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PMID: 11443097 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

The histone deacetylase genes HDA1 and RPD3 play distinct roles in regulation of high-frequency phenotypic switching in Candida albicans.

Journal of bacteriology ·Vol. 183 ·No. 15 ·2001-08-00 ·Pages 4614-25

Srikantha T, Tsai L, Daniels K, Klar AJ, Soll DR

Abstract

Five histone deacetylase genes (HDA1, RPD3, HOS1, HOS2, and HOS3) have been cloned from Candida albicans and characterized. Sequence analysis and comparison with 17 additional deacetylases resulted in a phylogenetic tree composed of three major groups. Transcription of the deacetylases HDA1 and RPD3 is down-regulated in the opaque phase of the white-opaque transition in strain WO-1. HOS3 is selectively transcribed as a 2.5-kb transcript in the white phase and as a less-abundant 2.3-kb transcript in the opaque phase. HDA1 and RPD3 were independently deleted in strain WO-1, and both switching between the white and opaque phases and the downstream regulation of phase-specific genes were analyzed. Deletion of HDA1 resulted in an increase in the frequency of switching from the white phase to the opaque phase, but had no effect on the frequency of switching from the opaque phase to the white phase. Deletion of RPD3 resulted in an increase in the frequency of switching in both directions. Deletion of HDA1 resulted in reduced white-phase-specific expression of the EFG1 3.2-kb transcript, but had no significant effect on white-phase-specific expression of WH11 or opaque-phase-specific expression of OP4, SAP1, and SAP3. Deletion of RPD3 resulted in reduced opaque-phase-specific expression of OP4, SAP1, and SAP3 and a slight reduction of white-phase-specific expression of WH11 and 3.2-kb EFG1. Deletion of neither HDA1 nor RPD3 affected the high level of white-phase expression and the low level of opaque-phase expression of the MADS box protein gene MCM1, which has been implicated in the regulation of opaque-phase-specific gene expression. In addition, there was no effect on the phase-regulated levels of expression of the other deacetylase genes. These results demonstrate that the two deacetylase genes HDA1 and RPD3 play distinct roles in the suppression of switching, that the two play distinct and selective roles in the regulation of phase-specific genes, and that the deacetylases are in turn regulated by switching.

MeSH Terms
Amino Acid Sequence Candida albicans/genetics,physiology Carrier Proteins/genetics Cloning, Molecular DNA-Binding Proteins/genetics Fungal Proteins/genetics,physiology Gene Expression Histone Deacetylases/genetics,physiology Intracellular Signaling Peptides and Proteins Minichromosome Maintenance 1 Protein Molecular Sequence Data Mutagenesis Nuclear Proteins Plant Proteins Repressor Proteins Saccharomyces cerevisiae Proteins Schizosaccharomyces pombe Proteins Sequence Homology, Amino Acid Transcription Factors/genetics
Chemicals
Carrier Proteins DNA-Binding Proteins Fungal Proteins Hos2 protein, S pombe Intracellular Signaling Peptides and Proteins Minichromosome Maintenance 1 Protein Nuclear Proteins Plant Proteins Repressor Proteins Saccharomyces cerevisiae Proteins Schizosaccharomyces pombe Proteins TUP1 protein, S cerevisiae Transcription Factors HDA1 protein, S cerevisiae Histone Deacetylases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Srikantha T
Department of Biological Sciences, University of Iowa, Iowa City, IA 52242, USA.
Tsai L
Daniels K
Klar A J
Soll D R
References (60)
60 references, click to expand
  1. Switching of Candida albicans during successive episodes of recurrent vaginitis.
    J Clin Microbiol. 1989 Apr;27(4):681-90 PMID: 2656742
  2. Regulation of gene expression by glucose in Saccharomyces cerevisiae: a role for ADA2 and ADA3/NGG1.
    J Bacteriol. 1999 Aug;181(16):4755-60 PMID: 10438741
  3. Bidirectional stimulation of the white-opaque transition of Candida albicans by ultraviolet irradiation.
    J Gen Microbiol. 1989 May;135(5):1201-8 PMID: 2695598
  4. Effects of neutrophils and in vitro oxidants on survival and phenotypic switching of Candida albicans WO-1.
    Infect Immun. 1990 May;58(5):1174-9 PMID: 2157666
  5. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription.
    Cell. 1990 Nov 16;63(4):751-62 PMID: 2225075
  6. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase.
    Nature. 2000 Feb 17;403(6771):795-800 PMID: 10693811
  7. EFG1 null mutants of Candida albicans switch but cannot express the complete phenotype of white-phase budding cells.
    J Bacteriol. 2000 Mar;182(6):1580-91 PMID: 10692363
  8. Sir2 links chromatin silencing, metabolism, and aging.
    Genes Dev. 2000 May 1;14(9):1021-6 PMID: 10809662
  9. Elevated phenotypic switching and drug resistance of Candida albicans from human immunodeficiency virus-positive individuals prior to first thrush episode.
    J Clin Microbiol. 2000 Oct;38(10):3595-607 PMID: 11015370
  10. Genomewide studies of histone deacetylase function in yeast.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13708-13 PMID: 11095743
  11. A histone deacetylation inhibitor and mutant promote colony-type switching of the human pathogen Candida albicans.
    Genetics. 2001 Jun;158(2):919-24 PMID: 11404352
  12. Construction of phylogenetic trees.
    Science. 1967 Jan 20;155(3760):279-84 PMID: 5334057
  13. Effects of low concentrations of zinc on the growth and dimorphism of Candida albicans: evidence for zinc-resistant and -sensitive pathways for mycelium formation.
    Infect Immun. 1979 Oct;26(1):348-54 PMID: 387610
  14. High-frequency switching of colony morphology in Candida albicans.
    Science. 1985 Nov 8;230(4726):666-9 PMID: 3901258
  15. "White-opaque transition": a second high-frequency switching system in Candida albicans.
    J Bacteriol. 1987 Jan;169(1):189-97 PMID: 3539914
  16. High-frequency switching in Candida strains isolated from vaginitis patients.
    J Clin Microbiol. 1987 Sep;25(9):1611-22 PMID: 2821060
  17. Unique phenotype of opaque cells in the white-opaque transition of Candida albicans.
    J Bacteriol. 1987 Dec;169(12):5579-88 PMID: 3316187
  18. Opaque-white phenotype transition: a programmed morphological transition in Candida albicans.
    J Bacteriol. 1988 Feb;170(2):895-9 PMID: 2828333
  19. Multiple Candida strains in the course of a single systemic infection.
    J Clin Microbiol. 1988 Aug;26(8):1448-59 PMID: 3049653
  20. A complementation analysis by parasexual recombination of Candida albicans morphological mutants.
    J Gen Microbiol. 1988 Jun;134(6):1587-95 PMID: 3065450
  21. A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA.
    Cell. 1989 Mar 10;56(5):771-6 PMID: 2647300
  22. High-frequency switching in Candida albicans.
    Clin Microbiol Rev. 1992 Apr;5(2):183-203 PMID: 1576587
  23. Transcription of the gene for a pepsinogen, PEP1, is regulated by white-opaque switching in Candida albicans.
    Mol Cell Biol. 1992 Jul;12(7):2997-3005 PMID: 1620110
  24. Coordinate regulation of two opaque-phase-specific genes during white-opaque switching in Candida albicans.
    Infect Immun. 1993 May;61(5):1823-8 PMID: 8478072
  25. Isogenic strain construction and gene mapping in Candida albicans.
    Genetics. 1993 Jul;134(3):717-28 PMID: 8349105
  26. A white-specific gene in the white-opaque switching system of Candida albicans.
    Gene. 1993 Sep 6;131(1):53-60 PMID: 7916716
  27. Three distinct secreted aspartyl proteinases in Candida albicans.
    J Bacteriol. 1993 Oct;175(19):6126-33 PMID: 8407785
  28. Genetic similarity and phenotypic diversity of commensal and pathogenic strains of Candida albicans isolated from the oral cavity.
    J Clin Microbiol. 1993 Dec;31(12):3190-9 PMID: 8308110
  29. An increase in switching frequency correlates with an increase in recombination of the ribosomal chromosomes of Candida albicans strain 3153A.
    Microbiology. 1994 Jul;140 ( Pt 7):1525-31 PMID: 8075795
  30. Expression of seven members of the gene family encoding secretory aspartyl proteinases in Candida albicans.
    Mol Microbiol. 1994 Oct;14(1):87-99 PMID: 7830564
  31. Increased phenotypic switching in strains of Candida albicans associated with invasive infections.
    J Clin Microbiol. 1994 Nov;32(11):2869-70 PMID: 7852592
  32. Functional analysis of the promoter of the phase-specific WH11 gene of Candida albicans.
    Mol Cell Biol. 1995 Mar;15(3):1797-805 PMID: 7862169
  33. Trichostatin A and trapoxin: novel chemical probes for the role of histone acetylation in chromatin structure and function.
    Bioessays. 1995 May;17(5):423-30 PMID: 7786288
  34. The sea pansy Renilla reniformis luciferase serves as a sensitive bioluminescent reporter for differential gene expression in Candida albicans.
    J Bacteriol. 1996 Jan;178(1):121-9 PMID: 8550405
  35. HDA1 and HDA3 are components of a yeast histone deacetylase (HDA) complex.
    J Biol Chem. 1996 Jun 28;271(26):15837-44 PMID: 8663039
  36. The histone deacetylase RPD3 counteracts genomic silencing in Drosophila and yeast.
    Nature. 1996 Dec 12;384(6609):589-91 PMID: 8955276
  37. HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14503-8 PMID: 8962081
  38. The WH11 gene of Candida albicans is regulated in two distinct developmental programs through the same transcription activation sequences.
    J Bacteriol. 1997 Jun;179(12):3837-44 PMID: 9190797
  39. Control of filament formation in Candida albicans by the transcriptional repressor TUP1.
    Science. 1997 Jul 4;277(5322):105-9 PMID: 9204892
  40. Histone deacetylases, acetoin utilization proteins and acetylpolyamine amidohydrolases are members of an ancient protein superfamily.
    Nucleic Acids Res. 1997 Sep 15;25(18):3693-7 PMID: 9278492
  41. Misexpression of the white-phase-specific gene WH11 in the opaque phase of Candida albicans affects switching and virulence.
    Infect Immun. 1997 Nov;65(11):4468-75 PMID: 9353021
  42. The Candida albicans CDR3 gene codes for an opaque-phase ABC transporter.
    J Bacteriol. 1997 Dec;179(23):7210-8 PMID: 9393682
  43. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  44. Transient inhibition of histone deacetylation alters the structural and functional imprint at fission yeast centromeres.
    Cell. 1997 Dec 26;91(7):1021-32 PMID: 9428524
  45. Switch of phenotype as an escape mechanism of the intruder.
    Mycoses. 1997;40 Suppl 2:9-12 PMID: 9476497
  46. Histone deacetylase activity of Rpd3 is important for transcriptional repression in vivo.
    Genes Dev. 1998 Mar 15;12(6):797-805 PMID: 9512514
  47. A role for histone deacetylase activity in HDAC1-mediated transcriptional repression.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3519-24 PMID: 9520398
  48. Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3.
    Nature. 1998 Apr 23;392(6678):831-5 PMID: 9572144
  49. Alteration of nucleosome structure as a mechanism of transcriptional regulation.
    Annu Rev Biochem. 1998;67:545-79 PMID: 9759497
  50. A fourth gene from the Candida albicans CDR family of ABC transporters.
    Gene. 1998 Oct 5;220(1-2):91-8 PMID: 9767132
  51. The two-component hybrid kinase regulator CaNIK1 of Candida albicans.
    Microbiology. 1998 Oct;144 ( Pt 10):2715-29 PMID: 9802013
  52. A MADS box protein consensus binding site is necessary and sufficient for activation of the opaque-phase-specific gene OP4 of Candida albicans.
    J Bacteriol. 1998 Dec;180(24):6607-16 PMID: 9852005
  53. A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors.
    Mol Cell Biol. 1999 Apr;19(4):3184-97 PMID: 10082585
  54. Three proteins define a class of human histone deacetylases related to yeast Hda1p.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):4868-73 PMID: 10220385
  55. Phenotypic switching in Candida albicans is controlled by a SIR2 gene.
    EMBO J. 1999 May 4;18(9):2580-92 PMID: 10228170
  56. Histone deacetylases: transcriptional repression with SINers and NuRDs.
    Trends Cell Biol. 1999 May;9(5):193-8 PMID: 10322454
  57. The regulation of gene activity by histones and the histone deacetylase RPD3.
    Cold Spring Harb Symp Quant Biol. 1998;63:391-9 PMID: 10384304
  58. A general requirement for the Sin3-Rpd3 histone deacetylase complex in regulating silencing in Saccharomyces cerevisiae.
    Genetics. 1999 Jul;152(3):921-32 PMID: 10388812
  59. Fundamentally different logic of gene regulation in eukaryotes and prokaryotes.
    Cell. 1999 Jul 9;98(1):1-4 PMID: 10412974
  60. Epigenetic inheritance of transcriptional states in S. cerevisiae.
    Cell. 1989 Nov 17;59(4):637-47 PMID: 2684414
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
DOI
10.1128/JB.183.15.4614-4625.2001
Published
2001-08-00
Pages
4614-25
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC95357
Subset
IM
Grants
NIAID NIH HHS · AI2392 · United States
External Links
PubMed source DOI: 10.1128/JB.183.15.4614-4625.2001 PMC Full Text View journal details
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