Protein localisation approaches for understanding yeast cell wall biogenesis

Microscopy Research and Technique

Volumn 51, Issue 6, 2000, Pages 601-612

  Molina, María ^a   Gil, Concha ^a   Pla, Jesús ^a   Arroyo, Javier ^a   Nombela, César ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Epitope tagging; GFP; GPI; Mannoprotein; Proteomics

Indexed keywords

BIOSYNTHESIS; CELL MEMBRANES; CYTOLOGY; MOLECULAR BIOLOGY; YEAST;

CELL WALL BIOGENESIS; CELL WALLS; CELL/B.E; EPITOPE-TAGGING; GFP; GPI; MANNOPROTEINS; PROTEIN LOCALIZATION; PROTEOMICS; YEAST CELL;

PROTEINS;

ARTICLE; CELL STRUCTURE; CELL SURFACE; CELL VIABILITY; CELL WALL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; YEAST;

EID: 0034671318     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/1097-0029(20001215)51:6<601::AID-JEMT9>3.0.CO;2-I     Document Type: Article

References (87)

1. Angiolella L, Facchin M, Stringaro A, Maras B, Simonetti N, Cassone A. 1996. Identification of a glucan-associated enolase as a main cell wall protein of Candida albicans and an indirect target of lipopeptide antimycotics. J Infect Dis 173:684-690.
2. Ash J, Dominguez M, Bergeron JJ, Thomas DY, Bourbonnais Y. 1995. The yeast proprotein convertase encoded by YAP3 is a glycophosphatidylinositol-anchored protein that localizes to the plasma membrane. J Biol Chem 270:20847-20854.
3. Blackstock WP, Weir MP. 1999. Proteomics: quantitative and physical mapping of cellular proteins. Trends Biotechnol 17:121-127.
4. Boone C, Sommer SS, Hensel A, Bussey H. 1990. Yeast KRE genes provide evidence for a pathway of cell wall beta-glucan assembly. J Cell Biol 110:1833-1843.
5. Bordier C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem 256:1604-1607.
6. Bulawa CE. 1993. Genetics and molecular biology of chitin synthesis in fungi. Annu Rev Microbiol 47:505-534.
7. Burns N, Grimwade B, Ross-Macdonald PB, Choi EY, Finberg K, Roeder GS, Snyder M. 1994. Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes Dev 8:1087-1105.
8. Cabib E, Sburlati A, Bowers B, Silverman SJ. 1989. Chitin synthase 1, an auxiliary enzyme for chitin synthesis in Saccharomyces cerevisiae. J Cell Biol 108:1665-1672.
9. Cabib E, Drgonova J, Drgon T. 1998. Role of small G proteins in yeast cell polarization and wall biosynthesis. Annu Rev Biochem 67:307-333.
10. Cappellaro C, Mrsa V, Tanner W. 1998. New potential cell wall glucanases of Saccharomyces cerevisiae and their involvement in mating. J Bacteriol 180:5030-5037.
11. Caro LHP, Tettelin H, Vossen JH, Ram AFJ, Van Den Ende H, Klis F M. 1997. In silicio identification of glycosyl-phosphatidylinositolanchored plasma membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13:1477-1489.
12. Casanova M, Lopez-Ribot JL, Martinez J P, Sentandreu R. 1992. Characterization of cell wall proteins from yeast and mycelial cells of Candida albicans by labelling with biotin: comparison with other techniques. Infect Immun 60:4898-4906.
13. Chaffin WL, Lopez-Ribot JL, Casanova M, Gozalbo D, Martinez JP. 1998. Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev 62:130-180.
14. Choi W, Santos B, Duran A, Cabib E. 1994. Are yeast chitin synthases regulated at the transcriptional or the posttranslational level? Mol Cell Biol 14:7685-7694.
15. Cid VJ, Duran A, del Rey F, Snyder MP, Nombela C, Sanchez M. 1995. Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae. Microbiol Rev 59:345-386.
16. Cleves AE, Bankaitis VA. 1992. Secretory pathway function in Saccharomyces cerevisiae. Adv Microb Physiol 33:73-144.
17. Cleves AE, Cooper DN, Barondes SH, Kelly RB. 1996. A new pathway for protein export in Saccharomyces cerevisiae. J Cell Biol 133: 1017-1026.
18. Conzelmann A, Riezman H, Desponds C, Bron C. 1988. A major 125-kd membrane glycoprotein of Saccharomyces cerevisiae is attached to the lipid bilayer through an inositol-containing phospholipid. EMBO J 7:2233-2240.
19. Cormack B. 1998. Green fluorescent protein as a reporter of transcription and protein localization in fungi. Curr Opin Microbiol 1:406-410.
20. Cormack B, Valdivia R, Falkow S. 1996. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33-38.
21. Corthals GL, Gygi SP, Aebersold R, Patterson SD. 2000. Identification of proteins by mass spectrometry. In: Rabilloud T, editor. Protcome research: two-dimensional gel electrophoresis and identification methods. Berlin: Springer Verlag, p 197-231.
22. Cubitt AB, Heim R, Adams SR, Boyd AE, Gross LA, Tsien RY. 1995. Understanding, improving and using green fluorescent proteins. Trends Biochem Sci 20:448-455.
23. Delagrave S, Hawtin RE, Silva CM, Yang MM, Youvan DC. 1995. Red-shifted excitation mutants of the green fluorescent protein. Biotechnology 13:151-154.
24. DeMarini DJ, Adams AE, Fares H, De VC, Valle G, Chuang JS, Pringle JR. 1997. A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J Cell Biol 139:75-93.
25. De Nobel H, Lipke PN. 1994. Is there a role for GPIs in yeast cell-wall assembly? Trends Cell Biol 4:42-45.
26. De Sampaïo G, Bourdineaud JP, Lauquin GJM. 1999. A constitutive role for GPI anchors in Saccharomyces cerevisiae: cell wall targeting. Mol Microbiol 34:247-256.
27. Edwards SR, Braley R, Chaffin WL. 1999. Enolase is present in the cell wall of Saccharomyces cerevisiae. FEMS Microbiol Lett 177: 211-216.
28. FleetGH. 1991. Cell walls. In: Rose AH, Harrison JS, editors. The yeasts, vol. 4. New York: Academic Press, p 199-277.
29. Goldman RC, Sullivan PA, Zakula D, Capobianco JO. 1995. Kinetics of beta-1,3 glucan interaction at the donor and acceptor sites of the fungal glucosyltransferase encoded by the BGL2 gene. Eur J Biochem 227:372-378.
30. Hamada K, Fukuchi S, Arisawa M, Baba M, Kitada K. 1998. Screening for glycosylphosphatidylinositol (GPI)-dependent cell wall proteins hi Saccharomyces cerevisiae. Mol Gen Genet 258: 53-59.
31. Hamada K, Terashima H, Arisawa M, Yabuki N, Kitada K. 1999. Amino acid residues in the omega-minus region participate in cellular localization of yeast glycosylphosphatidylinositol-attached proteins. J Bacteriol 181:3886-3889.
32. Jarvik JW, Telmer CA. 1998. Epitope tagging. Annu Rev Genet 32: 601-618.
33. Kapteyn JC, Ram AF, Groos EM, Kollar R, Montijn RC, Van Den Ende H, Llobell A, Cabib E, Klis FM. 1997. Altered extent of cross-linking of betal,6-glucosylated mannoproteins to chitin in Saccharomyces cerevisiae mutants with reduced cell wall beta1,3-glucan content. J Bacteriol 179:6279-6284.
34. Kapteyn JC, Van Den Ende H Klis FM. 1999. The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim Biophys Acta 1426:373-383.
35. Kikuchi M, Ikehara M. 1991. Conformational features of signal sequences and folding of secretory proteins in yeasts. Trends Biotechnol 9:208-211.
36. Klein RD, Gu Q, Goddard A, Rosenthal A. 1996. Selection for genes encoding secreted proteins and receptors. Proc Natl Acad Sci USA 93:7108-7113.
37. Klis FM. 1994. Review: cell wall assembly in yeast. Yeast 10:851-869.
38. Klis FM, Ram AFJ, Montijn RC, Kapteyn JC, Caro LHP, Vossen JH, Van Berkel MAA, Brekelmans SSC, Van den Ende H. 1998. Posttranslational modifications of secretory proteins. In: Brown AJP, Tuite MF, editors. Yeast gene analysis. London: Academic Press, p 223-238.
39. Kollár R, Reinhold BB, Petrakova E, Yeh HJ, Ashwell G, Drgonova J, Kapteyn J C, Klis FM, Cabib E. 1997. Architecture of the yeast cell wall. Beta(1→6)-glucan interconnects mannoprotein, beta(1→)3-glucan, and chitin. J Biol Chem 272:17762-17775.
40. Kumar A, Cheung KH, Ross-Macdonald P, Coelho PS, Miller P, Snyder M. 2000. TRIPLES: a database of gene function in Saccharomyces cerevisiae. Nucleic Acids Res 28:81-84.
41. Lipke PN, Ovalle R. 1998. Cell wall architecture in yeast: new structure and new challenges. J Bacteriol 180:3735-3740.
42. Lo WS, Dranginis AM. 1996. FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin. J Bacteriol 178:7144-7151.
43. Lu CF, Montijn RC, Brown JL, Klis F, Kurjan J, Bussey H, Lipke PN. 1995. Glycosyl phosphatidylinositol-dependent cross-linking of alphaagglutinin and beta 1,6-glucan in the Saccharomyces cerevisiae cell wall. J Cell Biol 128:333-340.
44. Mann M, Hojrup P, Roepstorff P. 1993. Use of mass spectrometric molecular weight information to identify proteins in sequence databases. Biol Mass Spectrom 22:338-345.
45. Martinez E, Segui-Real B, Silles E, Mazon M J, Sandoval IV. 1999. The prepropeptide of vacuolar aminopeptidase I is necessary and sufficient to target the fluorescent reporter protein GFP to the vacuole of yeast by the Ccvt pathway. Mol Microbiol 33:52-62.
46. Miegeville M, Morin O. 1977. New scanning electron microscopy contribution to the study of yeast protoplasts. C R Acad Sci Hebd Seances Acad Sci D 284:1935-1938.
47. Molano J, Bowers B, Cabib E. 1980. Distribution of chitin in the yeast cell wall. An ultrastructural and chemical study. J Cell Biol 85:199-212.
48. Montijn RC, Van Rinsum J, Van Schagen FA, Klis FM. 1994. Glucomannoproteins in the cell wall of Saccharomyces cerevisiae contain a novel type of carbohydrate side chain. J Biol Chem 269:19338-19342.
49. Montijn RC, Vink E, Muller WH, Verkleij A J, Van Den Ende H, Henrissat B, Klis FM. 1999. Localization of synthesis of betal,6-glucan in Saccharomyces cerevisiae. J Bacteriol 181:7414-7420.
50. Moukadiri I, Armero J, Abad A, Sentandreu R, Zueco J. 1997. Identification of a mannoprotein present in the inner layer of the cell wall of Saccharomyces cerevisiae. J Bacteriol 179:2154-2162.
51. Mrša V, Tanner W. 1999. Role of NaOH-extractable cell wall proteins CcwSp, Ccw6p, Ccw7p and Ccw8p (members of the Pir protein family) in stability of the Saccharomyces cerevisiae cell wall. Yeast 15:813-820.
52. Mrša V, Seidl T, Gentzsch M, Tanner W. 1997. Specific labelling of cell wall proteins by biotinylation. Identification of four covalently linked O-mannosylated proteins of Saccharomyces cerevisiae. Yeast 13:1145-1154.
53. Niedenthal RK, Riles L, Johnston M, Hegemann JH. 1996. Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast 12:773-786.
54. Nielsen H, Engelbrecht J, Brunak S, Von Heijne G. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 10:1-6.
55. O'Farrell PH. 1975. High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007-4021.
56. Orlean P. 1997. Biogenesis of yeast cell wall and surface components. In: Pringle JR, Broach JR, Jones EW, editors. The molecular and cellular biology of the yeast Saccharomyces. Cell cycle and cell biology. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, p 229-362.
57. Pammer M, Briza P, Ellinger A, Schuster T, Stucka R, Feldman H, Breitenbach M. 1992. DIT101 (CDS2, CAL1), a cell-cycle-regulated yeast gene required for synthesis of chirin in cell walls and chitosan in spore walls. Yeast 8:1089-1099.
58. Pappin DJC, Hojrup P, Bleasby AJ. 1993. Rapid identification of proteins by peptide-mass fingerprinting. Curr Biol 3:327-332.
59. Pardo M, Monteoliva L, Pla J, Sanchez M, Gil C, Nombela C. 1999. Two-dimensional analysis of proteins secreted by Saccharomyces cerevisiae regenerating protoplasts: a novel approach to study the cell wall. Yeast 15:459-472.
60. Pardo M, Ward M, Bains S, Molina M, Blackstock W, Gil C, Nombela C. 2000. A proteomic approach to study Saccharomyces cerevisiae cell wall biogenesis. Electrophoresis 21 (in press).
61. Pastor FIJ, Valentín E, Herrero E, Sentandreu R. 1984. Structure of Saccharomyces cerevisiae cell wall. Biochim Biophys Acta 802:292-300.
62. Popolo L, Vai M. 1999. The Gas1 glycoprotein, a putative wall polymer cross-linker. Biochim Biophys Acta 1426:385-400.
63. Pringle JR. 1991. Staining of bud scars and other cell wall chitin with calcofluor. Methods Enzymol 194:732-5:732-735.
64. Ram AF, Van Den Ende H, Klis FM. 1998. Green fluorescent proteincell wall fusion proteins are covalently incorporated into the cell wall of Saccharomyces cerevisiae. FEMS Microbiol Lett 162:249-255.
65. Roberts RL, Bowers B, Slater ML, Cabib E. 1983. Chitin synthesis and localization in cell division cycle mutants of Saccharomyces cerevisiae. Mol Cell Biol 3:922-930.
66. Rodríguez-Peña JM, Cid VJ, Arroyo J, Nombela C. 2000. A novel family of cell wall related proteins regulated differently during the yeast life cycle. Mol Cell Biol 20:3245-3255.
67. Ross-Macdonald P, Coelho PS, Roemer T, Agarwal S, Kumar A, Jansen R, Cheung KH, Sheehan A, Symoniatis D, Umansky L, Heidtman M, Nelson FK, Iwasaki H, Hager K, Gerstein M, Miller P, Roeder GS, Snyder M. 1999. Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature 402:413-418.
68. Santos B, Snyder M. 1997. Targeting of chitin synthase 3 to polarized growth sites in yeast requires Chs5p and Myo2p. J Cell Biol 136: 95-110.
69. Shahinian S, Bussey H. 2000. Beta-1,6-glucan synthesis in Saccharomyces cerevisiae. Mol Microbiol 35:477-489.
70. Shaw JA, Mol PC, Bowers B, Silverman SJ, Valdivieso MH, Daran A, Cabib E. 1991. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J Cell Biol 114:111-123.
71. Shevchenko A, Jensen ON, Podtelejnikov AV, Sagliocco F, Wilm M, Vorm O, Mortensen P, Boucherie H, Mann M. 1996a. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci USA 93:14440-14445.
72. Shevchenko A, Wilm M, Vorm O, Mann M. 1996b. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68:850-858.
73. Shibata N, Mizugami K, Takano K, Suzuki S. 1983. Isolation of mannan-protein complexes from viable cells of Saccharomyces cerevisiae X2180-1A wild type and Saccharomyces cerevisiae X2180-1 A-5 mutant strains by the action of Zymolyase-60000. J Bacteriol 156:552-558.
74. Smits GJ, Kapteyn JC, Van Den Ende H, Klis FM. 1999. Cell wall dynamics in yeast. Curr Op Microbiol 2:348-352.
75. Toh-E A, Yasunaga S, Nisogi H, Tanaka K, Oguchi T, Matsui Y. 1993. Three yeast genes, PIR1, PIR2 and PIR3, containing internal tandem repeats, are related to each other, and PIR1 and PIR2 are required for tolerance to heat shock. Yeast 9:481-494.
76. Trilla JA, Duran A, Roncero C. 1999. Chs7p, a new protein involved in the control of protein export from the endoplasmic reticulum that is specifically engaged in the regulation of chitin synthesis in Saccharomyces cerevisiae. J Cell Biol 145:1153-1163.
77. Tsien RY. 1998. The green fluorescent protein. Annu Rev Biochem 67:509-44:509-544.
78. Udenfriend S, Kodukula K. 1995. How glycosylphosphatidylinositol-anchored membrane proteins are made. Annu Rev Biochem 64:563-591.
79. Valdivieso MH, Mol PC, Shaw JA, Cabib E, Duran A. 1991. CAL1, a gene required for activity of chitin synthase 3 in Saccharomyces cerevisiae. J Cell Biol 114:101-109.
80. Valentin E, Herrero E, Pastor JFI, Sentandreu R. 1984. Solubilization and analysis of mannoprotein molecules from cell wall of Saccharomyces cerevisiae. Arch Microbiol 130:1419-1428.
81. Van Berkel MA, Caro LH, Montijn RC, Klis FM. 1994. Glucosylation of chimeric proteins in the cell wall of Saccharomyces cerevisiae. FEBS Lett 349:135-138.
82. Van Der Vaart JM, Te Biesebeke R, Chapman JW, Klis FM, Verrips CT. 1996. The beta-1, 6-glucan containing side-chain of cell wall proteins of Saccharomyces cerevisiae is bound to the glycan core of the GPI moiety. FEMS Microbiol Lett 145:401-407.
83. Van Risum J, Klis FM, Van Den Ende H. 1991. Cell wall glucomannoproteins of Saccharomyces cerevisiae mnn9. Yeast 7:717-726.
84. Vossen JH, Muller WH, Lipke PN, Klis FM. 1997. Restrictive glycosylphosphatidylinositol anchor synthesis in cwh6/gpi3 yeast cells causes aberrant biogenesis of cell wall proteins. J Bacteriol 179: 2202-2209.
85. Wilkins MR, Williams KL, Appel RD, Hochstrasser DF. 1997. Proteome research: new frontiers in functional genomics. Berlin: Springer-Verlag.
86. Yates JRIII, Speicher S, Griffin PR, Hunkapiller T. 1993. Peptide mass maps: a highlyinformative approach to protein identification. Anal Biochem 214:397-408.
87. Ziman M, Chuang JS, Tsung M, Hamamoto S, Schekman R. 1998. Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae. Mol Biol Cell 9:1565-1576.