wu D, Asiedu M, Adelstein RS, et al. A novel guanine nucleotide exchange factor MyoGEF is required for cytokinesis. Cell Cycle. 2006;5(11):1234–1239.
   Google Scholar
• Jantsch-Plunger V, Gönczy P, Romano A, et al. CYK-4: a Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J Cell Biol. 2000;149(7):1391–1404.
   PubMed Web of Science ®Google Scholar
• Canman JC, Lewellyn L, Laband K, et al. Inhibition of Rac by the GAP activity of centralspindlin is essential for cytokinesis. Science. 2008;322(5907):1543–1546.
   PubMed Web of Science ®Google Scholar
• Loria A, Longhini KM, Glotzer M. The RhoGAP domain of CYK-4 has an essential role in RhoA activation. Curr Biol. 2012;22(3):213–219.
   PubMed Web of Science ®Google Scholar
• Basant A, Glotzer M. A GAP that Divides. F1000Res. 2017;6:1788.
   PubMedGoogle Scholar
• Tse YC, Werner M, Longhini KM, et al. RhoA activation during polarization and cytokinesis of the early Caenorhabditis elegans embryo is differentially dependent on NOP-1 and CYK-4. Mol Biol Cell. 2012;23(20):4020–4031.
   PubMed Web of Science ®Google Scholar
• Bastos RN, Penate X, Bates M, et al. CYK4 inhibits Rac1-dependent PAK1 and ARHGEF7 effector pathways during cytokinesis. J Cell Biol. 2012;198(5):865–880.
   PubMed Web of Science ®Google Scholar
• Yoshizaki H, Ohba Y, Kurokawa K, et al. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J Cell Biol. 2003;162(2):223–232.
   PubMed Web of Science ®Google Scholar
• Zhang W, Robinson DN. Balance of actively generated contractile and resistive forces controls cytokinesis dynamics. Proc Natl Acad Sci U.S.A. 2005;102:7186–7191.
   Google Scholar
• Girard KD, Chaney C, Delannoy M, et al. Dynacortin contributes to cortical viscoelasticity and helps define the shape changes of cytokinesis. EMBO J. 2004;23(7):1536–1546.
   PubMed Web of Science ®Google Scholar
• Robinson DN, Cavet G, Warrick HM, et al. Quantitation of the distribution and flux of myosin-II during cytokinesis. BMC Cell Biol. 2002;3(1):4.
   PubMedGoogle Scholar
• Rosenblatt J, Cramer LP, Baum B, et al. Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell. 2004;117(3):361–372.
   PubMed Web of Science ®Google Scholar
• Wang Y-L. The mechanism of cortical ingression during early cytokinesis: thinking beyond the contractile ring hypothesis. Trends Cell Biol. 2005;15(11):581–588.
   PubMed Web of Science ®Google Scholar
• Crawford JM, Harden N, Leung T, et al. Cellularization in Drosophila melanogaster is disrupted by the inhibition of rho activity and the activation of Cdc42 function. Dev Biol. 1998;204(1):151–164.
   PubMed Web of Science ®Google Scholar
• Gotta M, Abraham MC, Ahringer J. CDC-42 controls early cell polarity and spindle orientation in C. elegans. Curr Biol. 2001;11(7):482–488.
   PubMed Web of Science ®Google Scholar
• Drechsel DN, Hyman AA, Hall A, et al. A requirement for Rho and Cdc42 during cytokinesis in Xenopus embryos. Curr Biol. 1997;7(1):12–23.
   PubMed Web of Science ®Google Scholar
• Dutartre H, Davoust J, Gorvel JP, et al. Cytokinesis arrest and redistribution of actin-cytoskeleton regulatory components in cells expressing the Rho GTPase CDC42Hs. J Cell Sci. 1996;109(2):367–377.
   PubMedGoogle Scholar
• Jordan SN, Davies T, Zhuravlev Y, et al. Cortical PAR polarity proteins promote robust cytokinesis during asymmetric cell division. J Cell Biol. 2016;212(1):39–49.
   PubMed Web of Science ®Google Scholar
• Schenk C, Bringmann H, Hyman AA, et al. Cortical domain correction repositions the polarity boundary to match the cytokinesis furrow in C. elegans embryos. Elegans Embryos. Development (Cambridge, England) 2010;137(10):1743–1753.
   PubMed Web of Science ®Google Scholar
• Spiering D, Hodgson L. Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adh Migr. 2011;5(2):170–180.
   PubMed Web of Science ®Google Scholar
• Reid T, Furuyashiki T, Ishizaki T, et al. Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rho-binding domain. J Biol Chem. 1996;271(23):13556–13560.
   PubMed Web of Science ®Google Scholar
• Ren XD, Kiosses WB, Schwartz MA. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 1999;18(3):578–585.
   PubMed Web of Science ®Google Scholar
• Boulter E, Garcia-Mata R, Guilluy C, et al. Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat Cell Biol. 2010;12(5):477–483.
   PubMed Web of Science ®Google Scholar
• Yonemura S, Hirao-Minakuchi K, Nishimura Y. Rho localization in cells and tissues. Exp Cell Res. 2004;295(2):300–314.
   PubMed Web of Science ®Google Scholar
• Piekny A, Werner M, Glotzer M. Cytokinesis: welcome to the Rho zone. Trends Cell Biol. 2005;15(12):651–658.
   PubMed Web of Science ®Google Scholar
• Jones GA, Bradshaw DS. Resonance Energy Transfer: from Fundamental Theory to Recent Applications. Front Phys. 2019;7:1–19.
   Web of Science ®Google Scholar
• Donnelly SK, Bravo-Cordero JJ, Hodgson L. Rho GTPase isoforms in cell motility: don’t fret, we have FRET. Cell Adh Migr. 2014;8(6):526–534.
   PubMed Web of Science ®Google Scholar
• Kraynov VS, Chamberlain C, Bokoch GM, et al. Localized Rac activation dynamics visualized in living cells. Science. 2000;290(5490):333–337.
   PubMed Web of Science ®Google Scholar
• Itoh RE, Kurokawa K, Ohba Y, et al. Activation of rac and cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol Cell Biol. 2002;22(18):6582–6591.
   PubMed Web of Science ®Google Scholar
• Pertz O, Hodgson L, Klemke RL, et al. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature. 2006;440(7087):1069–1072.
   PubMed Web of Science ®Google Scholar
• van Unen J, Reinhard NR, Yin T, et al. Plasma membrane restricted RhoGEF activity is sufficient for RhoA-mediated actin polymerization. Sci Rep. 2015;5(1):14693.
   PubMedGoogle Scholar
• Reinhard NR, van Helden SF, Anthony EC, et al. Spatiotemporal analysis of RhoA/B/C activation in primary human endothelial cells. Sci Rep. 2016;6(1):25502.
   PubMedGoogle Scholar
• Bement WM, Benink HA, von Dassow G. A microtubule-dependent zone of active RhoA during cleavage plane specification. J Cell Biol. 2005;170(1):91–101.
   PubMed Web of Science ®Google Scholar
• Benink HA, Bement WM. Concentric zones of active RhoA and Cdc42 around single cell wounds. J Cell Biol. 2005;168(3):429–439.
   PubMed Web of Science ®Google Scholar
• Bassi ZI, Verbrugghe KJ, Capalbo L, et al. Sticky/Citron kinase maintains proper RhoA localization at the cleavage site during cytokinesis. J Cell Biol. 2011;195(4):595–603.
   PubMed Web of Science ®Google Scholar
• Reyes CC, Jin M, Breznau EB, et al. Anillin Regulates Cell-Cell Junction Integrity by Organizing Junctional Accumulation of Rho-GTP and Actomyosin. Curr Biol. 2014;24(11):1263–1270.
   PubMed Web of Science ®Google Scholar
• Xiao S, Tong C, Yang Y, et al. Mitotic cortical waves predict future division sites by encoding positional and size information. Dev Cell. 2017;43(4):493–506 e493.
   PubMed Web of Science ®Google Scholar
• Mahlandt EK, Arts JJG, van der Meer WJ, et al. 2021. Visualizing endogenous RhoA activity with an improved localization-based, genetically encoded biosensor. bioRxiv:2021.2002.2008.430250.
   Google Scholar
• Motegi F, Velarde NV, Piano F, et al. Two phases of astral microtubule activity during cytokinesis in C. elegans embryos. Dev Cell. 2006;10(4):509–520.
   PubMed Web of Science ®Google Scholar
• Acharya BR, Nestor-Bergmann A, Liang X, et al. A Mechanosensitive RhoA pathway that protects epithelia against acute tensile stress. Dev Cell. 2018;47(4):439–452.e436.
   PubMed Web of Science ®Google Scholar
• Michaux JB, Robin FB, McFadden WM, et al. Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo. J Cell Biol. 2018;217:4230–4252.
   PubMed Web of Science ®Google Scholar
• Munjal A, Philippe J-M, Munro E, et al. A self-organized biomechanical network drives shape changes during tissue morphogenesis. Nature. 2015;524(7565):351–355.
   PubMed Web of Science ®Google Scholar
• Priya R, Gomez GA, Budnar S, et al. Feedback regulation through myosin II confers robustness on RhoA signalling at E-cadherin junctions. Nat Cell Biol. 2015;17(10):1282–1293.
   PubMed Web of Science ®Google Scholar
• Morris RG, Husain KB, Budnar S, et al. Anillin: the First Proofreading-like Scaffold? Bioessays. 2020;42(10):e2000055.
   PubMed Web of Science ®Google Scholar
• Kumfer KT, Cook SJ, Squirrell JM, et al. CGEF-1 and CHIN-1 regulate CDC-42 activity during asymmetric division in the Caenorhabditis elegans Embryo. Mol. Biol. Cell. 2010;21(2):266–277.
   PubMed Web of Science ®Google Scholar
• Golding AE, Visco I, Bieling P, et al. Extraction of active rhoGTPases by rhoGDI regulates spatiotemporal patterning of rhogtpases. Elife. 2019;8:1–26.
   Web of Science ®Google Scholar
• Davenport NR, Sonnemann KJ, Eliceiri KW, et al. Membrane dynamics during cellular wound repair. Mol. Biol. Cell. 2016;27(14):2272–2285.
   PubMed Web of Science ®Google Scholar
• Wagner E, Glotzer M. Local RhoA activation induces cytokinetic furrows independent of spindle position and cell cycle stage. J Cell Biol. 2016;213(6):641–649.
   PubMed Web of Science ®Google Scholar
• Harper SM, Neil LC, Gardner KH. Structural basis of a phototropin light switch. Science. 2003;301(5639):1541–1544. (80-.).
   PubMed Web of Science ®Google Scholar
• Bugaj LJ, Choksi AT, Mesuda CK, et al. Optogenetic protein clustering and signaling activation in mammalian cells. Nat Methods. 2013;10(3):249–252.
   PubMed Web of Science ®Google Scholar
• Peterman E, Valius M, Prekeris R. CLIC4 is a cytokinetic cleavage furrow protein that regulates cortical cytoskeleton stability during cell division. J Cell Sci. 2020;133:jcs241117.
   PubMed Web of Science ®Google Scholar
• Wang H, Vilela M, Winkler A, et al. LOVTRAP: an optogenetic system for photoinduced protein dissociation. Nat Methods. 2016;13(9):755–758.
   PubMed Web of Science ®Google Scholar
• Lambert TJ. FPbase: a community-editable fluorescent protein database. Nat Methods. 2019;16(4):277–278.
   PubMed Web of Science ®Google Scholar
• Datta R, Heaster T, Sharick J, et al. Fluorescence lifetime imaging microscopy: fundamentals and advances in instrumentation, analysis, and applications. J Biomed Opt. 2020;25(7):71203.
   PubMed Web of Science ®Google Scholar
• Mamontova AV, Solovyev ID, Savitsky AP, et al. Bright GFP with subnanosecond fluorescence lifetime. Sci Rep. 2018;8(1):13224.
   PubMedGoogle Scholar
• Keller L, Bery N, Tardy C, et al. Selection and characterization of a nanobody biosensor of GTP-Bound RHO Activities. Antibodies (Basel). 2019;8(1):8.
   PubMedGoogle Scholar
• Xia Z, Rao J. Biosensing and imaging based on bioluminescence resonance energy transfer. Curr Opin Biotechnol. 2009;20(1):37–44.
   PubMed Web of Science ®Google Scholar
• Bery N, Keller L, Soulié M, et al. A targeted protein degradation Cell-Based Screening for Nanobodies Selective toward the Cellular RHOB GTP-Bound Conformation. Cell Chem Biol. 2019;26(11):1544–1558.e1546.
   PubMed Web of Science ®Google Scholar
• Kodama Y, Hu CD. Bimolecular fluorescence complementation (BiFC): a 5-year update and future perspectives. Biotechniques. 2012;53(5):285–298.
   PubMed Web of Science ®Google Scholar
• Cabantous S, Nguyen HB, Pedelacq J-D, et al. A new protein-protein interaction sensor based on tripartite split-GFP association. Sci Rep. 2013;3(1):2854.
   PubMedGoogle Scholar
• Koraïchi F, Gence R, Bouchenot C, et al. High-content tripartite split-GFP cell-based assays to screen for modulators of small GTPase activation. J Cell Sci. 2018;131(1):1–12.
   Web of Science ®Google Scholar
• Wehr MC, Rossner MJ. Split protein biosensor assays in molecular pharmacological studies. Drug Discov Today. 2016;21(3):415–429.
   PubMed Web of Science ®Google Scholar
• Kamiyama D, Sekine S, Barsi-Rhyne B, et al. Versatile protein tagging in cells with split fluorescent protein. Nat Commun. 2016;7(1):11046.
   PubMedGoogle Scholar
• Pedelacq JD, Cabantous S. Development and applications of superfolder and split fluorescent protein detection systems in biology. Int J Mol Sci. 2019;20(14):3479.
   PubMed Web of Science ®Google Scholar
• Tebo AG, Gautier A. A split fluorescent reporter with rapid and reversible complementation. Nat Commun. 2019;10:1–8.
   PubMed Web of Science ®Google Scholar
• Shcherbakova DM, Cox Cammer N, Huisman TM, et al. Direct multiplex imaging and optogenetics of Rho GTPases enabled by near-infrared FRET. Nat Chem Biol. 2018;14(6):591–600.
   PubMed Web of Science ®Google Scholar
• Michaelson D, Silletti J, Murphy G, et al. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol. 2001;152(1):111–126.
   PubMed Web of Science ®Google Scholar
• Machacek M, Hodgson L, Welch C, et al. Coordination of Rho GTPase activities during cell protrusion. Nature. 2009;461(7260):99–103.
   PubMed Web of Science ®Google Scholar
• Fritz RD, Letzelter M, Reimann A, et al. A versatile toolkit to produce sensitive FRET biosensors to visualize signaling in time and space. Sci Signal. 2013;6(285):rs12.
   PubMed Web of Science ®Google Scholar
• Hodgson L, Spiering D, Sabouri-Ghomi M, et al. FRET binding antenna reports spatiotemporal dynamics of GDI-Cdc42 GTPase interactions. Nat Chem Biol. 2016;12(10):802–809.
   PubMed Web of Science ®Google Scholar
• Laviv T, Kim BB, Chu J, et al. Simultaneous dual-color fluorescence lifetime imaging with novel red-shifted fluorescent proteins. Nat Methods. 2016;13(12):989–992.
   PubMed Web of Science ®Google Scholar
• Nobis M, Herrmann D, Warren SC, et al. A RhoA-FRET Biosensor Mouse for Intravital Imaging in Normal Tissue Homeostasis and Disease Contexts. Cell Rep. 2017;21(1):274–288.
   PubMed Web of Science ®Google Scholar
• Zawistowski JS, Sabouri-Ghomi M, Danuser G, et al. A RhoC biosensor reveals differences in the activation kinetics of RhoA and RhoC in migrating cells. PloS One. 2013;8(11):e79877.
   PubMed Web of Science ®Google Scholar
• Hanna S, Miskolci V, Cox D, et al. A new genetically encoded single-chain biosensor for Cdc42 based on FRET, useful for live-cell imaging. PloS One. 2014;9(5):e96469.
   PubMed Web of Science ®Google Scholar
• Kim J, Lee S, Jung K, et al. Intensiometric biosensors visualize the activity of multiple small GTPases in vivo. Nat Commun. 2019;10(1):211.
   PubMedGoogle Scholar
• Fritz RD, Menshykau D, Martin K, et al. SrGAP2-Dependent integration of membrane geometry and Slit-Robo-Repulsive cues regulates fibroblast contact inhibition of Locomotion. Dev Cell. 2015;35(1):78–92.
   PubMed Web of Science ®Google Scholar
• Marston DJ, Anderson KL, Swift MF, et al. High Rac1 activity is functionally translated into cytosolic structures with unique nanoscale cytoskeletal architecture. Proc Natl Acad Sci U.S.A. 2019;116:1267–1272.
   Google Scholar
• Moshfegh Y, Bravo-Cordero JJ, Miskolci V, et al. A Trio–Rac1–Pak1 signalling axis drives invadopodia disassembly. Nat Cell Biol. 2014;16(6):571–583.
   Web of Science ®Google Scholar
• Miskolci V, Wu B, Moshfegh Y, et al. Optical tools to study the isoform-specific roles of small GTPases in immune cells. Journal of Immunology (Baltimore, Md.: 1950). 2016;196(8):3479–3493.
   PubMed Web of Science ®Google Scholar
• Donnelly SK, Cabrera R, Mao SPH, et al. Rac3 regulates breast cancer invasion and metastasis by controlling adhesion and matrix degradation. J Cell Biol. 2017;216(12):4331–4349.
   PubMed Web of Science ®Google Scholar