Hyphal growth in Candida albicans requires the phosphorylation of Sec2 by the Cdc28-Ccn1/Hgc1 kinase

EMBO Journal

Volumn 29, Issue 17, 2010, Pages 2930-2942

  Bishop, Amy ^a   Lane, Rachel ^a   Beniston, Richard ^a   Chapa Y Lazo, Bernardo ^a   Smythe, Carl ^a   Sudbery, Peter ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

cyclin dependent kinase; polarized exocytosis; polarized growth; Spitzenk rper

Indexed keywords

CYCLIN DEPENDENT KINASE; CYSTEINE RICH PROTEIN 61; FUNGAL PROTEIN; PROTEIN SEC2; SERINE; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ARTICLE; CANDIDA ALBICANS; CELL CYCLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FUNGUS GROWTH; FUNGUS HYPHAE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; CHEMISTRY; FLUORESCENCE MICROSCOPY; GENE DELETION; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROSCOPY; PHOSPHORYLATION; WESTERN BLOTTING;

BLOTTING, WESTERN; CANDIDA ALBICANS; CDC2-CDC28 KINASES; CYSTEINE-RICH PROTEIN 61; FUNGAL PROTEINS; GTP-BINDING PROTEINS; HUMANS; HYPHAE; MICROSCOPY; MICROSCOPY, FLUORESCENCE; MUTAGENESIS; PHOSPHORYLATION; SEQUENCE DELETION;

CANDIDA ALBICANS;

EID: 77956395106     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.158     Document Type: Article

References (48)

1. Bartnicki-Garcia S, Bartnicki DD, Gierz G, Lopezfranco R, Bracker CE (1995) Evidence that Spitzenkorper behavior determines the shape of a fungal hypha - a test of the hyphoid model. Exp Mycol 19: 153-159
2. Bartnicki-Garcia S, Hergert F, Gierz G (1989) Computer-simulation of fungal morphogenesis and the mathematical basis for hyphal (tip) growth. Protoplasma 153: 46-57
3. Beltrao P, Trinidad JC, Fiedler D, Roguev A, Lim WA, Shokat KM, Burlingame AL, Krogan NJ (2009) Evolution of phosphoregulation: comparison of phosphorylation patterns across yeast species. Plos Biol 7; doi:10.1371/journal. pbio.1000134
4. Bishop AC, Ubersax JA, Petsch DT, Matheos DP, Gray NS, Blethrow J, Shimizu E, Tsien JZ, Schultz PG, Rose MD, Wood JL, Morgan DO, Shokat KM (2000) A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407: 395-401
5. Biswas S, Van Dijck P, Datta A (2007) Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol Mol Biol Rev 71: 348-376
6. Bockmuhl DP, Krishnamurthy S, Gerads M, Sonneborn A, Ernst JF (2001) Distinct and redundant roles of the two protein kinase A isoforms Tpk1p and Tpk2p in morphogenesis and growth of Candida albicans. Mol Microbiol 42: 1243-1257
7. Bracker CE, Murphey DJ, Lopez-Franco R (1997) Laser microbeam manipulation of cell morphogenesis in growing hyphae. In Functional Imaging of Optical Manipulation of Living Cells, Farkas, DL, Tromberg BJ (eds) Washington: International Society for Optical Engineering, Bellingham
8. Brown AJP, Argimon S, Gow NAR (2007) Signal transduction and morphogenesis in Candida albicans. In Biology of the Fungal Cell, Howard RJ, Gow NAR (eds) Berlin: Springer. pp 167-194
9. Care RA, Trevethick J, Binley KM, Sudbery PE (1999) The MET3 promoter: a new tool for Candida albicans molecular genetics. Mol Microbiol 34: 792-798
10. Court H, Sudbery P (2007) Regulation of Cdc42 GTPase activity in the formation of hyphae in Candida albicans. Mol Biol Cell 18: 265-281
11. 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
12. Dong G, Medkova M, Novick P, Reinisch KM (2007) A catalytic coiled coil: structural insights into the activation of the Rab GTPase Sec4p by Sec2p. Mol Cell 25: 455-462
13. Elkind NB, Walch-Solimena C, Novick PJ (2000) The role of the COOH terminus of Sec2p in the transport of post-Golgi vesicles. J Cell Biol 149: 95-110
14. Endicott JA, Noble MEM, Tucker JA (1999) Cyclin-dependent kinases: inhibition and substrate recognition. Curr Opin Struct Biol 9: 738-744
15. Gerami-Nejad M, Berman J, Gale C (2001) Cassettes for PCRmediated construction of green, yellow and cyan fluorescent protein fusions in Candida albicans. Yeast 18: 859-880
16. Gerami-Nejad M, Hausauer D, McClellan M, Berman J, Gale C (2004) Cassettes for the PCR-mediated construction of regulatable alleles in Candida albicans. Yeast 21: 429-436
17. Girbardt M (1957) Der Spitzenkörper von polystictus versicolor. Planta 50: 47-50
18. Girbardt M (1969) Ultrastructure of apical region of fungal hyphae. Protoplasma 67: 413
19. 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
20. Goud B, Salminen A, Walworth NC, Novick PJ (1988) A GTP-binding protein required for secretion rapidly associates with secretory vesicles and the plasma-membrane in yeast. Cell 53: 753-768
21. Grove SN, Bracker CE (1970) Protoplasmic organization of hyphal tips amoung fungi: vesicles and Spitzenkörper. J Bacteriol 104: 989-1009
22. Grove SN, Bracker CE, Morre DJ (1970) An ultrastructural basis for hyphal tip growth in Pythium ultimum. Am J Botany 57: 245-266
23. Guo W, Roth D, Walch-Solimena C, Novick P (1999) The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 18: 1071-1080
24. Harris SD, Read ND, Roberson RW, Shaw B, Seiler S, Plamann M, Momany M (2005) Polarisome meets Spitzenkorper: microscopy, genetics, and genomics converge. Euk Cell 4: 225-229
25. Kurischko C, Kuravi VK, Wannissorn N, Nazarov P, Husain M, hang C, hokat KM, Caffery JM, Luca FC (2008) The yeast LATS/Ndr kinase Cbk1 regulates growth via Golgi-dependent glycosylation and secretion. Mol Biol Cell 19: 5559-5578
26. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, Fink GR (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949
27. 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: 506-515
28. McNemar MD, Fonzi WA (2002) Conserved serine/threonine kinase encoded by CBK1 regulates expression of several hypha-associated transcripts and genes encoding cell wall proteins in Candida albicans. J Bacteriol 184: 2058-2061
29. Medkova M, France YE, Coleman J, Novick P (2006) The rab exchange factor Sec2p reversibly associates with the exocyst. Mol Biol Cell 17: 2757-2769
30. Nair J, Muller H, Peterson M, Novick P (1990) Sec2 protein contains a coiled-coil domain essential for vesicular transport and a dispensable carboxy terminal domain. J Cell Biol 110: 1897-1909
31. Novick P, Brennwald P (1993) Friends and family - the role of the Rab GTPases in vesicular traffic. Cell 75: 597-601
32. Novick PJ, Goud B, Salminen A, Walworth NC, Nair J, Potenza M (1988) Regulation of vesicular traffic by a GTP-binding protein on the cytoplasmic surface of secretory vesicles in yeast. Cold Spring Harb Symp Quant Biol 53: 637-647
33. Novick P, Medkova M, Dong G, Hutagalung A, Reinisch K, Grosshans B (2007) Interactions between Rabs, tethers, SNAREs and their regulators in exocytosis. Biochem Soc Trans 34: 683-686
34. Ortiz D, Medkova M, Walch-Solimena C, Novick P (2002) Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J Cell Biol 157: 1005-1015
35. Park HO, Bi EF (2007) Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol Mol Biol Rev 71: 48-96
36. Schaub Y, Dunkler A, Walther A, Wendland J (2006) New pFAcassettes for PCR-based gene manipulation in Candida albicans. J Basic Microbiol 46: 416-429
37. Schulman BA, Lindstrom DL, Harlow E (1998) Substrate recruitment to cyclin-dependent kinase 2 by a multipurpose docking site on cyclin A. Proc Natl Acad Sci USA 95: 10453-10458
38. Sinha I, Wang YM, Philp R, Li CR, Yap WH, Wang Y (2007) Cyclindependent kinases control septin phosphorylation in Candida albicans hyphal development. Dev Cell 13: 421-432
39. 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
40. Sonneborn A, Bockmuhl DP, Gerads M, Kurpanek K, Sanglard D, Ernst JF (2000) Protein kinase A encoded by TPK2 regulates dimorphism of Candida albicans. Mol Microbiol 35: 386-396
41. Steinberg G (2007) Hyphal growth: a tale of motors, lipids, and the Spitzenkorper. Euk Cell 6: 351-360
42. Sudbery PE (2001) The germ tubes of Candida albicans hyphae and pseudohyphae show different patterns of septin ring localisation. Mol Microbiol 41: 19-31
43. Sudbery PE, Gow NAR, Berman J (2004) The distinct morphogenic states of Candida albicans. Trends Microbiol 12: 317-324
44. Walch-Solimena C, Collins RN, Novick PJ (1997) Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J Cell Biol 137: 1495-1509 (Pubitemid 27282232)
45. Walworth NC, Goud B, Kabcenell AK, Novick PJ (1989) Mutational analysis of Sec4 suggests a cyclical mechanism for the regulation of vesicular traffic. EMBO J 8: 1685-1693
46. 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
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
48. 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