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Genetic and molecular approaches to synthesis and action of the yeast killer toxin

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  • Pore-forming Proteins of Biological Membranes
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Summary

The K1 killer toxin ofSaccharomyces cerevisiae is a secreted, virally-coded protein lethal to sensitive yeasts. Killer yeasts are immune to the toxin they produce. This killer system has been extensively examined from genetic and molecular perspectives. Here we review the biology of killer yeasts, and examine the synthesis and action of the protein toxin and the immunity component. We summarise the structure of the toxin precursor gene and its protein products, outline the proteolytic processing of the toxin subunits from the precursor, and their passage through the yeast secretory pathway. We then discuss the mode of action of the toxin, its lectin-like interaction with a cell wall glucan, and its probable role in forming channels in the yeast plasma membrane. In addition we describe models of how a toxin precursor species functions as the immunity component, probably by interfering with channel formation. We conclude with a review of the functional domains of the toxin structural gene as determined by site-directed mutagenesis. This work has identified regions associated with glucan binding, toxin activity, and immunity.

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References

  1. Al-Aidroos, K., and Bussey, H., Chromosomal mutants ofSaccharomyces cerevisiae affecting the cell wall binding site for killer factor. Can. J. Microbiol.24 (1978) 228–237.

    Article  CAS  PubMed  Google Scholar 

  2. Bevan, E. A., Herring, A. J., and Mitchell, D. J., Preliminary characterization of two species of dsRNA in yeast and their relationship to the killer character. Nature, Lond.245 (1973) 81–86.

    Article  CAS  PubMed  Google Scholar 

  3. Boone, C., Bussey, H., Greene, D., Thomas, D. Y., and Vernet, T., Yeast killer toxin: site-directed mutations implicate the precursor protein as the immunity component. Cell46 (1986) 105–113.

    Article  CAS  PubMed  Google Scholar 

  4. Bostian, K. A., Elliot, Q., Bussey, H., Burn, V., Smith, A., and Tipper, D. J., Sequence of the preprotoxin dsRNA gene of type 1 killer yeast: multiple processing events produce a two component toxin. Cell36 (1984) 741–751.

    Article  CAS  PubMed  Google Scholar 

  5. Bostian, K. A., Hopper, J. E., Rogers, D. T., and Tipper, D. J., Translational analysis of the killer-associated virus-like particle dsRNA genome ofS. cerevisiae: M-dsRNA encodes toxin. Cell19 (1980) 404–414.

    Article  Google Scholar 

  6. Bostian, K. A., Jayachandran, S., and Tipper, D. J., A glycosylated protoxin in killer yeast: models for its structure and maturation. Cell32 (1983) 169–180.

    Article  CAS  PubMed  Google Scholar 

  7. Bussey, H., Yeast killer factor-induced turbidity changes in cells and spheroplasts of a sensitive strain. J. gen. Microbiol.82 (1974) 171–179.

    Article  Google Scholar 

  8. Bussey, H., Proteases and the processing of precursors to secreted proteins in yeast. Yeast4 (1988) 17–26.

    Article  CAS  PubMed  Google Scholar 

  9. Bussey, H., Boone, C., Dmochowska, A., Greene, D., Zhu, H., Lolle, S. J., Vernet, T., Dignard, D., and Thomas, D. Y., Secretion and action of yeast K1 killer toxin, in: Viruses of Fungi and Simple Eukaryotes, Mycology series, vol. 7, pp. 161–178. Eds Y. Koltin and M. J. Leibowitz. Marcel Dekker, New York 1988.

    Google Scholar 

  10. Bussey, H., Saville, D., Greene, D., Tipper, D. J., and Bostian, K. A., Secretion of yeast killer toxin: processing of the glycosylated precursor. Molec. cell. Biol.3 (1983) 1362–1370.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Bussey, H., Saville, D., Hutchins, K., and Palfree, R. G. E., Binding of yeast killer toxin to a cell wall receptor on sensitiveSaccharomyces cerevisiae. J. Bact.140 (1979) 888–892.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Bussey, H., and Sherman, D., Yeast killer factor: ATP leakage and coordinate inhibition of macromolecular synthesis in sensitive cells. Biochim. biophys. Acta298 (1973) 868–875.

    Article  CAS  PubMed  Google Scholar 

  13. Bussey, H., Sherman, D., and Somers, J. M., Action of yeast killer factor: a resistant mutant with sensitive spheroplasts. J. Bact.113 (1973) 1193–1197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bussey, H., and Skipper, N., Killing ofTorulopsis glabrata bySaccharomyces cerevisiae killer factor. Antimicrob. Agents Chemother.9 (1976) 352–354.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bussey, H., Steinmetz, O., and Saville, D., Protein secretion in yeast: two chromosomal mutants that oversecrete killer toxin inSaccharomyces cerevisiae. Curr. Genet.7 (1983) 449–456.

    Article  CAS  PubMed  Google Scholar 

  16. Bussey, H., Vernet, T., and Sdicu, A.-M., Mutual antagonism among killer yeasts: competition between K1 and K2 killers and a novel cDNA-based K1-K2 killer strain ofSaccharomyces cerevisiae. Can. J. Microbiol.34 (1988) 38–44.

    Article  CAS  PubMed  Google Scholar 

  17. de la Peña, P., Barros, F., Gascón, S., Lazo, P. S., and Ramos, S., The effect of yeast killer toxin on sensitive cells ofSaccharomyces cerevisiae. J. biol. Chem.256 (1981) 10420–10425.

    Article  PubMed  Google Scholar 

  18. de la Peña, P., Barros, F., Gascón, S., Ramos, S., and Lazo, P. S., Primary effects of yeast killer toxin. Biochem. biophys. Res. Commun.96 (1980) 544–550.

    Article  PubMed  Google Scholar 

  19. Dmochowska, A., Dignard, D., Henning, D., Thomas, D. Y., and Bussey, H., Yeast KEX1 gene encodes a putative protease with a carboxypeptidase B-like function involved in killer toxin and α-factor precursor processing. Cell50 (1987) 573–584.

    Article  CAS  PubMed  Google Scholar 

  20. El-Sherbeini, M., and Bostian, K. A., Viruses in fungi: infection of yeast with K1 and K2 killer viruses. Proc. natl Acad. Sci. USA84 (1987) 4293–4297.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gunge, N., Yeast DNA plasmids. A. Rev. Microbiol.37 (1983) 253–276.

    Article  CAS  Google Scholar 

  22. Hanes, S. D., Burn, V. E., Sturley, S. L., Tipper, D. J., and Bostian, K. A., Expression of a cDNA derived from the yeast killer preprotoxin gene: implications for processing and immunity. Proc. natl Acad. Sci. USA83 (1986) 1675–1679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hutchins, K., and Bussey, H., Cell wall receptor for yeast killer toxin: involvement of (1→6)-β-D-glucan. J. Bact.154 (1983) 161–169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Julius, D., Brake, A., Blair, L., Kunisawa, R., and Thorner, J., Isolation of the putative structural gene for the lysine-arginine cleaving endopeptidase required for processing of yeast prepro-α-factor. Cell37 (1984) 1075–1089.

    Article  CAS  PubMed  Google Scholar 

  25. Kagan, B. L., Mode of action of yeast killer toxins: channel formation in lipid bilayer membranes. Nature (1983) 709–711.

  26. Leibowitz, M. J., and Wickner, R. B., A chromosomal gene required for killer plasmid expression mating and sporulation inSaccharomyces cerevisiae. Proc. natl Acad. Sci. USA73 (1976) 2061–2065.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lolle, S. J., and Bussey, H., In vivo evidence for signal cleavage of the killer preprotoxin ofSaccharomyces cerevisiae. Molec. cell. Biol.6 (1986) 4274–4280.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Lolle, S. J., Skipper, N., Bussey, H., and Thomas, D. Y., The expression of cDNA clones of yeast M1 double stranded RNA in yeast confers both killer and immunity phenotypes. EMBO J.3 (1984) 1383–1387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Makower, M., and Bevan, E. A., The physiological basis of the killer character in yeast. Proc. Int. Congr. Genet. XI1 (1963) 202.

    Google Scholar 

  30. Maule, A. P., and Thomas, P. D., Strains of yeast lethal to brewery yeasts. J. Inst. Brew.79 (1973) 137–141.

    Article  Google Scholar 

  31. Middelbeek, E. J., Stumm, C., and Vogels, G. D., Effects ofPichia kluyveri killer toxin on sensitive cells. Antonie van Leeuwenhoek46 (1980) 205–220.

    Article  CAS  PubMed  Google Scholar 

  32. Mizuno, K., Nakamura, T., Oshima, T., Tanaka, S., and Matsuo, H., Yeast KEX2 gene encodes an endopeptidase homologous to subtilisin-like serine proteases. Biochem. biophys. Res. Comm.156 (1988) 246–254.

    Article  CAS  PubMed  Google Scholar 

  33. Palfree, R. G. E., and Bussey, H., Yeast killer toxin: purification and characterization of the protein toxin fromSaccharomyces cerevisiae. Eur. J. Biochem.93 (1979) 487–493.

    Article  CAS  PubMed  Google Scholar 

  34. Rogers, D., and Bevan, E. A., Group classification of killer yeasts based on cross-reactions between strains of different species and origin. J. gen. Microbiol.105 (1978) 199–202.

    Article  Google Scholar 

  35. Schmitt, M., and Radler, F., Mannoprotein of the yeast cell wall as primary receptor for the killer toxin ofSaccharomyces cerevisiae strain 28. J. gen. Microbiol.133 (1987) 3347–3354.

    CAS  PubMed  Google Scholar 

  36. Skipper, N., and Bussey, H., Mode of action of yeast toxins: energy requirement forSaccharomyces cerevisiae killer toxin. J. Bact.129 (1977) 668–677.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Skipper, N., Thomas, D. Y., and Lau, P. C. K., Cloning and sequencing of the preprotoxin-coding region of the M1-dsRNA. EMBO J.3 (1984) 107–111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Somers, J. M., and Bevan, E. A., The inheritance of the killer character in yeast. Genet. Res., Camb.13 (1969) 71–83.

    Article  CAS  Google Scholar 

  39. Starmer, W. T., Ganter, P., Aberdeen, V., Lachance, M. A., and Phaff, H. J., The ecological role of killer yeasts in natural communities of yeasts. Can. J. Microbiol.33 (1987) 783–796.

    Article  CAS  PubMed  Google Scholar 

  40. Sturley, S. L., Elliott, Q. E., LeVitre, J., Tipper, D. J., and Bostian, K., Mapping of functional domains within theSaccharomyces cerevisiae type 1 killer preprotoxin. EMBO J.5 (1986) 3381–3389.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Tipper, D. J., and Bostian, K. A., Double-stranded ribonucleic acid killer systems in yeasts. Microbiol. Rev.48 (1984) 125–156.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Vodkin, M. H., and Fink, G., A nucleic acid associated with a killer strain of yeast. Proc. natl Acad. Sci. USA70 (1973) 1069–1072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Vondrejs, A., A killer system in yeasts: applications to genetics and industry. Microbiol. Sci.4 (1987) 313–316.

    CAS  PubMed  Google Scholar 

  44. Wickner, R. B., Double-stranded RNA replication in yeast: the killer system. A. Rev. Biochem.55 (1986) 373–395.

    Article  CAS  Google Scholar 

  45. Wickner, R. B., and Leibowitz, M. J., Two chromosomal genes required for killer expression in killer strains ofSaccharomyces cerevisiae. Genetics82 (1976) 429–442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Woods, D. R., and Bevan, E. A., Studies on the nature of the killer factor produced bySaccharomyces cerevisiae. J. gen. Microbiol.51 (1968) 115–126.

    Article  CAS  PubMed  Google Scholar 

  47. Young, T. W., Killer yeasts, in: The Yeasts, vol. 2, 2nd Edn, pp. 131–164. Eds A. H. Rose and J. S. Harrison. Academic Press, London 1987.

    Google Scholar 

  48. Young, T. W., and Philliskirk, G., The production of a yeast killer factor in the chemostat and the effects of killer yeasts in mixed continuous cultures with a sensitive strain. J. appl. Bact.43 (1977) 425–436.

    Article  CAS  Google Scholar 

  49. Young, T. W., and Yagiu, M., A comparison of the killer character in different yeasts in its classification. Antonie van Leeuwenhoek. Microbiol. Serol.44 (1978) 59–77.

    Article  CAS  Google Scholar 

  50. Zhu, H., Bussey, H., Thomas, D. Y., Gagnon, J., and Bell, A. W., Determination of the carboxyl termini of the α and β subunits of yeast K1 killer toxin. J. biol. Chem.262 (1987) 10728–10732.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Dept of Biology, McGill University, H3A 1B1, Montreal, Quebec, Canada

    H. Bussey, C. Boone, H. Zhu, T. Vernet, M. Whiteway & D. Y. Thomas

  2. Genetic Engineering Section, National Research Council of Canada, Biotechnology Research Institute, H4P 2R2, Montreal, Quebec, Canada

    H. Bussey, C. Boone, H. Zhu, T. Vernet, M. Whiteway & D. Y. Thomas

Authors
  1. H. Bussey
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  2. C. Boone
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  3. H. Zhu
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  4. T. Vernet
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  5. M. Whiteway
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  6. D. Y. Thomas
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Bussey, H., Boone, C., Zhu, H. et al. Genetic and molecular approaches to synthesis and action of the yeast killer toxin. Experientia 46, 193–200 (1990). https://doi.org/10.1007/BF02027313

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