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PMID: 16467463 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The [PSI+] prion of Saccharomyces cerevisiae can be propagated by an Hsp104 orthologue from Candida albicans.

Eukaryotic cell ·Vol. 5 ·No. 2 ·2006-02-00 ·Pages 217-25

Zenthon JF, Ness F, Cox B, Tuite MF

Abstract

The molecular chaperone Hsp104 is not only a key component of the cellular machinery induced to disassemble aggregated proteins in stressed cells of Saccharomyces cerevisiae but also plays an essential role in the propagation of the [PSI+], [URE3], and [RNQ/PIN+] prions in this organism. Here we demonstrate that the fungal pathogen Candida albicans carries an 899-residue stress-inducible orthologue of Hsp104 (CaHsp104) that shows a high degree of amino acid identity to S. cerevisiae Hsp104 (ScHsp104). This identity is significantly lower in the N- and C-terminal regions implicated in substrate recognition and cofactor binding, respectively. CaHsp104 is able to provide all known functions of ScHsp104 in an S. cerevisiae hsp104 null mutant, i.e., tolerance to high-temperature stress, reactivation of heat-denatured proteins, and propagation of the [PSI+] prion. As also observed for ScHsp104, overexpression of CaHsp104 leads to a loss of the [PSI+] prion. However, unlike that of ScHsp104, CaHsp104 function is resistant to guanidine hydrochloride (GdnHCl), an inhibitor of the ATPase activity of this chaperone. These findings have implications both in terms of the mechanism of inhibition of Hsp104 by GdnHCl and in the evolution of the ability of fungal species to propagate prions.

MeSH Terms
Amino Acid Sequence Candida albicans/drug effects,metabolism Fungal Proteins/chemistry,metabolism Gene Expression Regulation, Fungal Genetic Complementation Test Guanidine/pharmacology Heat-Shock Proteins Hyperthermia, Induced Molecular Sequence Data Peptide Termination Factors Prions/metabolism Saccharomyces cerevisiae/cytology,genetics,metabolism Saccharomyces cerevisiae Proteins/metabolism Sequence Alignment Subcellular Fractions
Chemicals
Fungal Proteins Heat-Shock Proteins Peptide Termination Factors Prions SUP35 protein, S cerevisiae Saccharomyces cerevisiae Proteins HsP104 protein, S cerevisiae Guanidine
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Zenthon Joanna F
Protein Science Group, Department of Biosciences, University of Kent, Canterbury, Kent CT2 7NJ, United Kingdom.
Ness Frederique
Cox Brian
Tuite Mick F
References (48)
48 references, click to expand
  1. HSP104 required for induced thermotolerance.
    Science. 1990 Jun 1;248(4959):1112-5 PMID: 2188365
  2. Studies on transformation of Escherichia coli with plasmids.
    J Mol Biol. 1983 Jun 5;166(4):557-80 PMID: 6345791
  3. Hsp104 is required for tolerance to many forms of stress.
    EMBO J. 1992 Jun;11(6):2357-64 PMID: 1600951
  4. Defining a pathway of communication from the C-terminal peptide binding domain to the N-terminal ATPase domain in a AAA protein.
    Mol Cell. 2002 Apr;9(4):751-60 PMID: 11983167
  5. Dominant gain-of-function mutations in Hsp104p reveal crucial roles for the middle region.
    Mol Biol Cell. 2004 May;15(5):2061-72 PMID: 14978213
  6. Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants.
    EMBO J. 2002 Jan 15;21(1-2):12-21 PMID: 11782421
  7. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+].
    Science. 1995 May 12;268(5212):880-4 PMID: 7754373
  8. Structure and replication of yeast prions.
    Cell. 1998 Jul 10;94(1):13-6 PMID: 9674422
  9. Conservation of the prion properties of Ure2p through evolution.
    Mol Biol Cell. 2003 Aug;14(8):3449-58 PMID: 12925776
  10. Protein disaggregation mediated by heat-shock protein Hsp104.
    Nature. 1994 Dec 1;372(6505):475-8 PMID: 7984243
  11. The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state.
    Cell. 2003 Oct 17;115(2):229-40 PMID: 14567920
  12. Propagation of Saccharomyces cerevisiae [PSI+] prion is impaired by factors that regulate Hsp70 substrate binding.
    Mol Cell Biol. 2004 May;24(9):3928-37 PMID: 15082786
  13. Molecular perspectives on p97-VCP: progress in understanding its structure and diverse biological functions.
    J Struct Biol. 2004 Apr-May;146(1-2):44-57 PMID: 15037236
  14. Prions as protein-based genetic elements.
    Annu Rev Microbiol. 2002;56:703-41 PMID: 12142498
  15. Mechanism of cross-species prion transmission: an infectious conformation compatible with two highly divergent yeast prion proteins.
    Cell. 2005 Apr 8;121(1):49-62 PMID: 15820678
  16. Conservation of a portion of the S. cerevisiae Ure2p prion domain that interacts with the full-length protein.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99 Suppl 4:16384-91 PMID: 12177423
  17. Unscrambling an egg: protein disaggregation by AAA+ proteins.
    Microb Cell Fact. 2004 Jan 16;3(1):1 PMID: 14728719
  18. AAA+ proteins: have engine, will work.
    Nat Rev Mol Cell Biol. 2005 Jul;6(7):519-29 PMID: 16072036
  19. Mechanism of prion loss after Hsp104 inactivation in yeast.
    Mol Cell Biol. 2001 Jul;21(14):4656-69 PMID: 11416143
  20. The diploid genome sequence of Candida albicans.
    Proc Natl Acad Sci U S A. 2004 May 11;101(19):7329-34 PMID: 15123810
  21. Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA.
    Proc Natl Acad Sci U S A. 1972 Aug;69(8):2110-4 PMID: 4559594
  22. A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions.
    EMBO J. 1993 May;12(5):1997-2003 PMID: 8387917
  23. Guanidine hydrochloride inhibits the generation of prion "seeds" but not prion protein aggregation in yeast.
    Mol Cell Biol. 2002 Aug;22(15):5593-605 PMID: 12101251
  24. An animal model to discern torsin function: suppression of protein aggregation in C. elegans.
    Adv Neurol. 2004;94:79-85 PMID: 14509658
  25. The prion curing agent guanidinium chloride specifically inhibits ATP hydrolysis by Hsp104.
    J Biol Chem. 2004 Feb 27;279(9):7378-83 PMID: 14668331
  26. Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae.
    Genetics. 1996 Dec;144(4):1375-86 PMID: 8978027
  27. Analysis of the generation and segregation of propagons: entities that propagate the [PSI+] prion in yeast.
    Genetics. 2003 Sep;165(1):23-33 PMID: 14504215
  28. Molecular basis of a yeast prion species barrier.
    Cell. 2000 Jan 21;100(2):277-88 PMID: 10660050
  29. Hsp104 interacts with Hsp90 cochaperones in respiring yeast.
    Mol Cell Biol. 2001 Nov;21(22):7569-75 PMID: 11604493
  30. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  31. Chaperoning prions: the cellular machinery for propagating an infectious protein?
    Bioessays. 2005 Aug;27(8):823-32 PMID: 16015602
  32. Agents that cause a high frequency of genetic change from [psi+] to [psi-] in Saccharomyces cerevisiae.
    Genetics. 1981 Aug;98(4):691-711 PMID: 7037537
  33. Amino acid residue 184 of yeast Hsp104 chaperone is critical for prion-curing by guanidine, prion propagation, and thermotolerance.
    Proc Natl Acad Sci U S A. 2002 Jul 23;99(15):9936-41 PMID: 12105276
  34. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins.
    Cell. 1998 Jul 10;94(1):73-82 PMID: 9674429
  35. An Arabidopsis heat shock protein complements a thermotolerance defect in yeast.
    Plant Cell. 1994 Dec;6(12):1899-909 PMID: 7866032
  36. Analysis of the AAA sensor-2 motif in the C-terminal ATPase domain of Hsp104 with a site-specific fluorescent probe of nucleotide binding.
    Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):2732-7 PMID: 11867765
  37. Guanidine hydrochloride inhibits Hsp104 activity in vivo: a possible explanation for its effect in curing yeast prions.
    Curr Microbiol. 2001 Jul;43(1):7-10 PMID: 11375656
  38. Saccharomyces cerevisiae Hsp104 enhances the chaperone capacity of human cells and inhibits heat stress-induced proapoptotic signaling.
    Biochemistry. 2004 Jun 29;43(25):8107-15 PMID: 15209506
  39. Lon and Clp family proteases and chaperones share homologous substrate-recognition domains.
    Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):6678-82 PMID: 10359771
  40. Upregulation of the Hsp104 chaperone at physiological temperature during recovery from thermal insult.
    Mol Microbiol. 2004 Apr;52(1):217-25 PMID: 15049822
  41. The elimination of the yeast [PSI+] prion by guanidine hydrochloride is the result of Hsp104 inactivation.
    Mol Microbiol. 2001 Jun;40(6):1357-69 PMID: 11442834
  42. Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers.
    Science. 2004 Jun 18;304(5678):1793-7 PMID: 15155912
  43. The Candida albicans Sup35p protein (CaSup35p): function, prion-like behaviour and an associated polyglutamine length polymorphism.
    Microbiology. 2002 Apr;148(Pt 4):1049-60 PMID: 11932450
  44. Strains of [PSI(+)] are distinguished by their efficiencies of prion-mediated conformational conversion.
    EMBO J. 2001 Nov 15;20(22):6236-45 PMID: 11707395
  45. Molecular characterization of rice hsp101: complementation of yeast hsp104 mutation by disaggregation of protein granules and differential expression in indica and japonica rice types.
    Plant Mol Biol. 2003 Mar;51(4):543-53 PMID: 12650620
  46. Antagonistic interactions between yeast chaperones Hsp104 and Hsp70 in prion curing.
    Mol Cell Biol. 1999 Feb;19(2):1325-33 PMID: 9891066
  47. Transformation of intact yeast cells treated with alkali cations.
    J Bacteriol. 1983 Jan;153(1):163-8 PMID: 6336730
  48. The ClpB/Hsp104 molecular chaperone-a protein disaggregating machine.
    J Struct Biol. 2004 Apr-May;146(1-2):99-105 PMID: 15037241
Article Info
Journal
Eukaryotic cell
Abbr.
Eukaryot Cell
ISSN
1535-9778
Published
2006-02-00
Pages
217-25
Language
English
Region
United States
NLM ID
101130731
PMCID
PMC1405891
Subset
IM
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