GDI-Mediated Cell Polarization in Yeast Provides Precise Spatial and Temporal Control of Cdc42 Signaling

PLoS Computational Biology

Volumn 9, Issue 12, 2013, Pages

  Klünder, Ben ^a   Freisinger, Tina ^b   Wedlich Söldner, Roland ^b,c   Frey, Erwin ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SIGNALING; CELLS; CYTOLOGY; FEEDBACK; YEAST;

CELL DIFFERENTIATION; CELL MIGRATION; CELL POLARIZATION; CYTOSKELETAL STRUCTURES; GTPASES; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; POLARIS; SPATIAL CONTROL; TEMPORAL CONTROLS; YEAST SACCHAROMYCES CEREVISIAE;

POLARIZATION;

GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; PROTEIN CDC42;

ARTICLE; CELL CYCLE REGULATION; CELL POLARITY; CLUSTER ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; ENZYME SYNTHESIS; INTRACELLULAR SIGNALING; MATHEMATICAL MODEL; MOLECULAR STABILITY; NONHUMAN; POSITIVE FEEDBACK; PREDICTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SACCHAROMYCES CEREVISIAE; SPATIOTEMPORAL ANALYSIS; VALIDATION PROCESS;

CDC42 GTP-BINDING PROTEIN, SACCHAROMYCES CEREVISIAE; CELL POLARITY; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

EID: 84892727960     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003396     Document Type: Article

References (51)

1. Wodarz A, Näthke I, (2007) Cell polarity in development and cancer. Nat Cell Biol 9: 1016-1024.
2. Florian MC, Geiger H, (2010) Concise review: polarity in stem cells, disease, and aging. Stem Cells 28: 1623-1629.
3. Stengel K, Zheng Y, (2011) Cdc42 in oncogenic transformation, invasion, and tumorigenesis. Cell Signal 23: 1415-1423.
4. Irazoqui JE, Gladfelter AS, Lew DJ, (2003) Scaffold-mediated symmetry breaking by Cdc42p. Nat Cell Biol 5: 1062-1070.
5. Wedlich-Soldner R, Wai SC, Schmidt T, Li R, (2004) Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling. J Cell Biol 166: 889-900.
6. Wedlich-Soldner R, Altschuler S, Wu L, Li R, (2003) Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science 299: 1231-1235.
7. Yu JH, Crevenna AH, Bettenbühl M, Freisinger T, Wedlich-Söldner R, (2011) Cortical actin dynamics driven by formins and myosin V. J Cell Sci 124: 1533-1541.
8. Slaughter B, Das A, Schwartz J, Rubinstein B, Li R, (2009) Dual modes of Cdc42 recycling fine-tune polarized morphogenesis. Dev Cell 17: 823-835.
9. Bose I, Irazoqui JE, Moskow JJ, Bardes ES, Zyla TR, et al. (2001) Assembly of scaffold-mediated complexes containing Cdc42p, the exchange factor Cdc24p, and the effector Cla4p required for cell cycle-regulated phosphorylation of Cdc24p. J Biol Chem 276: 7176-7186.
10. Butty A-C, Perrinjaquet N, Petit A, Jaquenoud M, Segall JE, et al. (2002) A positive feedback loop stabilizes the guanine-nucleotide exchange factor Cdc24 at sites of polarization. EMBO J 21: 1565-1576.
11. Kozubowski L, Saito K, Johnson JM, Howell AS, Zyla TR, et al. (2008) Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr Biol 18: 1719-2176.
12. Altschuler SJ, Angenent SB, Wang Y, Wu LF, (2008) On the spontaneous emergence of cell polarity. Nature 454: 886-889.
13. Howell AS, Jin M, Wu C-F, Zyla TR, Elston TC, et al. (2012) Negative feedback enhances robustness in the yeast polarity establishment circuit. Cell 149: 322-333.
14. Freisinger T, Klünder B, Johnson J, Müller N, Pichler G, et al. (2013) Establishment of a robust single axis of cell polarity by coupling multiple positive feedback loops. Nat Commun 4: 1807.
15. Goryachev AB, Pokhilko AV, (2008) Dynamics of Cdc42 network embodies a Turing-type mechanism of yeast cell polarity. FEBS Lett 582: 1437-1443.
16. Howell AS, Savage NS, Johnson SA, Bose I, Wagner AW, et al. (2009) Singularity in polarization: rewiring yeast cells to make two buds. Cell 139: 731-743.
17. Savage NS, Layton AT, Lew DJ, (2012) Mechanistic mathematical model of polarity in yeast. Mol Biol Cell 23: 1998-2013.
18. Jose M, Tollis S, Nair D, Sibarita J-B, McCusker D, (2013) Robust polarity establishment occurs via an endocytosis-based cortical corralling mechanism. J Cell Biol 200: 407-418.
19. Marco E, Wedlich-Soldner R, Li R, Altschuler SJ, Wu LF, (2007) Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity. Cell 129: 411-422.
20. Slaughter BD, Schwartz JW, Li R, (2007) Mapping dynamic protein interactions in MAP kinase signaling using live-cell fluorescence fluctuation spectroscopy and imaging. Proc Natl Acad Sci USA 104: 20320-20325.
21. Ugolev Y, Berdichevsky Y, Weinbaum C, Pick E, (2008) Dissociation of Rac1(GDP).RhoGDI complexes by the cooperative action of anionic liposomes containing phosphatidylinositol 3,4,5-trisphosphate, Rac guanine nucleotide exchange factor, and GTP. J Biol Chem 283: 22257-22271.
22. Ghaemmaghami S, Huh W-K, Bower K, Howson RW, Belle A, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737-741.
23. Michaelson D, Silletti J, Murphy G, D'Eustachio P, Mark 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.
24. Koch G, Tanaka K, Masuda T, Yamochi W, Nonaka H, et al. (1997) Association of the Rho family small GTP-binding proteins with Rho GDP dissociation inhibitor (Rho GDI) in Saccharomyces cerevisiae. Oncogene 15: 417-422.
25. Johnson JL, Erickson JW, Cerione RA, (2009) New insights into how the Rho guanine nucleotide dissociation inhibitor regulates the interaction of Cdc42 with membranes. J Biol Chem 284: 23860-23871.
26. Li R, Wedlich-Soldner R, (2009) Bem1 complexes and the complexity of yeast cell polarization. Curr Biol 19: R194-R195.
27. Wai SC, Gerber SA, Li R, (2009) Multisite phosphorylation of the guanine nucleotide exchange factor Cdc24 during yeast cell polarization. PLoS ONE 4: e6563.
28. Gulli MP, Jaquenoud M, Shimada Y, Niederhäuser G, Wiget P, et al. (2000) Phosphorylation of the Cdc42 exchange factor Cdc24 by the PAK-like kinase Cla4 may regulate polarized growth in yeast. Mol Cell 6: 1155-1167.
29. Wild AC, Yu JW, Lemmon MA, Blumer KJ, (2004) The p21-activated protein kinase-related kinase Cla4 is a coincidence detector of signaling by Cdc42 and phosphatidylinositol 4-phosphate. J Biol Chem 279: 17101-17110.
30. Shimada Y, Wiget P, Gulli M-P, Bi E, Peter M, (2004) The nucleotide exchange factor Cdc24p may be regulated by auto-inhibition. EMBO J 23: 1051-1062.
31. Toenjes KA, Simpson D, Johnson DI, (2004) Separate membrane targeting and anchoring domains function in the localization of the S. cerevisiae Cdc24p guanine nucleotide exchange factor. Curr Genet 45: 257-264.
32. Zheng Y, Cerione R, Bender A, (1994) Control of the yeast bud-site assembly GTPase Cdc42. catalysis of guanine nucleotide exchange by Cdc24 and stimulation of GTPase activity by Bem3. J Biol Chem 269: 2369-2372.
33. Stevenson BJ, Ferguson B, De Virgilio C, Bi E, Pringle JR, et al. (1995) Mutation of RGA1, which encodes a putative GTPase-activating protein for the polarity-establishment protein Cdc42p, activates the pheromone-response pathway in the yeast Saccharomyces cerevisiae. Genes Dev 9: 2949-2963.
34. Marquitz AR, Harrison JC, Bose I, Zyla TR, McMillan JN, et al. (2002) The Rho-GAP Bem2p plays a GAP-independent role in the morphogenesis checkpoint. EMBO J 21: 4012-4025.
35. Smith GR, Givan SA, Cullen P, Sprague GF, (2002) GTPase-activating proteins for Cdc42. Eukaryot Cell 1: 469-480.
36. Wu Y-W, Oesterlin LK, Tan K-T, Waldmann H, Alexandrov K, et al. (2010) Membrane targeting mechanism of RAB GTPases elucidated by semisynthetic protein probes. Nat Chem Biol 6: 534-540.
37. Stowers L, Yelon D, Berg LJ, Chant J, (1995) Regulation of the polarization of T cells toward antigen-presenting cells by Ras-related GTPase CDC42. Proc Natl Acad Sci USA 92: 5027-5031.
38. Jung V, Wei W, Ballester R, Camonis J, Mi S, et al. (1994) Two types of RAS mutants that dominantly interfere with activators of RAS. Mol Cell Biol 14: 3707-3018.
39. Mori Y, Jilkine A, Edelstein-Keshet L, (2008) Wave-pinning and Cell Polarity from a Bistable Reaction-Diffusion System. Biophys J 94: 3684-3697.
40. Otsuji M, Ishihara S, Co C, Kaibuchi K, Mochizuki A, et al. (2007) A Mass Conserved Reaction-Diffusion System Captures Properties of Cell Polarity. PLoS Comput Biol 3: e108.
41. Levine H, Rappel W-J, (2005) Membrane-bound Turing patterns. Phys rev E 72: 061912.
42. Frey E, Kroy K, (2005) Brownian motion: a paradigm of soft matter and biological physics. Ann Phys (Leipzig) 14: 20-50.
43. Orlando K, Sun X, Zhang J, Lu T, Yokomizo L, et al. (2011) Exo-endocytic trafficking and the septin-based diffusion barrier are required for the maintenance of Cdc42p polarization during budding yeast asymmetric growth. Mol Biol Cell 22: 624-633.
44. Nern A, Arkowitz RA, (2000) Nucleocytoplasmic shuttling of the Cdc42p exchange factor Cdc24p. J Cell Biol 148: 1115-1122.
45. Knaus M, Pelli-Gulli M-P, van Drogen F, Springer S, Jaquenoud M, et al. (2007) Phosphorylation of Bem2p and Bem3p may contribute to local activation of Cdc42p at bud emergence. EMBO J 26: 4501-4513.
46. Shimada Y, Gulli MP, Peter M, (2000) Nuclear sequestration of the exchange factor Cdc24 by Far1 regulates cell polarity during yeast mating. Nat Cell Biol 2: 117-124.
47. Caviston JP, Tcheperegine SE, Bi E, (2002) Singularity in budding: a role for the evolutionarily conserved small GTPase Cdc42p. Proc Nat Acad Sci USA 99: 12185-12190.
48. Halatek J, Frey E, (2012) Highly Canalized MinD Transfer and MinE Sequestration Explain the Origin of Robust MinCDE-Protein Dynamics. Cell Rep 1: 741-752.
49. Hwang J-U, Vernoud V, Szumlanski A, Nielsen E, Yang Z, (2008) A tip-localized RHOGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr Biol 18: 1907-1916.
50. Sherman F, Fink GR, Hicks JB (1981) Methods in Yeast Genetics: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
51. Tokunaga M, Imamoto N, Sakata-Sogawa K, (2008) Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Meth 5: 159-161.