A new genetically encoded single-chain biosensor for Cdc42 based on FRET, useful for live-cell imaging

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Hanna, Samer ^a   Miskolci, Veronika ^a   Cox, Dianne ^a   Hodgson, Louis ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; FRACTALKINE; PROTEIN CDC42;

ANIMAL CELL; ARTICLE; BIOSENSOR; CELL ORGANELLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FIBROBLAST; FLUORESCENCE RESONANCE ENERGY TRANSFER; MACROPHAGE; MOLECULAR IMAGING; MOUSE; NONHUMAN; PHAGOCYTOSIS; PODOSOME; 3T3 CELL LINE; ANIMAL; CELL CULTURE; FLUOROMETRY; GENETIC PROCEDURES; VALIDATION STUDY;

ANIMALS; BIOSENSING TECHNIQUES; CDC42 GTP-BINDING PROTEIN; CELLS, CULTURED; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUOROMETRY; MICE; NIH 3T3 CELLS;

EID: 84900425523     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096469     Document Type: Article

References (40)

1. Johnson DI (1999) Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol Mol Biol Rev 63: 54-105.
2. Tang Y, Olufemi L, Wang MT, Nie D (2008) Role of Rho GTPases in breast cancer. Front Biosci 13: 759-776. (Pubitemid 351599780)
3. Cerione RA (2004) Cdc42: new roads to travel. Trends Cell Biol 14: 127-132.
4. Stengel K, Zheng Y (2011) Cdc42 in oncogenic transformation, invasion, and tumorigenesis. Cell Signal 23: 1415-1423.
5. Wennerberg K, Der CJ (2004) Rho-family GTPases: it's not only Rac and Rho (and I like it). J Cell Sci 117: 1301-1312. (Pubitemid 38559808)
6. Nalbant P, Hodgson L, Kraynov V, Toutchkine A, Hahn KM (2004) Activation of endogenous Cdc42 visualized in living cells. Science 305: 1615-1619. (Pubitemid 39296355)
7. Hodgson L, Nalbant P, Shen F, Hahn K (2006) Imaging and photobleach correction of Mero-CBD, sensor of endogenous Cdc42 activation. Methods Enzymol 406: 140-156. (Pubitemid 43207438)
8. Seth A, Otomo T, Yin HL, Rosen MK (2003) Rational design of genetically encoded fluorescence resonance energy transfer-based sensors of cellular Cdc42 signaling. Biochemistry 42: 3997-4008. (Pubitemid 36418292)
9. Itoh RE, Kurokawa K, Ohba Y, Yoshizaki H, Mochizuki N, et al. (2002) 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 22: 6582-6591.
10. Roberts PJ, Mitin N, Keller PJ, Chenette EJ, Madigan JP, et al. (2008) Rho Family GTPase modification and dependence on CAAX motif-signaled posttranslational modification. J Biol Chem 283: 25150-25163.
11. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, et al. (2009) Coordination of Rho GTPase activities during cell protrusion. Nature 461: 99-103.
12. Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci U S A 101: 10554-10559. (Pubitemid 38955780)
13. Hodgson L, Pertz O, Hahn KM (2008) Design and optimization of genetically encoded fluorescent biosensors: GTPase biosensors. Methods Cell Biol 85: 63-81.
14. Pertz O, Hodgson L, Klemke RL, Hahn KM (2006) Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440: 1069-1072.
15. Fritz RD, Letzelter M, Reimann A, Martin K, Fusco L, et al. (2013) A versatile toolkit to produce sensitive FRET biosensors to visualize signaling in time and space. Sci Signal 6: rs12.
16. Michaelson D, Silletti J, Murphy G, D'Eustachio P, Rush M, et al. (2001) Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol 152: 111-126. (Pubitemid 32102441)
17. Garcia-Mata R, Boulter E, Burridge K (2011) The 'invisible hand': regulation of RHO GTPases by RHOGDIs. Nat Rev Mol Cell Biol 12: 493-504.
18. Boulter E, Garcia-Mata R, Guilluy C, Dubash A, Rossi G, et al. (2010) Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat Cell Biol 12: 477-483.
19. Ren XD, Kiosses WB, Schwartz MA (1999) Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO Journal 18: 578-585. (Pubitemid 29057242)
20. Hodgson L, Shen F, Hahn K (2010) Biosensors for characterizing the dynamics of rho family GTPases in living cells. Curr Protoc Cell Biol Chapter 14: Unit 14 11 11-26.
21. Zawistowski J, Sabouri-Ghomi M, Danuser G, Hahn K, Hodgson L (2013) A RhoC biosensor reveals differences in the activation kinetics of RhoA and RhoC in migrating cells. Plos One In Press.
22. Park H, Cox D (2009) Cdc42 regulates Fc gamma receptor-mediated phagocytosis through the activation and phosphorylation of Wiskott-Aldrich syndrome protein (WASP) and neural-WASP. Mol Biol Cell 20: 4500-4508.
23. Dovas A, Gevrey JC, Grossi A, Park H, Abou-Kheir W, et al. (2009) Regulation of podosome dynamics by WASp phosphorylation: implication in matrix degradation and chemotaxis in macrophages. J Cell Sci 122: 3873-3882.
24. Park H, Cox D (2011) Syk regulates multiple signaling pathways leading to CX3CL1 chemotaxis in macrophages. J Biol Chem.
25. Cox D, Chang P, Zhang Q, Reddy PG, Bokoch GM, et al. (1997) Requirements for both Rac1 and Cdc42 in membrane ruffling and phagocytosis in leukocytes. J Exp Med 186: 1487-1494. (Pubitemid 27479808)
26. Liu H, Jiang D (2011) Fractalkine/CX3CR1 and atherosclerosis. Clin Chim Acta 412: 1180-1186.
27. Hoppe AD, Swanson JA (2004) Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis. Mol Biol Cell 15: 3509-3519. (Pubitemid 38989692)
28. Cervero P, Panzer L, Linder S (2013) Podosome reformation in macrophages: assays and analysis. Methods Mol Biol 1046: 97-121.
29. Linder S, Nelson D, Weiss M, Aepfelbacher M (1999) Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc Natl Acad Sci U S A 96: 9648-9653. (Pubitemid 29398786)
30. Cammer M, Gevrey JC, Lorenz M, Dovas A, Condeelis J, et al. (2009) The mechanism of CSF-1-induced Wiskott-Aldrich syndrome protein activation in vivo: a role for phosphatidylinositol 3-kinase and Cdc42. J Biol Chem 284: 23302-23311.
31. Blundell MP, Bouma G, Metelo J, Worth A, Calle Y, et al. (2009) Phosphorylation of WASp is a key regulator of activity and stability in vivo. Proc Natl Acad Sci U S A 106: 15738-15743.
32. Tzima E, Kiosses WB, del Pozo MA, Schwartz MA (2003) Localized cdc42 activation, detected using a novel assay, mediates microtubule organizing center positioning in endothelial cells in response to fluid shear stress. J Biol Chem 278: 31020-31023. (Pubitemid 36994615)
33. Park H, Cox D (2011) Syk regulates multiple signaling pathways leading to CX3CL1 chemotaxis in macrophages. J Biol Chem 286: 14762-14769.
34. Miskolci V, Spiering D, Cox D, Hodgson L (2013) A mix-and-measure assay for determining the activation status of endogenous Cdc42 in cytokine-stimulated macrophage cell lysates. Methods in Molecular Biology In Press.
35. Rizzo MA, Springer GH, Granada B, Piston DW (2004) An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 22: 445-449. (Pubitemid 38451376)
36. Parrini MC, Lei M, Harrison SC, Mayer BJ (2002) Pak1 kinase homodimers are autoinhibited in trans and dissociated upon activation by Cdc42 and Rac1. Molecular Cell 9: 73-83. (Pubitemid 34127772)
37. Spiering D, Hodgson L (2011) Multiplex Imaging of Rho GTPase Activities in Living Cells In: Rivero F, editor. Methods in Molecular Biology. New York: Humana Press, Inc.
38. Spiering D, Bravo-Cordero JJ, Moshfegh Y, Miskolci V, Hodgson L (2013) Quantitative Ratiometric Imaging of FRET-Biosensors in Living Cells. Methods Cell Biol 114: 593-609.
39. Spiering D, Hodgson L (2012) Multiplex Imaging of Rho Family GTPase Activities in Living Cells. Methods in Molecular Biology 827: 215-234.
40. Efron B, Tibshirani R (1993) An Introduction to the bootstrap. New York: Chapman & Hall. 436 p.