In Candida albicans, phosphorylation of Exo84 by Cdk1-Hgc1 is necessary for efficient hyphal extension

Molecular Biology of the Cell

Volumn 25, Issue 7, 2014, Pages 1097-1110

  Caballero Lima, David ^a   Sudbery, Peter E ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 1; CYCLIN HGC1; CYCLINE; EXOCYST; PHOSPHATIDYLSERINE; UNCLASSIFIED DRUG; FUNGAL PROTEIN; HYBRID PROTEIN;

ARTICLE; BINDING AFFINITY; BUDDING; CANDIDA ALBICANS; CELL MEMBRANE; CONTROLLED STUDY; FUNGUS HYPHAE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; ALLELE; AMINO ACID SEQUENCE; CELL POLARITY; CHEMISTRY; CYTOKINESIS; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; PHENOTYPE; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ALLELES; AMINO ACID SEQUENCE; CANDIDA ALBICANS; CDC2 PROTEIN KINASE; CELL POLARITY; CYTOKINESIS; FUNGAL PROTEINS; HUMANS; HYPHAE; MITOSIS; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PHOSPHATIDYLSERINES; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

EID: 84898711985     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-11-0688     Document Type: Article

References (47)

1. Adamo JE, Rossi G, Brennwald P (1999). The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Mol Biol Cell 10, 4121-4133
2. Bensen ES, Clemente-Blanco A, Finley KR, Correa-Bordes J, Berman J (2005). The mitotic cyclins Clb2p and Clb4p affect morphogenesis in Candida albicans. Mol Biol Cell 16, 3387-3400 (Pubitemid 40962607)
3. Bishop A, Lane R, Beniston R, Lazo B, Smythe C, Sudbery P (2010). Hyphal growth in Candida albicans requires the phosphorylation of Sec2 by the Cdc28-Ccn1/Hgc1 kinase. EMBO J 29, 2930-2942
4. Boyd C, Hughes T, Pypaert M, Novick P (2004). Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J Cell Biol 167, 889-901 (Pubitemid 39628111)
5. Brennwald P, Rossi G (2007). Spatial regulation of exocytosis and cell polarity: yeast as a model for animal cells. FEBS Lett 581, 2119-2124 (Pubitemid 46709909)
6. Caballero-Lima D, Kaneva IN, Watton SP, Sudbery PE, Craven CJ (2013). The spatial distribution of the exocyst and actin cortical patches is sufficient to organize hyphal tip growth. Eukaryot Cell 12, 998-1008
7. Chapa-Y-Lazo B, Lee S, Regan H, Sudbery P (2011). The mating projections of Saccharomyces cerevisiae and Candida albicans show key characteristics of hyphal growth. Fungal Biol 115, 547-556
8. Chen YL, Montedonico AE, Kauffman S, Dunlap JR, Menn FM, Reynolds TB (2010). Phosphatidylserine synthase and phosphatidylserine decarboxylase are essential for cell wall integrity and virulence in Candida albicans. Mol Microbiol 75, 1112-1132
9. Court H, Sudbery P (2007). Regulation of Cdc42 GTPase activity in the formation of hyphae in Candida albicans. Mol Biol Cell 18, 265-281 (Pubitemid 46066726)
10. Crampin H, Finley K, Gerami-Nejad M, Court H, Gale C, Berman J, Sudbery PE (2005). Candida albicans hyphae have a Spitzenkorper that is distinct from the polarisome found in yeast and pseudohyphae. J Cell Sci 118, 2935-2947 (Pubitemid 41136370)
11. Finger FP, Hughes TE, Novick P (1998). Sec3p is a spatial landmark for polarized secretion in budding yeast. Cell 92, 559-571 (Pubitemid 28101118)
12. Gola S, Martin R, Walther A, Dunkler A, Wendland J (2003). New modules for PCR-based gene targeting in Candida albicans: rapid and efficient gene targeting using 100 bp of flanking homology region. Yeast 20, 1339-1347 (Pubitemid 38016628)
13. Goranov AI, Amon A (2010). Growth and division not a one-way road. Curr Opin Cell Biol 22, 795-800
14. Guo W, Tamanoi F, Novick P (2001). Spatial regulation of the exocyst complex by Rho1 GTPase. Nat Cell Biol 3, 353-360 (Pubitemid 32288442)
15. He B, Guo W (2009). The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 21, 537-542
16. He B, Xi F, Zhang X, Zhang J, Guo W (2007a). Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane. EMBO J 26, 4053-4065 (Pubitemid 47462093)
17. He B, Xi FG, Zhang J, TerBush D, Zhang XY, Guo W (2007b). Exo70p mediates the secretion of specific exocytic vesicles at early stages of the cell cycle for polarized cell growth. J Cell Biol 176, 771-777 (Pubitemid 46425537)
18. Heider MR, Munson M (2012). Exorcising the exocyst complex. Traffic 13, 898-907
19. Jones LA, Sudbery PE (2010). Spitzenkorper, exocyst and polarisome components in Candida albicans hyphae show different patterns of localization and have distinct dynamic properties. Eukaryot Cell 9, 1455-1465
20. Kelley LA, Sternberg MJ (2009). Protein structure prediction on the Web: A case study using the Phyre server. Nat Protocols 4, 363-371
21. Klis FM, Boorsma A, De Groot PWJ (2006). Cell wall construction in Saccharomyces cerevisiae. Yeast 23, 185-202
22. Lavoie H, Sellam A, Askew C, Nantel A, Whiteway M (2008). A toolbox for epitope-tagging and genome-wide location analysis in Candida albicans. BMC Genomics 9, 578-591
23. Lee KL, Buckley HR, Cambell CC (1975). An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans. Sabouraudia 13, 148-153
24. Li CR, Lee RT-H, Wang YM, Zheng XD, Wang Y (2007). Candida albicans hyphal morphogenesis occurs in Sec3p-independent and Sec3p-dependent phases separated by septin ring formation. J Cell Sci 120, 1898-1907 (Pubitemid 46979781)
25. Luo G, Zhang J, Luca FC, Guo W (2013). Mitotic phosphorylation of Exo84 disrupts exocyst assembly and arrests cell growth. J Cell Biol 202, 97-111
26. McCusker D, Denison C, Anderson S, Egelhofer TA, Yates JR, Gygi SP, Kellogg DR (2007). Cdk1 coordinates cell-surface growth with the cell cycle. Nat Cell Biol 9, 506-U45
27. Punta M et al. (2012). The Pfam protein families database. Nucleic Acids Res 40, D290-D301
28. Roumanie O, Wu H, Molk JN, Rossi G, Bloom K, Brennwald P (2005). Rho GTPase regulation of exocytosis in yeast is independent of GTP hydrolysis and polarization of the exocyst complex. J Cell Biol 170, 583-594 (Pubitemid 41186933)
29. Sandquist JC, Kita AM, Bement WM (2011). The dead shall rise: Actin and myosin return to the spindle. Dev Cell 21, 410-419
30. Schaub Y, Dunkler A, Walther A, Wendland J (2006). New pFA-cassettes for PCR-based gene manipulation in Candida albicans. J Basic Microbiol 46, 416-429 (Pubitemid 44582323)
31. Sinha I, Wang YM, Philp R, Li CR, Yap WH, Wang Y (2007). Cyclin-dependent kinases control septin phosphorylation in Candida albicans hyphal development. Dev Cell 13, 421-432 (Pubitemid 47308673)
32. Siniossoglou S, Pelham HRB (2002). Vps51p links the VFT complex to the SNARE Tlg1p. J Biol Chem 277, 48318-48324 (Pubitemid 35470786)
33. Soll DR, Herman MA, Staebell MA (1985). The involvement of cell wall expansion in the two modes of mycelium formation of Candida albicans. J Gen Microbiol 131, 2367-2375 (Pubitemid 16215875)
34. Sudbery PE (2001). The germ tubes of Candida albicans hyphae and pseudohyphae show different patterns of septin ring localisation. Mol Microbiol 41, 19-31 (Pubitemid 32660980)
35. Sudbery PE (2011). Growth of Candida albicans hyphae. Nat Rev Microbiol 9, 737-748
36. Sudbery PE, Gow NAR, Berman J (2004). The distinct morphogenic states of Candida albicans. Trends Microbiol 12, 317-324 (Pubitemid 38829652)
37. Terbush DR, Maurice T, Roth D, Novick P (1996). The exocyst is a multi-protein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 15, 6483-6494 (Pubitemid 26413781)
38. Terbush DR, Novick P (1995). Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae. J Cell Biol 130, 299-312
39. Walther A, Wendland J (2008). Hyphal growth and virulence in Candida albicans. In: Human and Animal Relationships, ed. AA Brakhage and PF Zipfel, Berlin: Springer-Verlag, 95-114
40. Wang A, Raniga PP, Lane S, Lu Y, Liu HP (2009). Hyphal chain formation in Candida albicans: Cdc28-Hgc1 phosphorylation of Efg1 represses cell separation genes. Mol Cell Biol 29, 4406-4416
41. Wightman R, Bates S, Amnorrattapan P, Sudbery PE (2004). In Candida albicans, the Nim1 kinases Gin4 and Hsl1 negatively regulate pseudohypha formation and Gin4 also controls septin organization. J Cell Biol 164, 581-591 (Pubitemid 38233319)
42. Wilson B, Davis D, Mitchell AP (1999). Rapid hypothesis testing in Candida albicans through gene disruption with short homology regions. J Bacteriol 181, 1868-1874 (Pubitemid 29138620)
43. Wu H, Turner C, Gardner J, Temple B, Brennwald P (2010). The Exo70 subunit of the exocyst is an effector for both Cdc42 and Rho3 function in polarized exocytosis. Mol Biol Cell 21, 430-442
44. Zhang XY, Bi EF, Novick P, Du LL, Kozminski KG, Lipschutz JH, Guo W (2001). Cdc42 interacts with the exocyst and regulates polarized secretion. J Biol Chem 276, 46745-46750
45. Zhang X, Orlando K, He B, Xi F, Zhang J, Zajac A, Guo W (2008). Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J Cell Biol 180, 145-158
46. Zheng XD, Lee RTH, Wang YM, Lin QS, Wang Y (2007). Phosphorylation of Rga2, a Cdc42 GAP, by CDK/Hgc1 is crucial for Candida albicans hyphal growth. EMBO J 26, 3760-3769 (Pubitemid 47295881)
47. Zheng X, Wang Y, Wang Y (2004). Hgc1, a novel hypha-specific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis. EMBO J 23, 1845-1856 (Pubitemid 38649647)