Genome-wide screen of Saccharomyces cerevisiae for killer toxin HM-1 resistance

Yeast

Volumn 28, Issue 1, 2011, Pages 27-41

  Miyamoto, Masahiko ^a   Furuichi, Yasuhiro ^b   Komiyama, Tadazumi ^a  

^a NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

^b GeneCare Research Institute   (Japan)

Author keywords

Genome wide screen; HM 1; Killer toxin; N linked polysaccharide; Saccharomyces cerevisiae

Indexed keywords

1,2 ALPHA MANNOSIDASE; 1,3 BETA GLUCAN SYNTHASE; AQUAGLYCEROPORIN; GLYCAN; KILLER TOXIN HM 1; MANNOSE; MANNOSIDASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE HOG1P; UNCLASSIFIED DRUG; YEAST KILLER FACTOR;

ALG3 GENE; ARTICLE; BETA CHAIN; BINDING ASSAY; CAX4 GENE; CELL MEMBRANE; FUNGAL GENE; GENE DELETION; GENETIC SCREENING; MNS1 GENE; NONHUMAN; OPEN READING FRAME; OSMOLARITY; OSMOREGULATION; OST6 GENE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; WILD TYPE; YBL083C GENE;

CELL WALL; GENE DELETION; GENES, FUNGAL; GENOME, FUNGAL; GLUCOSYLTRANSFERASES; KILLER FACTORS, YEAST; MANNOSYLTRANSFERASES; MEMBRANE PROTEINS; OPEN READING FRAMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 78650473683     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.1818     Document Type: Article

References (97)

1. Aebi M, Gassenhuber J, Domdey H, te Heesen S. 1996. Cloning and characterization of the ALG3 gene of Saccharomyces cerevisiae. Glycobiology 6: 439-444.
2. Bae-Lee MS, Carman GM. 1984. Phosphatidylserine synthesis in Saccharomyces cerevisiae. Purification and characterization of membrane-associated phosphatidylserine synthase. J Biol Chem 259: 10857-10862.
3. Beese SE, Negishi T, Levin DE. 2009. Identification of positive regulators of the yeast fps1 glycerol channel. PLoS Genet 5: e1000738.
4. Bermejo C, Rodriguez E, Garcia R, et al. 2008. The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol Biol Cell 19: 1113-1124.
5. Bidlingmaier S, Snyder M. 2002. Large-scale identification of genes important for apical growth in Saccharomyces cerevisiae by directed allele replacement technology (DART) screening. Funct Integr Genomics 1: 345-356.
6. Bonifacino JS, Weissman AM. 1998. Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu Rev Cell Dev Biol 14: 19-57.
7. Breinig F, Tipper DJ, Schmitt MJ. 2002. Kre1p, the plasma membrane receptor for the yeast K1 viral toxin. Cell 108: 395-405.
8. Buschhorn BA, Kostova Z, Medicherla B, Wolf DH. 2004. A genome-wide screen identifies Yos9p as essential for ER-associated degradation of glycoproteins. FEBS Lett 577: 422-426.
9. Bussey H. 1981. Physiology of killer factor in yeast. Adv Microb Physiol 22: 93-122.
10. Bussey H, Saville D, Hutchins K, Palfree RG. 1979. Binding of yeast killer toxin to a cell wall receptor on sensitive Saccharomyces cerevisiae. J Bacteriol 140: 888-892.
11. Camirand A, Heysen A, Grondin B, Herscovics A. 1991. Glycoprotein biosynthesis in Saccharomyces cerevisiae. Isolation and characterization of the gene encoding a specific processing alpha-mannosidase. J Biol Chem 266: 15120-15127.
12. Chavan M, Rekowicz M, Lennarz W. 2003a. Insight into functional aspects of Stt3p, a subunit of the oligosaccharyl transferase. Evidence for interaction of the N-terminal domain of Stt3p with the protein kinase C cascade. J Biol Chem 278: 51441-51447.
13. Chavan M, Suzuki T, Rekowicz M, Lennarz W. 2003b. Genetic, biochemical, and morphological evidence for the involvement of N-glycosylation in biosynthesis of the cell wall beta1, 6-glucan of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 100: 15381-15386.
14. Clerc S, Hirsch C, Oggier DM, et al. 2009. Htm1 protein generates the N-glycan signal for glycoprotein degradation in the endoplasmic reticulum. J Cell Biol 184: 159-172.
15. Davenport KR, Sohaskey M, Kamada Y, Levin DE, Gustin MC. 1995. A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem 270: 30157-30161.
16. Fernandez F, Rush JS, Toke DA, et al. 2001. The CWH8 gene encodes a dolichyl pyrophosphate phosphatase with a luminally oriented active site in the endoplasmic reticulum of Saccharomyces cerevisiae. J Biol Chem 276: 41455-41464.
17. Friedmann E, Salzberg Y, Weinberger A, Shaltiel S, Gerst JE. 2002. YOS9, the putative yeast homolog of a gene amplified in osteosarcomas, is involved in the endoplasmic reticulum (ER)-Golgi transport of GPI-anchored proteins. J Biol Chem 277: 35274-35281.
18. Garcia R, Rodriguez-Pena JM, Bermejo C, Nombela C, Arroyo J. 2009. The high osmotic response and cell wall integrity pathways cooperate to regulate transcriptional responses to zymolyase-induced cell wall stress in Saccharomyces cerevisiae. J Biol Chem 284: 10901-10911.
19. Gascon S, Neumann NP, Lampen JO. 1968. Comparative study of the properties of the purified internal and external invertases from yeast. J Biol Chem 243: 1573-1577.
20. Gauss R, Jarosch E, Sommer T, Hirsch C. 2006. A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery. Nat Cell Biol 8: 849-854.
21. Hikiji T, Miura K, Kiyono K, Shibuya I, Ohta A. 1988. Disruption of the CHO1 gene encoding phosphatidylserine synthase in Saccharomyces cerevisiae. J Biochem 104: 894-900.
22. Hohmann S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66: 300-372.
23. Hong Z, Mann P, Brown NH, et al. 1994. Cloning and characterization of KNR4, a yeast gene involved in (1, 3)-beta-glucan synthesis. Mol Cell Biol 14: 1017-1025.
24. Hosokawa N, Wada I, Hasegawa K, et al. 2001. A novel ER alpha-mannosidase-like protein accelerates ER-associated degradation. EMBO Rep 2: 415-422.
25. Jakob CA, Burda P, Roth J, Aebi M. 1998. Degradation of misfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure. J Cell Biol 142: 1223-1233.
26. Jakob CA, Bodmer D, Spirig U, et al. 2001. Htm1p, a mannosidase-like protein, is involved in glycoprotein degradation in yeast. EMBO Rep 2: 423-430.
27. Jelinek-Kelly S, Herscovics A. 1988. Glycoprotein biosynthesis in Saccharomyces cerevisiae. Purification of the alpha-mannosidase which removes one specific mannose residue from Man9GlcNAc. J Biol Chem 263: 14757-14763.
28. Kanehara K, Kawaguchi S, Ng DT. 2007. The EDEM and Yos9p families of lectin-like ERAD factors. Semin Cell Dev Biol 18: 743-750.
29. Karaoglu D, Kelleher DJ, Gilmore R. 1997. The highly conserved Stt3 protein is a subunit of the yeast oligosaccharyltransferase and forms a subcomplex with Ost3p and Ost4p. J Biol Chem 272: 32513-32520.
30. Kasahara S, Ben Inoue S, Mio T, et al. 1994a. Involvement of cell wall beta-glucan in the action of HM-1 killer toxin. FEBS Lett 348: 27-32.
31. Kasahara S, Yamada H, Mio T, et al. 1994b. Cloning of the Saccharomyces cerevisiae gene whose overexpression overcomes the effects of HM-1 killer toxin, which inhibits beta-glucan synthesis. J Bacteriol 176: 1488-1499.
32. Kelleher DJ, Karaoglu D, Mandon EC, Gilmore R. 2003. Oligosaccharyltransferase isoforms that contain different catalytic STT3 subunits have distinct enzymatic properties. Mol Cell 12: 101-111.
33. Kimura T, Kitamoto N, Matsuoka K, Nakamura K, Iimura Y, Kito Y. 1993. Isolation and nucleotide sequences of the genes encoding killer toxins from Hansenula mrakii and H. saturnus. Gene 137: 265-270.
34. Kimura T, Kitamoto N, Ohta Y, Kito Y, Iimura YJ. 1995. Structural relationships among killer toxins secreted from the killer strains of the genus Williopsis. J Ferment Bioeng 80: 85-87.
35. Kimura T, Kitamoto N, Kito Y, et al. 1997. A novel yeast gene, RHK1, is involved in the synthesis of the cell wall receptor for the HM-1 killer toxin that inhibits beta-1, 3-glucan synthesis. Mol Gen Genet 254: 139-147.
36. Kimura T, Iimura Y, Komiyama T, Karita S, Sakka K, Ohmiya K. 1998. Killing mechanism by HM-1 killer toxin of Hansenula mrakii and application of HM-1 in fermentation process to prevent contamination with wild yeasts. Rec Res Devl Ferment Bioeng 1: 225-250.
37. Kimura T, Komiyama T, Furuichi Y, et al. 1999. N-glycosylation is involved in the sensitivity of Saccharomyces cerevisiae to HM-1 killer toxin secreted from Hansenula mrakii IFO 0895. Appl Microbiol Biotechnol 51: 176-184.
38. Knauer R, Lehle L. 1999. The oligosaccharyltransferase complex from Saccharomyces cerevisiae. Isolation of the OST6 gene, its synthetic interaction with OST3, and analysis of the native complex. J Biol Chem 274: 17249-17256.
39. Komiyama T, Ohta T, Urakami H, et al. 1996. Pore formation on proliferating yeast Saccharomyces cerevisiae cell buds by HM-1 killer toxin. J Biochem 119: 731-736.
40. Komiyama T, Zhang QZ, Miyamoto M, Selvakumar D, Furuichi Y. 2004. Monoclonal antibodies and sandwich ELISA for quantitation of HM-1 killer toxin. Biol Pharm Bull 27: 691-693.
41. Kopito RR. 1997. ER quality control: the cytoplasmic connection. Cell 88: 427-430.
42. Lee KS, Irie K, Gotoh Y, et al. 1993. A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol Cell Biol 13: 3067-3075.
43. Lesage G, Sdicu AM, Menard P, Shapiro J, Hussein S, Bussey H. 2004. Analysis of beta-1, 3-glucan assembly in Saccharomyces cerevisiae using a synthetic interaction network and altered sensitivity to caspofungin. Genetics 167: 35-49.
44. Letts VA, Klig LS, Bae-Lee M, Carman GM, Henry SA. 1983. Isolation of the yeast structural gene for the membrane-associated enzyme phosphatidylserine synthase. Proc Natl Acad Sci USA 80: 7279-7283.
45. Levin DE. 2005. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69: 262-291.
46. Liu Y, Choudhury P, Cabral CM, Sifers RN. 1999. Oligosaccharide modification in the early secretory pathway directs the selection of a misfolded glycoprotein for degradation by the proteasome. J Biol Chem 274: 5861-5867.
47. Lussier M, White AM, Sheraton J, et al. 1997. Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae. Genetics 147: 435-350.
48. Luyten K, Albertyn J, Skibbe WF, et al. 1995. Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J 14: 1360-1371.
49. Marquina D, Santos A, Peinado JM. 2002. Biology of killer yeasts. Int Microbiol 5: 65-71.
50. Martin H, Castellanos MC, Cenamor R, Sanchez M, Molina M, Nombela C. 1996. Molecular and functional characterization of a mutant allele of the mitogen-activated protein-kinase gene SLT2(MPK1) rescued from yeast autolytic mutants. Curr Genet 29: 516-522.
51. Martin H, Rodriguez-Pachon JM, Ruiz C, Nombela C, Molina M. 2000. Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J Biol Chem 275: 1511-1519.
52. Miller JP, Lo RS, Ben-Hur A, et al. 2005. Large-scale identification of yeast integral membrane protein interactions. Proc Natl Acad Sci USA 102: 12123-12128.
53. Miyamoto M, Han GD, Kimura T, Furuichi Y, Komiyama T. 2005. Alanine-scanning mutagenesis of HM-1 killer toxin and the essential residues for killing activity. J Biochem 137: 517-522.
54. Miyamoto M, Onozato N, Selvakumar D, Kimura T, Furuichi Y, Komiyama T. 2006. The role of the histidine-35 residue in the cytocidal action of HM-1 killer toxin. Microbiology 152: 2951-2958.
55. Mollapour M, Piper PW. 2007. Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquaglyceroporin for endocytosis, thereby rendering cells resistant to acetic acid. Mol Cell Biol 27: 6446-6456.
56. Mollapour M, Shepherd A, Piper PW. 2009. Presence of the Fps1p aquaglyceroporin channel is essential for Hog1p activation, but suppresses Slt2(Mpk1)p activation, with acetic acid stress of yeast. Microbiology 155: 3304-3311.
57. Nakatsukasa K, Nishikawa S, Hosokawa N, Nagata K, Endo T. 2001. Mnl1p, an alpha -mannosidase-like protein in yeast Saccharomyces cerevisiae, is required for endoplasmic reticulum-associated degradation of glycoproteins. J Biol Chem 276: 8635-8638.
58. Page N, Gerard-Vincent M, Menard P, et al. 2003. A Saccharomyces cerevisiae genome-wide mutant screen for altered sensitivity to K1 killer toxin. Genetics 163: 875-894.
59. Panaretou B, Piper P. 1996. Isolation of yeast plasma membranes. Methods Mol Biol 53: 117-121.
60. Paravicini G, Cooper M, Friedli L, et al. 1992. The osmotic integrity of the yeast cell requires a functional PKC1 gene product. Mol Cell Biol 12: 4896-4905.
61. Pardo M, Monteoliva L, Vazquez P, et al. 2004. PST1 and ECM33 encode two yeast cell surface GPI proteins important for cell wall integrity. Microbiology 150: 4157-4170.
62. Park H, Lennarz WJ. 2000. Evidence for interaction of yeast protein kinase C with several subunits of oligosaccharyl transferase. Glycobiology 10: 737-744.
63. Parlati F, Dominguez M, Bergeron JJ, Thomas DY. 1995. Saccharomyces cerevisiae CNE1 encodes an endoplasmic reticulum (ER) membrane protein with sequence similarity to calnexin and calreticulin and functions as a constituent of the ER quality control apparatus. J Biol Chem 270: 244-253.
64. Philips J, Herskowitz I. 1997. Osmotic balance regulates cell fusion during mating in Saccharomyces cerevisiae. J Cell Biol 138: 961-974.
65. Plemper RK, Wolf DH. 1999. Retrograde protein translocation: ERADication of secretory proteins in health and disease. Trends Biochem Sci 24: 266-270.
66. Rose M, Winston F, Hieter P. 1990. Method in Yeast Genetics: a Laboratory Source Manual. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY.
67. Santos A, San Mauro M, Abrusci C, Marquina D. 2007. Cwp2p, the plasma membrane receptor for Pichia membranifaciens killer toxin. Mol Microbiol 64: 831-843.
68. Schagger H, von Jagow G. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368-379.
69. Sekiya-Kawasaki M, Botstein D, Ohya Y. 1998. Identification of functional connections between calmodulin and the yeast actin cytoskeleton. Genetics 150: 43-58.
70. Selvakumar D, Zhang QZ, Miyamoto M, Furuichi Y, Komiyama T. 2006. Identification and characterization of a neutralizing monoclonal antibody for the epitope on HM-1 killer toxin. J Biochem 139: 399-406.
71. Sharma CB, Knauer R, Lehle L. 2001. Biosynthesis of lipid-linked oligosaccharides in yeast: the ALG3 gene encodes the Dol-P-Man:Man5GlcNAc2-PP-Dol mannosyltransferase. Biol Chem 382: 321-328.
72. Shirai T, Kimura T, Furuichi Y, Komiyama T. 2000. The involvement of two specific arginine residues in the action of HM-1 killer toxin was deduced from site-directed mutagenesis. Biol Pharm Bull 23: 998-1000.
73. Spirig U, Glavas M, Bodmer D, et al. 1997. The STT3 protein is a component of the yeast oligosaccharyltransferase complex. Mol Gen Genet 256: 628-637.
74. Sussman A, Huss K, Chio LC, et al. 2004. Discovery of cercosporamide, a known antifungal natural product, as a selective Pkc1 kinase inhibitor through high-throughput screening. Eukaryot Cell 3: 932-943.
75. Suzuki C, Ando Y, Machida S. 2001. Interaction of SMKT, a killer toxin produced by Pichia farinosa, with the yeast cell membranes. Yeast 18: 1471-1478.
76. Szathmary R, Bielmann R, Nita-Lazar M, Burda P, Jakob CA. 2005. Yos9 protein is essential for degradation of misfolded glycoproteins and may function as lectin in ERAD. Mol Cell 19: 765-775.
77. Takasuka T, Komiyama T, Furuichi Y, Watanabe T. 1995. Cell wall synthesis specific cytocidal effect of Hansenula mrakii toxin-1 on Saccharomyces cerevisiae. Cell Mol Biol Res 41: 575-581.
78. Tamas MJ, Luyten K, Sutherland FC, et al. 1999. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol Microbiol 31: 1087-1104.
79. Terashima H, Hamada K, Kitada K. 2003. The localization change of Ybr078w/Ecm33, a yeast GPI-associated protein, from the plasma membrane to the cell wall, affecting the cellular function. FEMS Microbiol Lett 218: 175-180.
80. Toh-e A, Oguchi T. 2002. Genetic characterization of genes encoding enzymes catalyzing addition of phospho-ethanolamine to the glycosylphosphatidylinositol anchor in Saccharomyces cerevisiae. Genes Genet Syst 77: 309-322.
81. Tong AH, Boone C. 2006. Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol Biol 313: 171-192.
82. Trimble RB, Maley F. 1977. Subunit structure of external invertase from Saccharomyces cerevisiae. J Biol Chem 252: 4409-4412.
83. Tsang VC, Peralta JM, Simons AR. 1983. Enzyme-linked immunoelectrotransfer blot techniques (EITB) for studying the specificities of antigens and antibodies separated by gel electrophoresis. Meth Enzymol 92: 377-291.
84. van Berkel MA, Rieger M, te Heesen S, et al. 1999. The Saccharomyces cerevisiae CWH8 gene is required for full levels of dolichol-linked oligosaccharides in the endoplasmic reticulum and for efficient N-glycosylation. Glycobiology 9: 243-253.
85. Winzeler EA, Shoemaker DD, Astromoff A, et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
86. Woolford CA, Dixon CK, Manolson MF, Wright R, Jones EW. 1990. Isolation and characterization of PEP5, a gene essential for vacuolar biogenesis in Saccharomyces cerevisiae. Genetics 125: 739-752.
87. Xu X, Azakami H, Kato A. 2004a. P-domain and lectin site are involved in the chaperone function of Saccharomyces cerevisiae calnexin homologue. FEBS Lett 570: 155-160.
88. Xu X, Kanbara K, Azakami H, Kato A. 2004b. Expression and characterization of Saccharomyces cerevisiae Cne1p, a calnexin homologue. J Biochem 135: 615-618.
89. Yamamoto T, Hiratani T, Hirata H, Imai M, Yamaguchi H. 1986a. Killer toxin from Hansenula mrakii selectively inhibits cell wall synthesis in a sensitive yeast. FEBS Lett 197: 50-54.
90. Yamamoto T, Imai M, Tachibana K, Mayumi M. 1986b. Application of monoclonal antibodies to the isolation and characterization of a killer toxin secreted by Hansenula mrakii. FEBS Lett 195: 253-257.
91. Yamamoto T, Uchida K, Hiratani T, Miyazaki T, Yagiu J, Yamaguchi H. 1988. In vitro activity of the killer toxin from yeast Hansenula mrakii against yeasts and molds. J Antibiot (Tokyo) 41: 398-403.
92. Yamashita S, Nikawa J. 1997. Phosphatidylserine synthase from yeast. Biochim Biophys Acta 1348: 228-235.
93. Yan Q, Lennarz WJ. 2002. Studies on the function of oligosaccharyl transferase subunits. Stt3p is directly involved in the glycosylation process. J Biol Chem 277: 47692-47700.
94. Yan W, Schilke B, Pfund C, Walter W, Kim S, Craig EA. 1998. Zuotin, a ribosome-associated DnaJ molecular chaperone. EMBO J 17: 4809-4817.
95. Yoshida S, Ohya Y, Nakano A, Anraku Y. 1995. STT3, a novel essential gene related to the PKC1/STT1 protein kinase pathway, is involved in protein glycosylation in yeast. Gene 164: 167-172.
96. Young TW, Yagiu M. 1978. A comparison of the killer character in different yeasts and its classification. Antonie Van Leeuwenhoek 44: 59-77.
97. Zufferey R, Knauer R, Burda P, et al. 1995. STT3, a highly conserved protein required for yeast oligosaccharyl transferase activity in vivo. EMBO J 14: 4949-4960.