SILAC-based proteomic quantification of chemoattractant-induced cytoskeleton dynamics on a second to minute timescale

Nature Communications

Volumn 5, Issue , 2014, Pages

  Sobczyk, Grzegorz J ^a   Wang, Jun ^a,b   Weijer, Cornelis J ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b Berry Genomics ^*  (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHEMOATTRACTANT; CYCLIC AMP; CYTOSKELETON PROTEIN; AMINO ACID; CHEMOTACTIC FACTOR; GREEN FLUORESCENT PROTEIN; PROTEOME; PROTOZOAL PROTEIN;

GERM CELL; MICROSCOPY; PROTEOMICS; SIGNALING; TIMESCALE;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL FRACTIONATION; CELL FUNCTION; CELL POPULATION; COMPARATIVE STUDY; CONFOCAL LASER MICROSCOPY; CYTOSKELETON; DICTYOSTELIUM; IN VIVO STUDY; INTRACELLULAR SPACE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENE INACTIVATION; GENETICS; ISOTOPE LABELING; KINETICS; MASS SPECTROMETRY; METABOLISM; MUTATION; PROCEDURES; PROTEIN TRANSPORT; TIME;

AMINO ACIDS; CHEMOTACTIC FACTORS; CYCLIC AMP; CYTOSKELETAL PROTEINS; CYTOSKELETON; DICTYOSTELIUM; GENE KNOCKOUT TECHNIQUES; GREEN FLUORESCENT PROTEINS; ISOTOPE LABELING; KINETICS; MASS SPECTROMETRY; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MUTATION; PROTEIN TRANSPORT; PROTEOME; PROTEOMICS; PROTOZOAN PROTEINS; TIME FACTORS;

EID: 84904723748     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4319     Document Type: Article

References (61)

1. Allen, S. J., Crown, S. E. & Handel, T. M. Chemokine: receptor structure, interactions, and antagonism. Annu. Rev. Immunol. 25, 787-820 (2007).
2. Condeelis, J., Singer, R. H. & Segall, J. E. The great escape: when cancer cells hijack the genes for chemotaxis and motility. Annu. Rev. Cell Dev. Biol. 21, 695-718 (2005).
3. Bagorda, A. & Parent, C. A. Eukaryotic chemotaxis at a glance. J. Cell Sci. 121, 2621-2624 (2008).
4. Affolter, M. & Weijer, C. J. Signaling to cytoskeletal dynamics during chemotaxis. Dev. Cell 9, 19-34 (2005).
5. Rericha, E. C. & Parent, C. A. Steering in quadruplet: the complex signaling pathways directing chemotaxis. Sci. Signal. 1, pe26 (2008).
6. Swaney, K. F., Huang, C. H. & Devreotes, P. N. Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu. Rev. Biophys. 39, 265-289 (2010).
7. Veltman, D. M., Keizer-Gunnik, I. & Van Haastert, P. J. Four key signaling pathways mediating chemotaxis in Dictyostelium discoideum. J. Cell Biol. 180, 747-753 (2008).
8. Xu, X. et al. Coupling mechanism of a GPCR and a heterotrimeric G protein during chemoattractant gradient sensing in Dictyostelium. Sci. Signal. 3, ra71 (2010).
9. Manahan, C. L., Iglesias, P. A., Long, Y. & Devreotes, P. N. Chemoattractant signaling in Dictyostelium discoideum. Annu. Rev. Cell Dev. Biol. 20, 223-253 (2004).
10. Kortholt, A. & van Haastert, P. J. Highlighting the role of Ras and Rap during Dictyostelium chemotaxis. Cell Signal. 20, 1415-1422 (2008).
11. Sasaki, A. T. & Firtel, R. A. Regulation of chemotaxis by the orchestrated activation of Ras, PI3K, and TOR. Eur. J. Cell Biol. 85, 873-895 (2006).
12. Cai, H. et al. Ras-mediated activation of the TORC2-PKB pathway is critical for chemotaxis. J. Cell. Biol. 190, 233-245 (2010).
13. Hanna, S. & El-Sibai, M. Signaling networks of Rho GTPases in cell motility. Cell Signal. 25, 1955-1961 (2013).
14. Vlahou, G. & Rivero, F. Rho GTPase signaling in Dictyostelium discoideum: insights from the genome. Eur. J. Cell Biol. 85, 947-959 (2006).
15. Bourne, H. R., Sanders, D. A. & McCormick, F. The GTPase superfamily: conserved structure and molecular mechanism. Nature 349, 117-127 (1991).
16. Boguski, M. S. & McCormick, F. Proteins regulating Ras and its relatives. Nature 366, 643-654 (1993).
17. Chen, L. et al. Two phases of actin polymerization display different dependencies on PI(3,4,5)P3 accumulation and have unique roles during chemotaxis. Mol. Biol. Cell 14, 5028-5037 (2003).
18. Orelio, C. & Kuijpers, T. W. Shwachman-Diamond syndrome neutrophils have altered chemoattractant-induced F-actin polymerization and polarization characteristics. Haematologica 94, 409-413 (2009).
19. Weiner, O. D. et al. Spatial control of actin polymerization during neutrophil chemotaxis. Nat. Cell Biol. 1, 75-81 (1999).
20. Levi, S., Polyakov, M. V. & Egelhoff, T. T. Myosin II dynamics in Dictyostelium: determinants for filament assembly and translocation to the cell cortex during chemoattractant responses. Cell Motil. Cytoskeleton 53, 177-188 (2002).
21. Bosgraaf, L. & van Haastert, P. J. The regulation of myosin II in Dictyostelium. Eur. J. Cell Biol. 85, 969-979 (2006).
22. Eddy, R. J., Han, J. & Condeelis, J. S. Capping protein terminates but does not initiate chemoattractant-induced actin assembly in Dictyostelium. J. Cell. Biol. 139, 1243-1253 (1997).
23. Ong, S. E. & Mann, M. A practical recipe for stable isotope labelling by amino acids in cell culture (SILAC). Nat. Protoc. 1, 2650-2660 (2006).
24. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V. & Mann, M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860 (2006).
25. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008).
26. Insall, R. et al. Dynamics of the Dictyostelium Arp2/3 complex in endocytosis, cytokinesis, and chemotaxis. Cell Motil. Cytoskeleton 50, 115-128 (2001).
27. Patel, M., Pelletier, A. & Cote, J. F. Opening up on ELMO regulation: New insights into the control of Rac signaling by the DOCK180/ELMO complex. Small GTPases 2, 268-275 (2011).
28. Yan, J. et al. A Gbetagamma effector, ElmoE, transduces GPCR signaling to the actin network during chemotaxis. Dev. Cell 22, 92-103 (2012).
29. Cote, J. F. & Vuori, K. Identification of an evolutionarily conserved superfamily of DOCK180-related proteins with guanine nucleotide exchange activity. J. Cell Sci. 115, 4901-4913 (2002).
30. Meller, N., Merlot, S. & Guda, C. CZH proteins: a new family of Rho-GEFs. J. Cell Sci. 118, 4937-4946 (2005).
31. Wu, Y. C. & Horvitz, H. R. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 392, 501-504 (1998).
32. Para, A. et al. Dictyostelium Dock180-related RacGEFs regulate the actin cytoskeleton during cell motility. Mol. Biol. Cell 20, 699-707 (2009).
33. Friedberg, F. & Rivero, F. Single and multiple CH (calponin homology) domain containing multidomain proteins in Dictyostelium discoideum: an inventory. Mol. Biol. Rep. 37, 2853-2862 (2009).
34. Insall, R. H., Borleis, J. & Devreotes, P. N. The aimless RasGEF is required for processing of chemotactic signals through G-protein-coupled receptors in Dictyostelium. Curr. Biol. 6, 719-729 (1996).
35. Kae, H. et al. Cyclic AMP signalling in Dictyostelium: G-proteins activate separate Ras pathways using specific RasGEFs. EMBO Rep. 8, 477-482 (2007).
36. van Egmond, W. N. & van Haastert, P. J. Characterization of the Roco protein family in Dictyostelium discoideum. Eukaryot. Cell 9, 751-761 (2010).
37. Marin, I., van Egmond, W. N. & van Haastert, P. J. The Roco protein family: a functional perspective. FASEB J. 22, 3103-3110 (2008).
38. Bosgraaf, L. et al. RasGEF-containing proteins GbpC and GbpD have differential effects on cell polarity and chemotaxis in Dictyostelium. J. Cell Sci. 118, 1899-1910 (2005).
39. Riedl, J. et al. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605-607 (2008).
40. Yang, Y. et al. PakB binds to the SH3 domain of Dictyostelium Abp1 and regulates its effects on cell polarity and early development. Mol. Biol. Cell 24, 2216-2227 (2013).
41. de la Roche, M., Mahasneh, A., Lee, S. F., Rivero, F. & Cote, G. P. Cellular distribution and functions of wild-type and constitutively activated Dictyostelium PakB. Mol. Biol. Cell 16, 238-247 (2005).
42. Jeon, T. J., Lee, D. J., Lee, S., Weeks, G. & Firtel, R. A. Regulation of Rap1 activity by RapGAP1 controls cell adhesion at the front of chemotaxing cells. J. Cell. Biol. 179, 833-843 (2007).
43. Lee, M. R. & Jeon, T. J. Cell migration: regulation of cytoskeleton by Rap1 in Dictyostelium discoideum. J. Microbiol. 50, 555-561 (2012).
44. Cote, J. F. & Vuori, K. In vitro guanine nucleotide exchange activity of DHR-2/DOCKER/CZH2 domains. Methods Enzymol. 406, 41-57 (2006).
45. Blagg, S. L. & Insall, R. H. Control of SCAR activity in Dictyostelium discoideum. Biochem. Soc. Trans. 32, 1113-1114 (2004).
46. Ibarra, N., Pollitt, A. & Insall, R. H. Regulation of actin assembly by SCAR/WAVE proteins. Biochem. Soc. Trans. 33, 1243-1246 (2005).
47. Vazquez, F. & Devreotes, P. Regulation of PTEN function as a PIP3 gatekeeper through membrane interaction. Cell Cycle 5, 1523-1527 (2006).
48. Kortholt, A., King, J. S., Keizer-Gunnink, I., Harwood, A. J. & Van Haastert, P. J. Phospholipase C regulation of phosphatidylinositol 3,4,5-trisphosphatemediated chemotaxis. Mol. Biol. Cell 18, 4772-4779 (2007).
49. Han, J. W., Leeper, L., Rivero, F. & Chung, C. Y. Role of RacC for the regulation of WASP and phosphatidylinositol 3-kinase during chemotaxis of Dictyostelium. J. Biol. Chem. 281, 35224-35234 (2006).
50. Chen, C. L., Wang, Y., Sesaki, H. & Iijima, M. Myosin I links PIP3 signaling to remodeling of the actin cytoskeleton in chemotaxis. Sci. Signal. 5, ra10 (2012).
51. Veltman, D. M. & Insall, R. H. WASP family proteins: their evolution and its physiological implications. Mol. Biol. Cell 21, 2880-2893 (2010).
52. Vartiainen, M. K. & Machesky, L. M. The WASP-Arp2/3 pathway: genetic insights. Curr. Opin. Cell Biol. 16, 174-181 (2004).
53. Brenner, M. & Thoms, S. D. Caffeine blocks activation of cyclic AMP synthesis in Dictyostelium discoideum. Dev. Biol. 101, 136-146 (1984).
54. de Hoon, M. J., Imoto, S., Nolan, J. & Miyano, S. Open source clustering software. Bioinformatics 20, 1453-1454 (2004).
55. Saldanha, A. J. Java Treeview-extensible visualization of microarray data. Bioinformatics 20, 3246-3248 (2004).
56. Kim, J. Y. et al. Random mutagenesis of the cAMP chemoattractant receptor, cAR1, of Dictyostelium. Mutant classes that cause discrete shifts in agonist affinity and lock the receptor in a novel activational intermediate. J. Biol. Chem. 272, 2060-2068 (1997).
57. Veltman, D. M., Akar, G., Bosgraaf, L. & Van Haastert, P. J. A new set of small, extrachromosomal expression vectors for Dictyostelium discoideum. Plasmid 61, 110-118 (2009).
58. Faix, J., Kreppel, L., Shaulsky, G., Schleicher, M. & Kimmel, A. R. A rapid and efficient method to generate multiple gene disruptions in Dictyostelium discoideum using a single selectable marker and the Cre-loxP system. Nucleic Acids Res. 32, e143 (2004).
59. de Hostos, E. L. et al. Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. J. Cell. Biol. 120, 163-173 (1993).
60. Bosgraaf, L., van Haastert, P. J. & Bretschneider, T. Analysis of cell movement by simultaneous quantification of local membrane displacement and fluorescent intensities using Quimp2. Cell Motil. Cytoskeleton 66, 156-165 (2009).
61. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).