Home LiteratureArticle Details
PMID: 16628217 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Opaque cells signal white cells to form biofilms in Candida albicans.

The EMBO journal ·Vol. 25 ·No. 10 ·2006-05-17 ·Pages 2240-52

Daniels KJ, Srikantha T, Lockhart SR, Pujol C, Soll DR

Abstract

Upon homozygosis from a/alpha to a/a or alpha/alpha, Candida albicans must still switch from the 'white' to 'opaque' phenotype to mate. It was, therefore, surprising to discover that pheromone selectively upregulated mating-associated genes in mating-incompetent white cells without causing G1 arrest or shmoo formation. White cells, like opaque cells, possess pheromone receptors, although their distribution and redistribution upon pheromone treatment differ between the two cell types. In speculating about the possible role of the white cell pheromone response, it is hypothesized that in overlapping white a/a and alpha/alpha populations in nature, rare opaque cells, through the release of pheromone, signal majority white cells of opposite mating type to form a biofilm that facilitates mating. In support of this hypothesis, it is demonstrated that pheromone induces cohesiveness between white cells, minority opaque cells increase two-fold the thickness of majority white cell biofilms, and majority white cell biofilms facilitate minority opaque cell chemotropism. These results reveal a novel form of communication between switch phenotypes, analogous to the inductive events during embryogenesis in higher eukaryotes.

MeSH Terms
Biofilms Candida albicans/cytology,physiology Cell Communication/physiology Chemotaxis/physiology Gene Expression Regulation, Fungal Genes, Mating Type, Fungal Phenotype Pheromones/metabolism Receptors, Pheromone/metabolism Reproducibility of Results
Chemicals
Pheromones Receptors, Pheromone
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Daniels Karla J
Department of Biological Sciences, The University of Iowa, Iowa City, IA 52242, USA.
Srikantha Thyagarajan
Lockhart Shawn R
Pujol Claude
Soll David R
References (41)
41 references, click to expand
  1. The formation of the mesoderm in urodelean amphibians : I. Induction by the endoderm.
    Wilhelm Roux Arch Entwickl Mech Org. 1969 Dec;162(4):341-373 PMID: 28304543
  2. MFalpha1, the gene encoding the alpha mating pheromone of Candida albicans.
    Eukaryot Cell. 2003 Dec;2(6):1350-60 PMID: 14665468
  3. Ultrastructure and antigenicity of the unique cell wall pimple of the Candida opaque phenotype.
    J Bacteriol. 1990 Jan;172(1):224-35 PMID: 2403540
  4. Cell biology of mating in Candida albicans.
    Eukaryot Cell. 2003 Feb;2(1):49-61 PMID: 12582122
  5. Misexpression of the opaque-phase-specific gene PEP1 (SAP1) in the white phase of Candida albicans confers increased virulence in a mouse model of cutaneous infection.
    Infect Immun. 1999 Dec;67(12):6652-62 PMID: 10569787
  6. 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
  7. High-frequency switching in Candida strains isolated from vaginitis patients.
    J Clin Microbiol. 1987 Sep;25(9):1611-22 PMID: 2821060
  8. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p.
    Curr Biol. 2005 Jun 21;15(12):1150-5 PMID: 15964282
  9. Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans.
    Eukaryot Cell. 2005 Sep;4(9):1562-73 PMID: 16151249
  10. Mating-type gene switching in Saccharomyces cerevisiae.
    Annu Rev Genet. 1998;32:561-99 PMID: 9928492
  11. Opaque-white phenotype transition: a programmed morphological transition in Candida albicans.
    J Bacteriol. 1988 Feb;170(2):895-9 PMID: 2828333
  12. A white-specific gene in the white-opaque switching system of Candida albicans.
    Gene. 1993 Sep 6;131(1):53-60 PMID: 7916716
  13. A syntaxin homolog encoded by VAM3 mediates down-regulation of a yeast G protein-coupled receptor.
    J Biol Chem. 1999 Jan 15;274(3):1835-41 PMID: 9880567
  14. The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans.
    FEMS Microbiol Lett. 2002 Aug 27;214(1):95-100 PMID: 12204378
  15. Developmental expression of a tandemly repeated, proline-and glutamine-rich amino acid motif on hyphal surfaces on Candida albicans.
    J Biol Chem. 1996 Mar 15;271(11):6298-305 PMID: 8626424
  16. Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns.
    Eukaryot Cell. 2004 Apr;3(2):536-45 PMID: 15075282
  17. Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces.
    Infect Immun. 2002 Feb;70(2):878-88 PMID: 11796623
  18. Evolution of fungal sex chromosomes.
    Mol Microbiol. 2004 Jan;51(2):299-306 PMID: 14756773
  19. In Candida albicans, white-opaque switchers are homozygous for mating type.
    Genetics. 2002 Oct;162(2):737-45 PMID: 12399384
  20. "White-opaque transition": a second high-frequency switching system in Candida albicans.
    J Bacteriol. 1987 Jan;169(1):189-97 PMID: 3539914
  21. Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus.
    J Bacteriol. 2000 Oct;182(19):5513-20 PMID: 10986256
  22. Life cycle of the budding yeast Saccharomyces cerevisiae.
    Microbiol Rev. 1988 Dec;52(4):536-53 PMID: 3070323
  23. Unique phenotype of opaque cells in the white-opaque transition of Candida albicans.
    J Bacteriol. 1987 Dec;169(12):5579-88 PMID: 3316187
  24. Alpha-pheromone-induced "shmooing" and gene regulation require white-opaque switching during Candida albicans mating.
    Eukaryot Cell. 2003 Oct;2(5):847-55 PMID: 14555467
  25. Candida biofilm: a well-designed protected environment.
    Med Mycol. 2005 May;43(3):191-208 PMID: 16010846
  26. Role of dimorphism in the development of Candida albicans biofilms.
    J Med Microbiol. 1999 Jul;48(7):671-679 PMID: 10403418
  27. Direct evidence for ligand-induced internalization of the yeast alpha-factor pheromone receptor.
    Mol Cell Biol. 1994 Nov;14(11):7245-55 PMID: 7935439
  28. Most frequent scenario for recurrent Candida vaginitis is strain maintenance with "substrain shuffling": demonstration by sequential DNA fingerprinting with probes Ca3, C1, and CARE2.
    J Clin Microbiol. 1996 Apr;34(4):767-77 PMID: 8815082
  29. Biofilm formation by Candida species on the surface of catheter materials in vitro.
    Infect Immun. 1994 Mar;62(3):915-21 PMID: 8112864
  30. Oocyte-somatic cell interactions during follicle development in mammals.
    Anim Reprod Sci. 2004 Jul;82-83:431-46 PMID: 15271471
  31. The regulation of EFG1 in white-opaque switching in Candida albicans involves overlapping promoters.
    Mol Microbiol. 2003 Apr;48(2):523-36 PMID: 12675809
  32. Phenotypic switching in Candida glabrata accompanied by changes in expression of genes with deduced functions in copper detoxification and stress.
    Eukaryot Cell. 2005 Aug;4(8):1434-45 PMID: 16087748
  33. Metabolic specialization associated with phenotypic switching in Candidaalbicans.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14907-12 PMID: 12397174
  34. Unique aspects of gene expression during Candida albicans mating and possible G(1) dependency.
    Eukaryot Cell. 2005 Jul;4(7):1175-90 PMID: 16002644
  35. Switching at the cellular level in the white-opaque transition of Candida albicans.
    J Gen Microbiol. 1990 Oct;136(10):1925-36 PMID: 2269869
  36. High-frequency switching in Candida albicans.
    Clin Microbiol Rev. 1992 Apr;5(2):183-203 PMID: 1576587
  37. Identification and characterization of a Candida albicans mating pheromone.
    Mol Cell Biol. 2003 Nov;23(22):8189-201 PMID: 14585977
  38. Candida albicans biofilm-defective mutants.
    Eukaryot Cell. 2005 Aug;4(8):1493-502 PMID: 16087754
  39. The adhesin Hwp1 and the first daughter cell localize to the a/a portion of the conjugation bridge during Candida albicans mating.
    Mol Biol Cell. 2003 Dec;14(12):4920-30 PMID: 14565982
  40. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating.
    Cell. 2002 Aug 9;110(3):293-302 PMID: 12176317
  41. Cloning and characterization of ECE1, a gene expressed in association with cell elongation of the dimorphic pathogen Candida albicans.
    Infect Immun. 1993 Sep;61(9):3648-55 PMID: 8359888
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2006-05-17
Epub
2006-00-20
Pages
2240-52
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1462973
Subset
IM
Grants
NIAID NIH HHS · AI2392 · 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]