Phosphoregulation of Nap1 plays a role in septin ring dynamics and morphogenesis in Candida albicans

mBio

Volumn 5, Issue 1, 2014, Pages

  Huang, Zhen Xing ^a   Zhao, Pan ^a   Zeng, Gui Sheng ^a   Wang, Yan Ming ^a   Sudbery, Ian ^b   Wang, Yue ^a,c  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOSOME ASSEMBLY PROTEIN 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE CDC14; PHOSPHOSERINE; PHOSPHOTHREONINE; PHOSPHOTRANSFERASE; PROTEIN CLA4; PROTEIN GIN4; SEPTIN; SEPTIN RING ASSOCIATED KINASE; UNCLASSIFIED DRUG;

ALLELE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; CELL CYCLE; CELL STRUCTURE; CLUSTER ANALYSIS; CONTROLLED STUDY; FILAMENTOUS ALGA; FUNGAL CELL; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE DELETION; GENE MUTATION; HETEROZYGOTE; HOST PATHOGEN INTERACTION; MOLECULAR DYNAMICS; MORPHOGENESIS; MOUSE; MUTANT; NAP1 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; CELL CYCLE; DISEASE MODELS, ANIMAL; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; MACROMOLECULAR SUBSTANCES; MASS SPECTROMETRY; MICE; MICE, INBRED BALB C; MUTAGENESIS, SITE-DIRECTED; NUCLEOSOME ASSEMBLY PROTEIN 1; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEPTINS; VIRULENCE;

EID: 84903367204     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00915-13     Document Type: Article

References (47)

1. Hartwell LH. 1971. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp. Cell Res. 69: 265-276. http://dx.doi.org/10.1016/0014-4827(71)90223-0.
2. Oh Y, Bi E. 2011. Septin structure and function in yeast and beyond. Trends Cell Biol. 21:141-148. http://dx.doi.org/10.1016/ j.tcb.2010.11.006.
3. Saarikangas J, Barral Y. 2011. The emerging functions of septins in metazoans. EMBO Rep. 12:1118-1126. http://dx.doi.org/10.1038/ embor.2011.193.
4. Spiliotis ET, Gladfelter AS. 2012. Spatial guidance of cell asymmetry: septin GTPases show the way. Traffic 13:195-203. http://dx.doi.org/ 10.1111/j.1600-0854.2011.01268.x.
5. Bertin A, McMurray MA, Grob P, Park SS, Garcia G III, Patanwala I, Ng HL, Alber T, Thorner J, Nogales E. 2008. Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc. Natl. Acad. Sci. U. S. A. 105:8274-8279. http://dx.doi.org/10.1073/pnas.0803330105.
6. Longtine MS, Theesfeld CL, McMillan JN, Weaver E, Pringle JR, Lew DJ. 2000. Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol. Cell. Biol. 20:4049-4061. http:// dx.doi.org/10.1128/MCB.20.11.4049-4061.2000.
7. Warenda AJ, Konopka JB. 2002. Septin function in Candida albicans morphogenesis. Mol. Biol. Cell 13:2732-2746. http://dx.doi.org/10.1091/ mbc.E02-01-0013.
8. Keaton MA, Lew DJ. 2006. Eavesdropping on the cytoskeleton: progress and controversy in the yeast morphogenesis checkpoint. Curr. Opin. Microbiol. 9:540-546. http://dx.doi.org/10.1016/j.mib.2006.10.004.
9. Smolka MB, Chen SH, Maddox PS, Enserink JM, Albuquerque CP, Wei XX, Desai A, Kolodner RD, Zhou H. 2006. An FHA domain-mediated protein interaction network of Rad53 reveals its role in polarized cell growth. J. Cell Biol. 175:743-753. http://dx.doi.org/10.1083/ jcb.200605081.
10. Castillon GA, Adames NR, Rosello CH, Seidel HS, Longtine MS, Cooper JA, Heil-Chapdelaine RA. 2003. Septins have a dual role in controlling mitotic exit in budding yeast. Curr. Biol. 13:654-658. http:// dx.doi.org/10.1016/S0960-9822(03)00247-1.
11. Barral Y, Mermall V, Mooseker MS, Snyder M. 2000. Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast. Mol. Cell 5:841-851. http://dx.doi.org/10.1016/S1097-2765(00)80324-X.
12. Takizawa PA, DeRisi JL, Wilhelm JE, Vale RD. 2000. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 290:341-344. http://dx.doi.org/10.1126/ science.290.5490.341.
13. Li CR, Lee RT, Wang YM, Zheng XD, Wang Y. 2007. Candida albicans hyphal morphogenesis occurs in Sec3p-independent and Sec3pdependent phases separated by septin ring formation. J. Cell Sci. 120: 1898-1907. http://dx.doi.org/10.1242/jcs.002931.
14. Gladfelter AS, Pringle JR, Lew DJ. 2001. The septin cortex at the yeast mother-bud neck. Curr. Opin. Microbiol. 4:681-689. http://dx.doi.org/ 10.1016/S1369-5274(01)00269-7.
15. McMurray MA, Thorner J. 2009. Septins: molecular partitioning and the generation of cellular asymmetry. Cell Div. 4:18. http://dx.doi.org/ 10.1186/1747-1028-4-18.
16. Gladfelter AS, Zyla TR, Lew DJ. 2004. Genetic interactions among regulators of septin organization. Eukaryot. Cell 3:847-854. http:// dx.doi.org/10.1128/EC.3.4.847-854.2004.
17. Tjandra H, Compton J, Kellogg D. 1998. Control of mitotic events by the Cdc42 GTPase, the Clb2 cyclin and a member of the PAK kinase family. Curr. Biol. 8:991-1000. http://dx.doi.org/10.1016/S0960-9822(07)00419-8.
18. Altman R, Kellogg D. 1997. Control of mitotic events by Nap1 and the Gin4 kinase. J. Cell Biol. 138:119-130. http://dx.doi.org/10.1083/ jcb.138.1.119.
19. Li CR, Yong JY, Wang YM, Wang Y. 2012. CDK regulates septin organization through cell-cycle-dependent phosphorylation of the Nim1-related kinase Gin4. J. Cell Sci. 125:2533-2543. http://dx.doi.org/10.1242/ jcs.104497.
20. 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. http://dx.doi.org/10.1016/ j.devcel.2007.06.011.
21. Ishimi Y, Yasuda H, Hirosumi J, Hanaoka F, Yamada M. 1983. A protein which facilitates assembly of nucleosome-like structures in vitro in mammalian cells. J. Biochem. 94:735-744.
22. Zlatanova J, Seebart C, Tomschik M. 2007. Nap1: taking a closer look at a juggler protein of extraordinary skills. FASEB J. 21:1294-1310. http:// dx.doi.org/10.1096/fj.06-7199rev.
23. Kellogg DR, Murray AW. 1995. NAP1 acts with Clb1 to perform mitotic functions and to suppress polar bud growth in budding yeast. J. Cell Biol. 130:675-685. http://dx.doi.org/10.1083/jcb.130.3.675.
24. Ohkuni K, Shirahige K, Kikuchi A. 2003. Genome-wide expression analysis of NAP1 in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 306:5-9. http://dx.doi.org/10.1016/S0006-291X(03)00907-0.
25. Miyaji-Yamaguchi M, Kato K, Nakano R, Akashi T, Kikuchi A, Nagata K. 2003. Involvement of nucleocytoplasmic shuttling of yeast Nap1 in mitotic progression. Mol. Cell. Biol. 23:6672-6684. http://dx.doi.org/ 10.1128/MCB.23.18.6672-6684.2003.
26. Park YJ, Luger K. 2006. The structure of nucleosome assembly protein 1. Proc. Natl. Acad. Sci. U. S. A. 103:1248-1253. http://dx.doi.org/10.1073/ pnas.0508002103.
27. Calvert ME, Keck KM, Ptak C, Shabanowitz J, Hunt DF, Pemberton LF. 2008. Phosphorylation by casein kinase 2 regulates Nap1 localization and function. Mol. Cell. Biol. 28:1313-1325. http://dx.doi.org/10.1128/ MCB.01035-07.
28. Corner BE, Magee PT. 1997. Candida pathogenesis: unravelling the threads of infection. Curr. Biol. 7:R691-R694. http://dx.doi.org/10.1016/ S0960-9822(06)00357-5.
29. Jacobsen ID, Wilson D, Wächtler B, Brunke S, Naglik JR, Hube B. 2012. Candida albicans dimorphism as a therapeutic target. Expert Rev. Anti Infect. Ther. 10:85-93. http://dx.doi.org/10.1586/eri.11.152.
30. Sudbery PE. 2001. The germ tubes of Candida albicans hyphae and pseudohyphae show different patterns of septin ring localization. Mol. Microbiol. 41:19-31. http://dx.doi.org/10.1046/j.1365-2958.2001.02459.x.
31. Warenda AJ, Kauffman S, Sherrill TP, Becker JM, Konopka JB. 2003. Candida albicans septin mutants are defective for invasive growth and virulence. Infect. Immun. 71:4045-4051. http://dx.doi.org/10.1128/ IAI.71.7.4045-4051.2003.
32. 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. http://dx.doi.org/10.1038/sj.emboj.7600195.
33. Berman J. 2006. Morphogenesis and cell cycle progression in Candida albicans. Curr. Opin. Microbiol. 9:595-601. http://dx.doi.org/10.1016/ j.mib.2006.10.007.
34. Sudbery PE. 2011. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9:737-748. http://dx.doi.org/10.1038/nrmicro2636.
35. Longtine MS, DeMarini DJ, Valencik ML, Al-Awar OS, Fares H, De Virgilio C, Pringle JR. 1996. The septins: roles in cytokinesis and other processes. Curr. Opin. Cell Biol. 8:106-119. http://dx.doi.org/10.1016/ S0955-0674(96)80054-8.
36. Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T. 2006. Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 5:749-757.
37. Dobbelaere J, Gentry MS, Hallberg RL, Barral Y. 2003. Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev. Cell 4:345-357. http://dx.doi.org/10.1016/S1534-5807(03)00061-3.
38. Clemente-Blanco A, González-Novo A, Machín F, Caballero-Lima D, Aragón L, Sánchez M, de Aldana CR, Jiménez J, Correa-Bordes J. 2006. The Cdc14p phosphatase affects late cell-cycle events and morphogenesis in Candida albicans. J. Cell Sci. 119:1130-1143. http://dx.doi.org/10.1242/ jcs.02820.
39. Wightman R, Bates S, Amornrrattanapan P, Sudbery P. 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. http://dx.doi.org/10.1083/jcb.200307176.
40. Lew DJ. 2003. The morphogenesis checkpoint: how yeast cells watch their figures. Curr. Opin. Cell Biol. 15:648-653. http://dx.doi.org/10.1016/ j.ceb.2003.09.001.
41. Umeyama T, Kaneko A, Nagai Y, Hanaoka N, Tanabe K, Takano Y, Niimi M, Uehara Y. 2005. Candida albicans protein kinase CaHsl1p regulates cell elongation and virulence. Mol. Microbiol. 55:381-395. http://dx.doi.org/10.1111/j.1365-2958.2004.04405.x.
42. González-Novo A, Correa-Bordes J, Labrador L, Sánchez M, Vázquez de Aldana CR, Jiménez J. 2008. Sep7 is essential to modify septin ring dynamics and inhibit cell separation during Candida albicans hyphal growth. Mol. Biol. Cell 19:1509-1518. http://dx.doi.org/10.1091/ mbc.E07-09-0876.
43. Mitchell L, Lau A, Lambert JP, Zhou H, Fong Y, Couture JF, Figeys D, Baetz K. 2011. Regulation of septin dynamics by the Saccharomyces cerevisiae lysine acetyltransferase NuA4. PLoS One 6:e25336. http://dx.doi.org/ 10.1371/journal.pone.0025336.
44. Murad AM, Lee PR, Broadbent ID, Barelle CJ, Brown AJ. 2000. CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16:325-327. http://dx.doi.org/10.1002/1097-0061(20000315)16:4.
45. Bennett RJ, Uhl MA, Miller MG, Johnson AD. 2003. Identification and characterization of a Candida albicans mating pheromone. Mol. Cell. Biol. 23:8189-8201. http://dx.doi.org/10.1128/MCB.23.22.8189-8201.2003.
46. Kruppa MD. 2009. Candida albicans gene expression in an in vivo infection model. Methods Mol. Biol. 499:77-83. http://dx.doi.org/10.1007/ 978-1-60327-151-6_9.
47. Wilson RB, Davis D, Enloe BM, Mitchell AP. 2000. A recyclable Candida albicans URA3 cassette for PCR product-directed gene disruptions. Yeast 16:65-70. http://dx.doi.org/10.1002/(SICI)1097-0061(20000115)16:1.