Home LiteratureArticle Details
PMID: 11809828 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Hyphal elongation is regulated independently of cell cycle in Candida albicans.

Molecular biology of the cell ·Vol. 13 ·No. 1 ·2002-01-00 ·Pages 134-45

Hazan I, Sepulveda-Becerra M, Liu H

Abstract

The mechanism for apical growth during hyphal morphogenesis in Candida albicans is unknown. Studies from Saccharomyces cerevisiae indicate that cell morphogenesis may involve cell cycle regulation by cyclin-dependent kinase. To examine whether this is the mechanism for hyphal morphogenesis, the temporal appearance of different spindle pole body and spindle structures, the cell cycle-regulated rearrangements of the actin cytoskeleton, and the phosphorylation state of the conserved Tyr19 of Cdc28 during the cell cycle were compared and found to be similar between yeast and serum-induced hyphal apical cells. These data suggest that hyphal elongation is not mediated by altering cell cycle progression or through phosphorylation of Tyr19 of Cdc28. We have also shown that germ tubes can evaginate before spindle pole body duplication, chitin ring formation, and DNA replication. Similarly, tip-associated actin polarization in each hypha occurs before the events of the G(1)/S transition and persists throughout the cell cycle, whereas cell cycle-regulated actin assemblies come and go. We have also shown that cells in phases other than G(1) can be induced to form hyphae. Hyphae induced from G(1) cells have no constrictions, and the first chitin ring is positioned in the germ tube at various distances from the base. Hyphae induced from budded cells have a constriction and a chitin ring at the bud neck, beyond which the hyphae continue to elongate with no further constrictions. Our data suggest that hyphal elongation and cell cycle morphogenesis programs are uncoupled, and each contributes to different aspects of cell morphogenesis.

MeSH Terms
Actins/metabolism Blotting, Western CDC28 Protein Kinase, S cerevisiae/metabolism Candida albicans/cytology,growth & development,metabolism Cell Cycle/physiology DNA, Fungal/metabolism Flow Cytometry Fluorescent Dyes/chemistry G1 Phase/physiology Hyphae/growth & development Indoles/chemistry Kinetics Microscopy, Fluorescence Morphogenesis Phosphorylation Protein Kinases/chemistry,metabolism Saccharomyces cerevisiae/cytology,growth & development,metabolism Spindle Apparatus/metabolism Tubulin/metabolism Tyrosine/metabolism
Chemicals
Actins DNA, Fungal Fluorescent Dyes Indoles Tubulin Tyrosine DAPI Protein Kinases CDC28 Protein Kinase, S cerevisiae
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hazan Idit
Department of Biological Chemistry, University of California-Irvine, Irvine, CA 92697-1700, USA.
Sepulveda-Becerra Marisa
Liu Haoping
References (47)
47 references, click to expand
  1. An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida Albicans.
    Sabouraudia. 1975 Jul;13(2):148-53 PMID: 808868
  2. Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis.
    J Cell Biol. 1998 Sep 7;142(5):1301-12 PMID: 9732290
  3. Filament ring formation in the dimorphic yeast Candida albicans.
    J Cell Biol. 1983 Feb;96(2):486-93 PMID: 6339518
  4. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces.
    J Cell Biol. 1984 Mar;98(3):922-33 PMID: 6365930
  5. A characterization of pH-regulated dimorphism in Candida albicans.
    Mycopathologia. 1984 Mar 15;85(1-2):21-30 PMID: 6374461
  6. Morphogenesis in Candida albicans.
    Crit Rev Microbiol. 1985;12(1):45-93 PMID: 3893894
  7. Temporal and spatial differences in cell wall expansion during bud and mycelium formation in Candida albicans.
    J Gen Microbiol. 1985 Jun;131(6):1467-80 PMID: 3900277
  8. Differences in actin localization during bud and hypha formation in the yeast Candida albicans.
    J Gen Microbiol. 1986 Jul;132(7):2035-47 PMID: 3540192
  9. A morphogenesis checkpoint monitors the actin cytoskeleton in yeast.
    J Cell Biol. 1998 Sep 21;142(6):1487-99 PMID: 9744879
  10. Control of Saccharomyces cerevisiae filamentous growth by cyclin-dependent kinase Cdc28.
    Mol Cell Biol. 1999 Feb;19(2):1369-80 PMID: 9891070
  11. Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast.
    Genes Dev. 1999 Jan 15;13(2):176-87 PMID: 9925642
  12. Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity.
    Microbiol Mol Biol Rev. 1999 Mar;63(1):54-105 PMID: 10066831
  13. A G1 cyclin is necessary for maintenance of filamentous growth in Candida albicans.
    Mol Cell Biol. 1999 Jun;19(6):4019-27 PMID: 10330142
  14. The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p.
    Mol Cell Biol. 1999 Oct;19(10):6929-39 PMID: 10490630
  15. Regulation of G2/M progression by the STE mitogen-activated protein kinase pathway in budding yeast filamentous growth.
    Mol Biol Cell. 1999 Oct;10(10):3301-16 PMID: 10512868
  16. Variation in cytoplasmic microtubule organization and spindle length between the two forms of the dimorphic fungus Candida albicans.
    J Cell Sci. 1988 Oct;91 ( Pt 2):211-20 PMID: 3077140
  17. A versatile microtiter assay for the universal cdc2 cell cycle regulator.
    Anal Biochem. 1990 May 15;187(1):94-7 PMID: 2164794
  18. The role of microfilaments and microtubules in apical growth and dimorphism of Candida albicans.
    J Gen Microbiol. 1990 Jun;136(6):1067-75 PMID: 2200842
  19. Staining of actin with fluorochrome-conjugated phalloidin.
    Methods Enzymol. 1991;194:729-31 PMID: 2005819
  20. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins.
    J Cell Biol. 1993 Mar;120(6):1305-20 PMID: 8449978
  21. Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast.
    EMBO J. 1993 May;12(5):1969-78 PMID: 8491189
  22. Isogenic strain construction and gene mapping in Candida albicans.
    Genetics. 1993 Jul;134(3):717-28 PMID: 8349105
  23. Saccharomyces cerevisiae G1 cyclins are differentially involved in invasive and pseudohyphal growth independent of the filamentation mitogen-activated protein kinase pathway.
    Genetics. 1999 Dec;153(4):1535-46 PMID: 10581264
  24. Cell-cycle checkpoints that ensure coordination between nuclear and cytoplasmic events in Saccharomyces cerevisiae.
    Curr Opin Genet Dev. 2000 Feb;10(1):47-53 PMID: 10679396
  25. Transcriptional control of cell type and morphogenesis in Candida albicans.
    Curr Opin Microbiol. 2000 Dec;3(6):582-8 PMID: 11121777
  26. Temporal and spatial regulation of Rho-type guanine-nucleotide exchange factors: the yeast perspective.
    Genes Dev. 2001 Feb 15;15(4):365-79 PMID: 11230144
  27. The role of the cytoskeleton in the polarized growth of the germ tube in Candida albicans.
    Microbiology. 1994 Feb;140 ( Pt 2):271-80 PMID: 8180692
  28. The role of microfilaments and microtubules during pH-regulated morphological transition in Candida albicans.
    Microbiology. 1994 Feb;140 ( Pt 2):281-7 PMID: 8180693
  29. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog.
    Science. 1994 Dec 9;266(5191):1723-6 PMID: 7992058
  30. Molecular cloning and analysis of CDC28 and cyclin homologues from the human fungal pathogen Candida albicans.
    Mol Gen Genet. 1994 Dec 15;245(6):716-23 PMID: 7830719
  31. Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae.
    Mol Biol Cell. 1994 Sep;5(9):1003-22 PMID: 7841518
  32. G1 cyclin turnover and nutrient uptake are controlled by a common pathway in yeast.
    Genes Dev. 1995 Feb 15;9(4):399-409 PMID: 7883165
  33. Cell cycle control of morphogenesis in budding yeast.
    Curr Opin Genet Dev. 1995 Feb;5(1):17-23 PMID: 7749320
  34. Mutational analysis of morphologic differentiation in Saccharomyces cerevisiae.
    Genetics. 1995 Aug;140(4):1259-75 PMID: 7498768
  35. Budding yeast morphogenesis: signalling, cytoskeleton and cell cycle.
    Curr Opin Cell Biol. 1995 Dec;7(6):845-55 PMID: 8608015
  36. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins.
    Cell. 1996 Mar 8;84(5):687-97 PMID: 8625407
  37. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells.
    Cell. 1996 Mar 8;84(5):699-709 PMID: 8625408
  38. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene.
    Cell. 1996 Mar 8;84(5):711-22 PMID: 8625409
  39. Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast.
    Mol Biol Cell. 1996 Nov;7(11):1657-66 PMID: 8930890
  40. Roles of Wee1 and Nim1 protein kinases in regulating the switch from mitotic division to sexual development in Schizosaccharomyces pombe.
    Mol Cell Biol. 1997 Jan;17(1):10-7 PMID: 8972180
  41. Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans.
    Microbiology. 1997 Feb;143 ( Pt 2):303-11 PMID: 9043107
  42. Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex.
    J Cell Biol. 1997 Aug 11;138(3):629-41 PMID: 9245791
  43. Virulence and hyphal formation of Candida albicans require the Ste20p-like protein kinase CaCla4p.
    Curr Biol. 1997 Aug 1;7(8):539-46 PMID: 9259554
  44. Nonfilamentous C. albicans mutants are avirulent.
    Cell. 1997 Sep 5;90(5):939-49 PMID: 9298905
  45. Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1.
    Science. 1998 Feb 27;279(5355):1355-8 PMID: 9478896
  46. Germ tube growth of Candida albicans.
    Curr Top Med Mycol. 1997 Dec;8(1-2):43-55 PMID: 9504066
  47. Commitment to germ tube or bud formation during release from stationary phase in Candida albicans.
    Exp Cell Res. 1979 Apr;120(1):167-79 PMID: 35359
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2002-01-00
Pages
134-45
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC65078
Subset
IM
Grants
NIGMS NIH HHS · R01 GM055155 · United States
NIGMS NIH HHS · GM-55155 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]