1887

Chapter 8 : Cell Cycle and Growth Control in Species

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Cell Cycle and Growth Control in Species, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817176/9781555815394_Chap08-1.gif /docserver/preview/fulltext/10.1128/9781555817176/9781555815394_Chap08-2.gif

Abstract:

This chapter describes the major morphologies and the current understanding of the cell biological and cell cycle features that distinguish them. It highlights recent insights into how cell cycle regulators influence the formation of hypha-specific cellular features in particular. Since morphogenesis and cell cycle regulation have been studied most extensively in , the chapter primarily focuses on work in . The important distinction between yeast and pseudohyphae is that pseudohyphae spend more time in G phase of the cell cycle than yeast cells , and they continue to elongate during this time. There has long been a controversy as to how pseudohyphae are related to true hyphae. Initial models suggested that yeast cells, pseudohyphae, and true hyphae reside along a continuum. Later, based on differences in cell cycle dynamics and subcellular structures, it was proposed that pseudohyphae and hyphae represent two distinct morphological states, with pseudohyphae being more like yeast form growth with respect to cell cycle progression and cell biological markers. Recent work has shed light on cell biological features associated with cell cycle progression in chlamydospores and is discussed in theis chapter. In the genome sequence, there are three G cyclins (Ccn1, Cln3, and Hgc1) and two G or B-type/mitotic cyclins (Clb2 and Clb4) that are predicted to associate with Cdc28.

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8

Key Concept Ranking

Spindle Pole Bodies
0.45413086
DNA Synthesis
0.45366636
DNA Damage
0.44776154
Plasma Membrane
0.4262912
Transmission Electron Microscopy
0.41106647
Replication Factor C
0.41106647
0.45413086
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Different morphologies imaged by differential interference contrast microscopy: (a) yeast cells; (b) true hyphae (arrow, septum); (c) pseudohyphae; (d) chlamydospore (arrow) on a suspensor cell (arrowhead); (e) opaque cells. Scale bars, 10 µm. doi:10.1128/9781555817176.ch8.f1

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Dynamics of organelles and cytoskeletal components during cell cycle progression in yeast and the first cell cycle of pseudohyphae and hyphae following induction of unbudded yeast cells. Hyphal germ tubes emerge prior to the G/S transition. The localization patterns of cytoskeletal elements are described in more detail in the text. Reprinted from reference with permission from Elsevier. doi:10.1128/9781555817176.ch8.f2

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Method of calculation of the Mi ( ). , length; d, maximum diameter; s, diameter at mother-daughter cell junction. The morphology ratio (/d) has a value near 1.0 in a sphere and becomes larger in a more filamentous cell. doi:10.1128/9781555817176.ch8.f3

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Spitzenkörper (a and b) and polarisome (d) structures at hyphal tips. FM4-64-stained vesicles (a, asterisk) and Mlc1-YFP (b) localize apically to a spherical body. Polarisome-associated protein Bud6 tagged with YFP localizes in a crescent at hyphal tips (d; corresponding differential interference contrast image is in panel c). Scale bars, 2 µm (a), 10 µm (b), and 1 µm (c). Inset (b, square), magnification of ×5. doi:10.1128/9781555817176.ch8.f4

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

Relationship between vacuolar inheritance and hyphal elongation during cell cycle progression. Cell cycle progression is noted by the arrow to the left. Prior to mitosis, the parental vacuole enlarges relative to the total cell volume. Sub-apical hyphal cells contain large vacuoles and pause at G phase; apical cells have smaller vacuolar volumes (and thus a higher volume of cytoplasm) and actively progress through the cell cycle. Prior to branching (reentry into the cell cycle [bottom panel]), subapical cell vacuoles become smaller and the volume of cytoplasm becomes larger relative to the total cell volume. Gray, vacuole; black, nucleus; black line, septum; gray line, septin ring (“presumptum”). Adapted from references and with permission from Elsevier and the American Society for Microbiology. doi:10.1128/9781555817176.ch8.f5

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6
FIGURE 6

Septin localization during the cell cycle. Shown are time-lapse differential interference contrast (top panel of each set) and fluorescence (bottom panel of each set) images of cells expressing a Cdc10 septin-yellow fluorescent protein fusion protein. In pseudohyphae (A), a septin cap localizes to the presumptive pseudohyphal bud site in G phase (a). Throughout the S and G phases, the septins organize into a collar at the mother-bud neck (b). At mitosis, the septin collar splits into two rings (c). Cytokinesis occurs between the two rings, the rings disassemble, and the new septin cap appears during the next G (d and e). Bar, 5 µm. In hyphae (B), as the germ tube emerges, a septin spot localizes to the hyphal tip (a, asterisk) and a basal septin band is visible at the mother-daughter neck (a, arrow). The classic septin ring marks the future site of septation (the presumptum; b, arrow). At later time points, the septin ring splits into two rings (c, arrowhead). Bar, 10 µm. doi:10.1128/9781555817176.ch8.f6

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 7
FIGURE 7

Cell cycle progression and cyclin levels differ in yeast cells and hyphae. In general, G cyclins persist longer and mitotic cyclins appear later in hyphae than in yeast cells. Adapted from data in references , and . doi:10.1128/9781555817176.ch8.f7

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 8
FIGURE 8

Model of G cyclin-mediated maintenance of hyphal growth and hyphaspecific cellular features. Two cyclin-CDK complexes, Ccn1-Cdc28 and Hgc1-Cdc28, act sequentially to activate the Cdc11 septin and to promote polarized growth. In addition, Hgc1-Cdc28 phosphorylates, and inhibits the localization of, the Cdc42 GAP Rga2, which results in enhancement of Cdc42 activity at the hyphal tip. Hgc1-Cdc28 also promotes the maintenance of cell-cell attachments through two pathways: phosphorylation of Sep7 to prevent Cdc14 from acting at the septum and phosphorylation of Efg1 to inhibit the expression of Ace2-activated target genes. expression is partially dependent upon the hypha-specific transcriptional activator ( ). Dotted arrows with question marks indicate possible interactions that have not been demonstrated conclusively. doi:10.1128/9781555817176.ch8.f8

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555817176.ch08
1. Akashi, T.,, T. Kanbe, and, K. Tanaka. 1994. The role of the cytoskeleton in the polarized growth of the germ tube in Candida albicans. Microbiology 140(Pt. 2):271280.
2. Akisada, T.,, K. Harada,, M. Niimi, and, A. Kamaguchi. 1983. Production of contiguously arranged chlamydospores in Candida albicans. J. Gen. Microbiol. 129:23272330.
3. Alby, K.,, and R. J. Bennett. 2009. Stress-induced phenotypic switching in Candida albicans. Mol. Biol. Cell 20:31783191.
4. Amberg, D. C.,, J. E. Zahner,, J. W. Mulholland,, J. R. Pringle, and, D. Botstein. 1997. Aip3p/Bud6p, a yeast actin-interacting protein that is involved in morphogenesis and the selection of bipolar budding sites. Mol. Biol. Cell 8:729753.
5. Andaluz, E.,, T. Ciudad,, J. Gomez-Raja,, R. Calderone, and, G. Larriba. 2006. Rad52 depletion in Candida albicans triggers both the DNA-damage checkpoint and filamentation accompanied by but independent of expression of hypha-specific genes. Mol. Microbiol. 59:14521472.
6. Anderson, J. M.,, and D. R. Soll. 1986. Differences in actin localization during bud and hypha formation in the yeast Candida albicans. J. Gen. Microbiol. 132:20352047.
7. Bachewich, C.,, A. Nantel, and, M. Whiteway. 2005. Cell cycle arrest during S or M phase generates polarized growth via distinct signals in Candida albicans. Mol. Microbiol. 57:942959.
8. Bachewich, C.,, D. Y. Thomas, and, M. Whiteway. 2003. Depletion of a polo-like kinase in Candida albicans activates cyclase-dependent hyphal-like growth. Mol. Biol. Cell 14:21632180.
9. Bachewich, C.,, and M. Whiteway. 2005. Cyclin Cln3p links G1 progression to hyphal and pseudohyphal development in Candida albicans. Eukaryot. Cell 4:95102.
10. Bai, C.,, N. Ramanan,, Y. M. Wang, and, Y. Wang. 2002. Spindle assembly checkpoint component CaMad2p is indispensable for Candida albicans survival and virulence in mice. Mol. Microbiol. 45:3144.
11. Bakerspigel, A.,, and S. Burke. 1974. A possible function of the chlamydospores of Candida albicans. Mycopathol. Mycol. Appl. 54:147152.
12. Banerjee, M.,, D. S. Thompson,, A. Lazzell,, P. L. Carlisle,, C. Pierce,, C. Monteagudo,, J. L. Lopez-Ribot, and, D. Kadosh. 2008. UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol. Biol. Cell 19:13541365.
13. Barelle, C. J.,, E. A. Bohula,, S. J. Kron,, D. Wessels,, D. R. Soll,, A. Schafer,, A. J. Brown, and, N. A. Gow. 2003. Asynchronous cell cycle and asymmetric vacuolar inheritance in true hyphae of Candida albicans. Eukaryot. Cell 2:398410.
14. Barelle, C. J.,, M. L. Richard,, C. Gaillardin,, N. A. Gow, and, A. J. Brown. 2006. Candida albicans VAC8 is required for vacuolar inheritance and normal hyphal branching. Eukaryot. Cell 5:359367.
15. Bartnicki-Garcia, S.,, D. D. Bartnicki,, G. Gierz,, R. Lopez-Franco, and, C. E. Bracker. 1995. Evidence that Spitzenkörper behavior determines the shape of a fungal hypha: a test of the hyphoid model. Exp. Mycol. 19:153159.
16. Barton, R.,, and K. Gull. 1988. Variation in cytoplasmic microtubule organization and spindle length between the two forms of the dimorphic fungus Candida albicans. J. Cell Sci. 91(Pt 2):211220.
17. Bassilana, M.,, J. Hopkins, and, R. A. Arkowitz. 2005. Regulation of the Cdc42/Cdc24 GTPase module during Candida albicans hyphal growth. Eukaryot. Cell 4:588603.
18. Bastidas, R. J.,, and J. Heitman. 2009. Trimorphic stepping stones pave the way to fungal virulence. Proc. Natl. Acad. Sci. USA 106:351352.
19. Bennett, R. J.,, and A. D. Johnson. 2005. Mating in Candida albicans and the search for a sexual cycle. Annu. Rev. Microbiol. 59:233255.
20. Bensen, E. S.,, A. Clemente-Blanco,, K. R. Finley,, J. Correa-Bordes, and, J. Berman. 2005. The mitotic cyclins Clb2p and Clb4p affect morphogenesis in Candida albicans. Mol. Biol. Cell 16:33873400.
21. Bensen, E. S.,, S. G. Filler, and, J. Berman. 2002. A fork-head transcription factor is important for true hyphal as well as yeast morphogenesis in Candida albicans. Eukaryot. Cell 1:787798.
22. Berman, J. 2006. Morphogenesis and cell cycle progression in Candida albicans. Curr. Opin. Microbiol. 9:595601.
23. Brand, A.,, S. Shanks,, V. M. Duncan,, M. Yang,, K. Mackenzie, and, N. A. Gow. 2007. Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr. Biol. 17:347352.
24. Brand, A.,, A. Vacharaksa,, C. Bendel,, J. Norton,, P. Haynes,, M. Henry-Stanley,, C. Wells,, K. Ross,, N. A. Gow, and, C. A. Gale. 2008. An internal polarity landmark is important for externally induced hyphal behaviors in Candida albicans. Eukaryot. Cell 7:712720.
25. Braun, B. R.,, and A. D. Johnson. 1997. Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277:105109.
26. Braun, B. R.,, D. Kadosh, and, A. D. Johnson. 2001. NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J. 20:47534761.
27. Bruatto, M.,, and A. Delu. 1993. Microscopical evidences for the presence of a nucleus in Candida albicans chlamydoconidia. Mycopathologia 122:103105.
28. Carlisle, P. L.,, M. Banerjee,, A. Lazzell,, C. Monteagudo,, J. L. Lopez-Ribot, and, D. Kadosh. 2009. Expression levels of a filament-specific transcriptional regulator are sufficient to determine Candida albicans morphology and virulence. Proc. Natl. Acad. Sci. USA 106:599604.
29. Chaffin, W. L. 1984. The relationship between yeast cell size and cell division in Candida albicans. Can. J. Microbiol. 30:192203.
30. Chant, J.,, and I. Herskowitz. 1991. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 65:12031212.
31. Chapa y Lazo, B.,, S. Bates, and, P. Sudbery. 2005. The G1 cyclin Cln3 regulates morphogenesis in Candida albicans. Eukaryot. Cell 4:9094.
32. Clemente-Blanco, A.,, A. Gonzalez-Novo,, F. Machin,, D. Caballero-Lima,, L. Aragon,, M. Sanchez,, C. R. de Al-dana,, J. Jimenez, and, J. Correa-Bordes. 2006. The Cdc14p phosphatase affects late cell-cycle events and morphogenesis in Candida albicans. J. Cell Sci. 119:11301143.
33. Côte, P.,, H. Hogues, and, M. Whiteway. 2009. Transcriptional analysis of the Candida albicans cell cycle. Mol. Biol. Cell 20:33633373.
34. Côte, P.,, and M. Whiteway. 2008. The role of Candida albicans FAR1 in regulation of pheromone-mediated mating, gene expression and cell cycle arrest. Mol. Microbiol. 68:392404.
35. Court, H.,, and P. Sudbery. 2007. Regulation of Cdc42 GTPase activity in the formation of hyphae in Candida albicans. Mol. Biol. Cell 18:265281.
36. Crampin, H.,, K. Finley,, M. Gerami-Nejad,, H. Court,, C. Gale,, J. Berman, and, P. Sudbery. 2005. Candida albicans hyphae have a Spitzenkörper that is distinct from the polarisome found in yeast and pseudohyphae. J. Cell Sci. 118:29352947.
37. Crombie, T.,, N. A. Gow, and, G. W. Gooday. 1990. Influence of applied electrical fields on yeast and hyphal growth of Candida albicans. J. Gen. Microbiol. 136:311317.
38. Dunkler, A.,, A. Walther,, C. A. Specht, and, J. Wend-land. 2005. Candida albicans CHT3 encodes the functional homolog of the Cts1 chitinase of Saccharomyces cerevisiae. Fungal Genet. Biol. 42:935947.
39. Dunkler, A.,, and J. Wendland. 2007. Candida albicans Rho-type GTPase-encoding genes required for polarized cell growth and cell separation. Eukaryot. Cell 6:844854.
40. Elson, S. L.,, S. M. Noble,, N. V. Solis,, S. G. Filler, and, A. D. Johnson. 2009. An RNA transport system in Candida albicans regulates hyphal morphology and invasive growth. PLoS Genet. 5:e1000664.
41. Enjalbert, B.,, and M. Whiteway. 2005. Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot. Cell 4:12031210.
42. Enserink, J. M.,, M. B. Smolka,, H. Zhou, and, R. D. Kolodner. 2006. Checkpoint proteins control morphogenetic events during DNA replication stress in Saccharomyces cerevisiae. J. Cell Biol. 175:729741.
43. Filler, S. G.,, and D. C. Sheppard. 2006. Fungal invasion of normally non-phagocytic host cells. PLoS Pathog. 2:e129.
44. Finley, K. R.,, and J. Berman. 2005. Microtubules in Candida albicans hyphae drive nuclear dynamics and connect cell cycle progression to morphogenesis. Eukaryot. Cell 4:16971711.
45. Finley, K. R.,, K. J. Bouchonville,, A. Quick, and, J. Berman. 2008. Dynein-dependent nuclear dynamics affect morphogenesis in Candida albicans by means of the Bub2p spindle checkpoint. J. Cell Sci. 121:466476.
46. Futcher, B. 1999. Cell cycle synchronization. Methods Cell Sci. 21:7986.
47. Gale, C. A.,, M. Gerami-Nejad,, M. McClellan,, S. Vandoninck,, M. S. Longtine, and, J. Berman. 2001. Candida albicans Int1p interacts with the septin ring in yeast and hyphal cells. Mol. Biol. Cell 12:35383549.
48. Gale, C. A.,, M. D. Leonard,, K. R. Finley,, L. Christensen,, M. McClellan,, D. Abbey,, C. Kurischko,, E. Bensen,, I. Tzafrir,, S. Kauffman,, J. Becker, and, J. Berman. 2009. SLA2 mutations cause SWE1-mediated cell cycle pheno-types in Candida albicans and Saccharomyces cerevisiae. Microbiology 155:38473859.
49. Gildor, T.,, R. Shemer,, A. Atir-Lande, and, D. Kornitzer. 2005. Coevolution of cyclin Pcl5 and its substrate Gcn4. Eukaryot. Cell 4:310318.
50. Girbardt, M. 1957. Der Spitzenkörper von Polystictus versicolor. Planta 50:4759.
51. Gonzalez-Novo, A.,, J. Correa-Bordes,, L. Labrador,, M. Sanchez,, C. R. Vazquez de Aldana, and, J. Jimenez. 2008. Sep7 is essential to modify septin ring dynamics and inhibit cell separation during Candida albicans hyphal growth. Mol. Biol. Cell 19:15091518.
52. Gow, N. A. 1997. Germ tube growth of Candida albicans. Curr. Top. Med. Mycol. 8:4355.
53. Gow, N. A.,, and G. W. Gooday. 1987. Cytological aspects of dimorphism in Candida albicans. Crit. Rev. Microbiol. 15:7378.
54. Gow, N. A.,, and G. W. Gooday. 1982. Growth kinetics and morphology of colonies of the filamentous form of Candida albicans. J. Gen. Microbiol. 128:21872194.
55. Gow, N. A.,, and G. W. Gooday. 1982. Vacuolation, branch production and linear growth of germ tubes in Candida albicans. J. Gen. Microbiol. 128:21952198.
56. Guan, K. L.,, and Y. Rao. 2003. Signalling mechanisms mediating neuronal responses to guidance cues. Nat. Rev. Neurosci. 4:941956.
57. Harcus, D.,, A. Nantel,, A. Marcil,, T. Rigby, and, M. Whiteway. 2004. Transcription profiling of cyclic AMP signaling in Candida albicans. Mol. Biol. Cell 15:44904499.
58. Hausauer, D. L.,, M. Gerami-Nejad,, C. Kistler-Anderson, and, C. A. Gale. 2005. Hyphal guidance and invasive growth in Candida albicans require the Ras-like GTPase Rsr1p and its GTPase-activating protein Bud2p. Eukaryot. Cell 4:12731286.
59. Hazan, I.,, and H. Liu. 2002. Hyphal tip-associated localization of Cdc42 is F-actin dependent in Candida albicans. Eukaryot. Cell 1:856864.
60. Hazan, I.,, M. Sepulveda-Becerra, and, H. Liu. 2002. Hyphal elongation is regulated independently of cell cycle in Candida albicans. Mol. Biol. Cell 13:134145.
61. Herrero, A. B.,, M. C. Lopez,, L. Fernandez-Lago, and, A. Dominguez. 1999. Candida albicans and Yarrowia lipolytica as alternative models for analysing budding patterns and germ tube formation in dimorphic fungi. Microbiology 145:27272737.
62. Homann, O. R.,, J. Dea,, S. M. Noble, and, A. D. Johnson. 2009. A phenotypic profile of the Candida albicans regulatory network. PLoS Genet. 5:e1000783.
63. Hornby, J. M.,, E. C. Jensen,, A. D. Lisec,, J. J. Tasto,, B. Jahnke,, R. Shoemaker,, P. Dussault, and, K. W. Nicker-son. 2001. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 67:29822992.
64. Howell, A. S.,, N. S. Savage,, S. A. Johnson,, I. Bose,, A. W. Wagner,, T. R. Zyla,, H. F. Nijhout,, M. C. Reed,, A. B. Goryachev, and, D. J. Lew. 2009. Singularity in polarization: rewiring yeast cells to make two buds. Cell 139:731743.
65. Huang, D.,, H. Friesen, and, B. Andrews. 2007. Pho85, a multifunctional cyclin-dependent protein kinase in budding yeast. Mol. Microbiol. 66:303314.
66. Irazoqui, J. E.,, A. S. Howell,, C. L. Theesfeld, and, D. J. Lew. 2005. Opposing roles for actin in Cdc42p polarization. Mol. Biol. Cell 16:12961304.
67. Jansons, V. K.,, and W. J. Nickerson. 1970. Induction, morphogenesis, and germination of the chlamydospore of Candida albicans. J. Bacteriol. 104:910921.
68. Jorgensen, P.,, and M. Tyers. 2004. How cells coordinate growth and division. Curr. Biol. 14:R1014–R1027.
69. Kadosh, D.,, and A. D. Johnson. 2005. Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol. Biol. Cell 16:29032912.
70. Kaksonen, M.,, Y. Sun, and, D. G. Drubin. 2003. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115:475487.
71. Kelly, M. T.,, D. M. MacCallum,, S. D. Clancy,, F. C. Odds,, A. J. Brown, and, G. Butler. 2004. The Candida albicans CaACE2 gene affects morphogenesis, adherence and virulence. Mol. Microbiol. 53:969983.
72. Kim, S. M.,, D. D. Dubey, and, J. A. Huberman. 2003. Early-replicating heterochromatin. Genes Dev. 17:330335.
73. Koren, A.,, H. J. Tsai,, I. Tirosh,, L. Burrack,, N. Barkai, and, J. Berman. 2010. Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLOS Genet. 6:e1001068.
74. Kron, S. J.,, and N. A. Gow. 1995. Budding yeast morphogenesis: signalling, cytoskeleton and cell cycle. Curr. Opin. Cell Biol. 7:845855.
75. Lew, D. J. 2003. The morphogenesis checkpoint: how yeast cells watch their figures. Curr. Opin. Cell Biol. 15:648653.
76. Li, C. R.,, R. T. Lee,, Y. M. Wang,, X. D. Zheng, and, Y. Wang. 2007. Candida albicans hyphal morphogenesis occurs in Sec3p-independent and Sec3p-dependent phases separated by septin ring formation. J. Cell Sci. 120:18981907.
77. Li, C. R.,, Y. M. Wang,, X. De Zheng,, H. Y. Liang,, J. C. Tang, and, Y. Wang. 2005. The formin family protein CaBni1p has a role in cell polarity control during both yeast and hyphal growth in Candida albicans. J. Cell Sci. 118:26372648.
78. Li, W. J.,, Y. M. Wang,, X. D. Zheng,, Q. M. Shi,, T. T. Zhang,, C. Bai,, D. Li,, J. L. Sang, and, Y. Wang. 2006. The F-box protein Grr1 regulates the stability of Ccn1, Cln3 and Hof1 and cell morphogenesis in Candida albicans. Mol. Microbiol. 62:212226.
79. Loeb, J. D.,, M. Sepulveda-Becerra,, I. Hazan, and, H. Liu. 1999. A G1 cyclin is necessary for maintenance of filamentous growth in Candida albicans. Mol. Cell. Biol. 19:40194027.
80. Longtine, M. S.,, and E. Bi. 2003. Regulation of septin organization and function in yeast. Trends Cell Biol. 13:403409.
81. Longtine, M. S.,, C. L. Theesfeld,, J. N. McMillan,, E. Weaver,, J. R. Pringle, and, D. J. Lew. 2000. Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol. Cell. Biol. 20:40494061.
82. Lopez-Franco, R.,, S. Bartnicki-Garcia, and, C. E. Bracker. 1994. Pulsed growth of fungal hyphal tips. Proc. Natl. Acad. Sci. USA 91:1222812232.
83. Luo, J.,, E. A. Vallen,, C. Dravis,, S. E. Tcheperegine,, B. Drees, and, E. Bi. 2004. Identification and functional analysis of the essential and regulatory light chains of the only type II myosin Myo1p in Saccharomyces cerevisiae. J. Cell Biol. 165:843855.
84. Martin, R.,, A. Walther, and, J. Wendland. 2005. Ras1-induced hyphal development in Candida albicans requires the formin Bni1. Eukaryot. Cell 4:17121724.
85. Martin, S. W.,, L. M. Douglas, and, J. B. Konopka. 2005. Cell cycle dynamics and quorum sensing in Candida albicans chlamydospores are distinct from budding and hyphal growth. Eukaryot. Cell 4:11911202.
86. McMillan, J. N.,, M. S. Longtine,, R. A. Sia,, C. L. Theesfeld,, E. S. Bardes,, J. R. Pringle, and, D. J. Lew. 1999. The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p. Mol. Cell. Biol. 19:69296939.
87. Merson-Davies, L. A.,, and F. C. Odds. 1989. A morphology index for characterization of cell shape in Candida albicans. J. Gen. Microbiol. 135:31433152.
88. Miller, M. G.,, and A. D. Johnson. 2002. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 110:293302.
89. Miller, S. E.,, and W. R. Finnerty. 1979. Age-related physiological studies comparing Candida albicans chlamydospores to yeasts. Can. J. Microbiol. 25:765772.
90. Mitchell, L. H.,, and D. R. Soll. 1979. Commitment to germ tube or bud formation during release from stationary phase in Candida albicans. Exp. Cell Res. 120:167179.
91. Miyakawa, Y. 2000. Identification of a Candida albicans homologue of the PHO85 gene, a negative regulator of the PHO system in Saccharomyces cerevisiae. Yeast 16:10451051.
92. Montazeri, M.,, and H. G. Hedrick. 1984. Factors affecting spore formation in a Candida albicans strain. Appl. Environ. Microbiol. 47:13411342.
93. Moran, G. P.,, D. M. MacCallum,, M. J. Spiering,, D. C. Coleman, and, D. J. Sullivan. 2007. Differential regulation of the transcriptional repressor NRG1 accounts for altered host-cell interactions in Candida albicans and Candida dubliniensis. Mol. Microbiol. 66:915929.
94. Moseley, J. B.,, and B. L. Goode. 2006. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70:605645.
95. Nantel, A.,, D. Dignard,, C. Bachewich,, D. Harcus,, A. Marcil,, A. P. Bouin,, C. W. Sensen,, H. Hogues,, M. van het Hoog,, P. Gordon,, T. Rigby,, F. Benoit,, D. C. Tessier,, D. Y. Thomas, and, M. Whiteway. 2002. Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13:34523465.
96. Nielsen, K.,, and J. Heitman. 2007. Sex and virulence of human pathogenic fungi. Adv. Genet. 57:143173.
97. Odds, F. C. 1988. Candida and Candidosis, p. 42–59. Tindall, London, United Kingdom.
98. Ozaki-Kuroda, K.,, Y. Yamamoto,, H. Nohara,, M. Kinoshita,, T. Fujiwara,, K. Irie, and, Y. Takai. 2001. Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:827839.
99. Park, H. O.,, J. Chant, and, I. Herskowitz. 1993. BUD2 encodes a GTPase-activating protein for Bud1/Rsr1 necessary for proper bud-site selection in yeast. Nature 365:269274.
100. Pruyne, D.,, M. Evangelista,, C. Yang,, E. Bi,, S. Zigmond,, A. Bretscher, and, C. Boone. 2002. Role of formins in actin assembly: nucleation and barbed-end association. Science 297:612615.
101. Rajnicek, A. M.,, L. E. Foubister, and, C. D. McCaig. 2006. Growth cone steering by a physiological electric field requires dynamic microtubules, microfilaments and Rac-mediated filopodial asymmetry. J. Cell Sci. 119:17361745.
102. Rajnicek, A. M.,, L. E. Foubister, and, C. D. McCaig. 2006. Temporally and spatially coordinated roles for Rho, Rac, Cdc42 and their effectors in growth cone guidance by a physiological electric field. J. Cell Sci. 119:17231735.
103. Raudonis, B. M.,, and A. G. Smith. 1982. Germination of the chlamydospores of Candida albicans. Mycopathologia 78:8791.
104. Reynaga-Pena, C. G.,, G. Gierz, and, S. Bartnicki-Garcia. 1997. Analysis of the role of the Spitzenkörper in fungal morphogenesis by computer simulation of apical branching in Aspergillus niger. Proc. Natl. Acad. Sci. USA 94:90969101.
105. Saville, S. P.,, A. L. Lazzell,, A. K. Chaturvedi,, C. Monteagudo, and, J. L. Lopez-Ribot. 2008. Use of a genetically engineered strain to evaluate the pathogenic potential of yeast cell and filamentous forms during Candida albicans systemic infection in immunodeficient mice. Infect. Immun. 76:97102.
106. Sellam, A.,, C. Askew,, E. Epp,, F. Tebbji,, A. Mullick,, M. Whiteway, and, A. Nantel. 2010. Role of the transcription factor CaNdt80p in cell separation, hyphal growth and virulence in Candida albicans. Eukaryot. Cell 9:634644.
107. Sevilla, M. J.,, and F. C. Odds. 1986. Development of Candida albicans hyphae in different growth media—variations in growth rates, cell dimensions and timing of morphogenetic events. J. Gen. Microbiol. 132:30833088.
108. Shannon, J. L. 1981. Scanning and transmission electron microscopy of Candida albicans chlamydospores. J. Gen. Microbiol. 125:199203.
109. Sheu, Y. J.,, B. Santos,, N. Fortin,, C. Costigan, and, M. Snyder. 1998. Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol. Cell. Biol. 18:40534069.
110. Shi, Q. M.,, Y. M. Wang,, X. D. Zheng,, R. T. Lee, and, Y. Wang. 2007. Critical role of DNA checkpoints in mediating genotoxic-stress-induced filamentous growth in Candida albicans. Mol. Biol. Cell 18:815826.
111. Shrewsbury, J. F. D. 1934. The genus Monilia. J. Pathol. Bacteriol. 38:313354.
112. Sinha, I.,, Y. M. Wang,, R. Philp,, C. R. Li,, W. H. Yap, and, Y. Wang. 2007. Cyclin-dependent kinases control septin phosphorylation in Candida albicans hyphal development. Dev. Cell 13:421432.
113. Slutsky, B.,, M. Staebell,, J. Anderson,, L. Risen,, M. Pfaller, and, D. R. Soll. 1987. “White-opaque transition”: a second high-frequency switching system in Candida albicans. J. Bacteriol. 169:189197.
114. Smolka, M. B.,, S. H. Chen,, P. S. Maddox,, J. M. Enserink,, C. P. Albuquerque,, X. X. Wei,, A. Desai,, R. D. Kolodner, and, H. Zhou. 2006. An FHA domain-mediated protein interaction network of Rad53 reveals its role in polarized cell growth. J. Cell Biol. 175:743753.
115. Snyder, M. 1989. The SPA2 protein of yeast localizes to sites of cell growth. J. Cell Biol. 108:14191429.
116. Soll, D. R. 1997. Gene regulation during high-frequency switching in Candida albicans. Microbiology 143(Pt. 2):279288.
117. Soll, D. R. 2009. Why does Candida albicans switch? FEMS Yeast Res. 9:973989.
118. Soll, D. R.,, and L. H. Mitchell. 1983. Filament ring formation in the dimorphic yeast Candida albicans. J. Cell Biol. 96:486493.
119. Soll, D. R.,, B. Morrow, and, T. Srikantha. 1993. High-frequency phenotypic switching in Candida albicans. Trends Genet. 9:6165.
120. Song, Y.,, and J. Y. Kim. 2006. Role of CaBud6p in the polarized growth of Candida albicans. J. Microbiol. 44:311319.
121. Staib, P.,, and J. Morschhauser. 2007. Chlamydospore formation in Candida albicans and Candida dubliniensis—an enigmatic developmental programme. Mycoses 50:112.
122. Staib, P.,, and J. Morschhauser. 2005. Liquid growth conditions for abundant chlamydospore formation in Candida dubliniensis. Mycoses 48:5054.
123. Stuart, D.,, and C. Wittenberg. 1995. CLN3, not positive feedback, determines the timing of CLN2 transcription in cycling cells. Genes Dev. 9:27802794.
124. Sudbery, P.,, N. Gow, and, J. Berman. 2004. The distinct morphogenic states of Candida albicans. Trends Microbiol. 12:317324.
125. Sudbery, P. E. 2001. The germ tubes of Candida albicans hyphae and pseudohyphae show different patterns of septin ring localization. Mol. Microbiol. 41:1931.
126. Torosantucci, A.,, and A. Cassone. 1983. Induction and morphogenesis of chlamydospores in an agerminative variant of Candida albicans. Sabouraudia 21:4957.
127. Uchida, M.,, G. McDermott,, M. Wetzler,, M. A. Le Gros,, M. Myllys,, C. Knoechel,, A. E. Barron, and, C. A. Larabell. 2009. Soft X-ray tomography of phenotypic switching and the cellular response to antifungal peptoids in Candida albicans. Proc. Natl. Acad. Sci. USA 106:1937519380.
128. Uhl, M. A.,, M. Biery,, N. Craig, and, A. D. Johnson. 2003. Haploinsufficiency-based large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C. albicans. EMBO J. 22:26682678.
129. Umeyama, T.,, A. Kaneko,, M. Niimi, and, Y. Uehara. 2006. Repression of CDC28 reduces the expression of the morphology-related transcription factors, Efg1p, Nrg1p, Rbf1p, Rim101p, Fkh2p and Tec1p and induces cell elongation in Candida albicans. Yeast 23:537552.
130. Uppuluri, P.,, and W. L. Chaffin. 2007. Defining Candida albicans stationary phase by cellular and DNA replication, gene expression and regulation. Mol. Microbiol. 64:15721586.
131. van der Walt, J. P. 1967. Sexually active strains of Candida albicans and Cryptococcus albidus. Antonie van Leeuwenhoek 33:246256.
132. Vernis, L.,, A. Abbas,, M. Chasles,, C. M. Gaillardin,, C. Brun,, J. A. Huberman, and, P. Fournier. 1997. An origin of replication and a centromere are both needed to establish a replicative plasmid in the yeast Yarrowia lipolytica. Mol. Cell. Biol. 17:19952004.
133. Veses, V.,, M. Casanova,, A. Murgui,, A. Dominguez,, N. A. Gow, and, J. P. Martinez. 2005. ABG1, a novel and essential Candida albicans gene encoding a vacuolar protein involved in cytokinesis and hyphal branching. Eukaryot. Cell 4:10881101.
134. Veses, V.,, A. Richards, and, N. A. Gow. 2009. Vacuole inheritance regulates cell size and branching frequency of Candida albicans hyphae. Mol. Microbiol. 71:505519.
135. Vidotto, V.,, M. Bruatto,, G. Accattatis, and, S. Caramello. 1996. Observation on the nucleic acids in the chlamydospores of Candida albicans. New Microbiol. 19:327334.
136. Wang, A.,, S. Lane,, Z. Tian,, A. Sharon,, I. Hazan, and, H. Liu. 2007. Temporal and spatial control of HGC1 expression results in Hgc1 localization to the apical cells of hyphae in Candida albicans. Eukaryot. Cell 6:253261.
137. Wang, Y. 2009. CDKs and the yeast-hyphal decision. Curr. Opin. Microbiol. 12:644649.
138. Warenda, A. J.,, and J. B. Konopka. 2002. Septin function in Candida albicans morphogenesis. Mol. Biol. Cell 13:27322746.
139. Whiteway, M.,, and C. Bachewich. 2007. Morphogenesis in Candida albicans. Annu. Rev. Microbiol. 61:529553.
140. Wightman, R.,, S. Bates,, P. Amornrrattanapan, and, P. Sudbery. 2004. In Candida albicans, the Nim1 kinases Gin4 and Hsl1 negatively regulate pseudohypha formation and Gin4 also controls septin organization. J. Cell Biol. 164:581591.
141. Wolfe, K. H.,, and D. C. Shields. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708713.
142. Yaar, L.,, M. Mevarech, and, Y. Koltin. 1997. A Candida albicans RAS-related gene (CaRSR1) is involved in budding, cell morphogenesis and hypha development. Microbiology 143:30333044.
143. Yokoyama, K.,, H. Kaji,, K. Nishimura, and, M. Miyaji. 1990. The role of microfilaments and microtubules in apical growth and dimorphism of Candida albicans. J. Gen. Microbiol. 136:10671075.
144. Zeidler, U.,, T. Lettner,, C. Lassnig,, M. Muller,, R. Lajko,, H. Hintner,, M. Breitenbach, and, A. Bito. 2009. UME6 is a crucial downstream target of other transcriptional regulators of true hyphal development in Candida albicans. FEMS Yeast Res. 9:126142.
145. Zheng, X.,, and Y. Wang. 2004. Hgc1, a novel hyphaspecific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis. EMBO J. 23:18451856.
146. Zheng, X. D.,, R. T. Lee,, Y. M. Wang,, Q. S. Lin, and, Y. Wang. 2007. Phosphorylation of Rga2, a Cdc42 GAP, by CDK/Hgc1 is crucial for Candida albicans hyphal growth. EMBO J. 26:37603769.
147. Zheng, X. D.,, Y. M. Wang, and, Y. Wang. 2003. CaSPA2 is important for polarity establishment and maintenance in Candida albicans. Mol. Microbiol. 49:13911405.
148. Zhu, W.,, and S. G. Filler. 2010. Interactions of Candida albicans with epithelial cells. Cell. Microbiol. 12:273282.
149. Ziman, M.,, D. Preuss,, J. Mulholland,, J. M. O’Brien,, D. Botstein, and, D. I. Johnson. 1993. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity. Mol. Biol. Cell 4:13071316.
150. Zou, H.,, H. M. Fang,, Y. Zhu, and, Y. Wang. 2009. Candida albicans Cyr1, Cap1 and G-actin form a sensor/effector apparatus for activating cAMP synthesis in hyphal growth. Mol. Microbiol. 75:579591.

Tables

Generic image for table
TABLE 1

Cell biological features of morphologies

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8
Generic image for table
TABLE 2

Cell cycle-related gene sequences in C.

Citation: Gale C, Berman J. 2012. Cell Cycle and Growth Control in Species, p 101-124. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch8

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error