Cell wall construction in Saccharomyces cerevisiae

In this review, we discuss new insights in cell wall architecture and cell wall construction in the ascomycetous yeast Saccharomyces cerevisiae. Transcriptional profiling studies combined with biochemical work have provided ample evidence that the cell wall is a highly adaptable organelle. In particular, the protein population that is anchored to the stress‐bearing polysaccharides of the cell wall, and forms the interface with the outside world, is highly diverse. This diversity is believed to play an important role in adaptation of the cell to environmental conditions, in growth mode and in survival. Cell wall construction is tightly controlled and strictly coordinated with progression of the cell cycle. This is reflected in the usage of specific cell wall proteins during consecutive phases of the cell cycle and in the recent discovery of a cell wall integrity checkpoint. When the cell is challenged with stress conditions that affect the cell wall, a specific transcriptional response is observed that includes the general stress response, the cell wall integrity pathway and the calcineurin pathway. This salvage mechanism includes increased expression of putative cell wall assemblases and some potential cross‐linking cell wall proteins, and crucial changes in cell wall architecture. We discuss some more enzymes involved in cell wall construction and also potential inhibitors of these enzymes. Finally, we use both biochemical and genomic data to infer that the architectural principles used by S. cerevisiae to build its cell wall are also used by many other ascomycetous yeasts and also by some mycelial ascomycetous fungi. Copyright © 2006 John Wiley & Sons, Ltd.

[1]  J. Hoheisel,et al.  Genome-wide Analysis of the Response to Cell Wall Mutations in the Yeast Saccharomyces cerevisiae* , 2003, Journal of Biological Chemistry.

[2]  H. Kitagaki,et al.  A Temperature-Sensitive dcw1 Mutant of Saccharomyces cerevisiae Is Cell Cycle Arrested with Small Buds Which Have Aberrant Cell Walls , 2004, Eukaryotic Cell.

[3]  M. Hayashibe,et al.  Polysaccharide composition of the cell wall of baker's yeast with special reference to cell walls obtained from large- and small-sized cells , 1976 .

[4]  Stanley Brul,et al.  Role of cell cycle-regulated expression in the localized incorporation of cell wall proteins in yeast. , 2006, Molecular biology of the cell.

[5]  F. Klis,et al.  The glucanase‐soluble mannoproteins limit cell wall porosity in Saccharomyces cerevisiae , 1990, Yeast.

[6]  A. Tinkelenberg,et al.  Transcriptional Profiling Identifies Two Members of the ATP-binding Cassette Transporter Superfamily Required for Sterol Uptake in Yeast* , 2002, The Journal of Biological Chemistry.

[7]  D. E. Levin,et al.  Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect , 1992, The Journal of cell biology.

[8]  D. Manners,et al.  Isolation and composition of an alkali-soluble glucan from the cell walls of Saccharomyces cerevisiae. , 1976, Journal of general microbiology.

[9]  K. Hellingwerf,et al.  Proteomic Analysis of Candida albicans Cell Walls Reveals Covalently Bound Carbohydrate-Active Enzymes and Adhesins , 2004, Eukaryotic Cell.

[10]  M. Whiteway,et al.  Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. , 2003, Molecular biology of the cell.

[11]  F. Klis,et al.  Green fluorescent protein-cell wall fusion proteins are covalently incorporated into the cell wall of Saccharomyces cerevisiae. , 1998, FEMS microbiology letters.

[12]  Stanley Brul,et al.  Characterization of the transcriptional response to cell wall stress in Saccharomyces cerevisiae , 2004, Yeast.

[13]  M. Vai,et al.  The Gas1 glycoprotein, a putative wall polymer cross-linker. , 1999, Biochimica et biophysica acta.

[14]  E. Cabib.  The septation apparatus, a chitin-requiring machine in budding yeast. , 2004, Archives of biochemistry and biophysics.

[15]  K. Takeo,et al.  Quantitative three-dimensional structural analysis of Exophiala dermatitidis yeast cells by freeze-substitution and serial ultrathin sectioning. , 2003, Journal of electron microscopy.

[16]  F. Klis,et al.  Increased Cell Wall Porosity in Saccharomyces cerevisiae after Treatment with Dithiothreitol or EDTA , 1989 .

[17]  K. Hellingwerf,et al.  Genome‐wide identification of fungal GPI proteins , 2003, Yeast.

[18]  S. Silverman,et al.  The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle , 1991, The Journal of cell biology.

[19]  H. Shimoi,et al.  Structure of the glucan-binding sugar chain of Tip1p, a cell wall protein of Saccharomyces cerevisiae. , 1999, Biochimica et biophysica acta.

[20]  W. Tanner,et al.  New Potential Cell Wall Glucanases ofSaccharomyces cerevisiae and Their Involvement in Mating , 1998, Journal of bacteriology.

[21]  K. Davies,et al.  Regulatory mechanisms controlling expression of the DAN/TIR mannoprotein genes during anaerobic remodeling of the cell wall in Saccharomyces cerevisiae. , 2001, Genetics.

[22]  F. Klis,et al.  Characterisation of CwpA, a putative glycosylphosphatidylinositol-anchored cell wall mannoprotein in the filamentous fungus Aspergillus niger. , 2005, Fungal genetics and biology : FG & B.

[23]  F. Reggiori,et al.  Deletion of GPI7, a Yeast Gene Required for Addition of a Side Chain to the Glycosylphosphatidylinositol (GPI) Core Structure, Affects GPI Protein Transport, Remodeling, and Cell Wall Integrity* , 1999, The Journal of Biological Chemistry.

[24]  E. Cabib,et al.  Saccharomyces cerevisiae mannoproteins form an external cell wall layer that determines wall porosity , 1984, Journal of bacteriology.

[25]  M. Molina,et al.  Protein localisation approaches for understanding yeast cell wall biogenesis , 2000, Microscopy research and technique.

[26]  P. Mol,et al.  Linkages between glucosaminoglycan and glucan determine alkali-insolubility of the glucan in walls of Saccharomyces cerevisiae , 1987 .

[27]  David E. Levin,et al.  Cell Wall Integrity Signaling in Saccharomyces cerevisiae , 2005, Microbiology and Molecular Biology Reviews.

[28]  E. Dodou,et al.  The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-activated protein kinase pathway , 1997, Molecular and cellular biology.

[29]  F. Klis,et al.  GPI7 affects cell-wall protein anchorage in Saccharomyces cerevisiae and Candida albicans. , 2002, Microbiology.

[30]  Yudong D. He,et al.  Functional Discovery via a Compendium of Expression Profiles , 2000, Cell.

[31]  D. Krysan,et al.  Yapsins Are a Family of Aspartyl Proteases Required for Cell Wall Integrity in Saccharomyces cerevisiae , 2005, Eukaryotic Cell.

[32]  F. Klis,et al.  The linkage of (1–3)‐β‐glucan to chitin during cell wall assembly in Saccharomyces cerevisiae , 1994, Yeast.

[33]  J. Kijne,et al.  A rapid and selective assay for measuring cell surface hydrophobicity of brewer's yeast cells , 1996, Yeast.

[34]  U. Jung,et al.  Genome‐wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway , 1999, Molecular microbiology.

[35]  F. Klis,et al.  Cell wall perturbation in yeast results in dual phosphorylation of the Slt2/Mpk1 MAP kinase and in an Slt2-mediated increase in FKS2-lacZ expression, glucanase resistance and thermotolerance. , 2000, Microbiology.

[36]  B. Haarer,et al.  Fluorescence microscopy methods for yeast. , 1989, Methods in cell biology.

[37]  Thierry Ferreira,et al.  SUT1-promoted sterol uptake involves the ABC transporter Aus1 and the mannoprotein Dan1 whose synergistic action is sufficient for this process. , 2004, The Biochemical journal.

[38]  K. Hamada,et al.  Up-regulation of genes encoding glycosylphosphatidylinositol (GPI)-attached proteins in response to cell wall damage caused by disruption of FKS1 in Saccharomyces cerevisiae , 2000, Molecular and General Genetics MGG.

[39]  D Botstein,et al.  Three Cell Wall Mannoproteins Facilitate the Uptake of Iron in Saccharomyces cerevisiae * , 2001, The Journal of Biological Chemistry.

[40]  P. Robbins,et al.  Architecture of the yeast cell wall. The linkage between chitin and beta(1-->3)-glucan. , 1995, The Journal of biological chemistry.

[41]  E. Cabib,et al.  Synthase III-dependent Chitin Is Bound to Different Acceptors Depending on Location on the Cell Wall of Budding Yeast*♦ , 2005, Journal of Biological Chemistry.

[42]  J. C. Kapteyn,et al.  Identification and characterization of a major building block in the cell wall of Saccharomyces cerevisiae. , 1997, Biochemical Society transactions.

[43]  F. M. Yeong.  Severing all ties between mother and daughter: cell separation in budding yeast , 2005, Molecular microbiology.

[44]  P. Orlean.  3 Biogenesis of Yeast Wall and Surface Components , 1997 .

[45]  Michael Ruogu Zhang,et al.  Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. , 1998, Molecular biology of the cell.

[46]  H. Kitagaki,et al.  Sed1p Is a Major Cell Wall Protein ofSaccharomyces cerevisiae in the Stationary Phase and Is Involved in Lytic Enzyme Resistance , 1998, Journal of bacteriology.

[47]  K. Hellingwerf,et al.  Dynamics of cell wall structure in Saccharomyces cerevisiae. , 2002, FEMS microbiology reviews.

[48]  P. Barré,et al.  Saccharomyces cerevisiae PAU genes are induced by anaerobiosis , 2000, Molecular microbiology.

[49]  R. Rachel,et al.  Mating type‐specific cell‐cell recognition of Saccharomyces cerevisiae: cell wall attachment and active sites of a‐ and alpha‐agglutinin. , 1994, The EMBO journal.

[50]  V. Baladrón,et al.  Eng1p, an Endo-1,3-β-Glucanase Localized at the Daughter Side of the Septum, Is Involved in Cell Separation in Saccharomyces cerevisiae , 2002, Eukaryotic Cell.

[51]  S. Brul,et al.  The incorporation of mannoproteins in the cell wall of S. cerevisiae and filamentous Ascomycetes , 1997, Antonie van Leeuwenhoek.

[52]  P. Lipke,et al.  Cell surface anchorage and ligand-binding domains of the Saccharomyces cerevisiae cell adhesion protein alpha-agglutinin, a member of the immunoglobulin superfamily , 1993, Molecular and cellular biology.

[53]  J. Latgé,et al.  Identification of the catalytic residues of the first family of beta(1-3)glucanosyltransferases identified in fungi. , 2000 .

[54]  J. Bähler.  Cell-cycle control of gene expression in budding and fission yeast. , 2005, Annual review of genetics.

[55]  S. Young,et al.  Sodium hydroxide-induced conformational change in schizophyllan detected by the fluorescence dye, aniline blue , 1998 .

[56]  C. Nombela,et al.  Mechanisms for targeting of the Saccharomyces cerevisiae GPI-anchored cell wall protein Crh2p to polarised growth sites. , 2002, Journal of cell science.

[57]  H. Bussey,et al.  An in vitro assay for (1 → 6)‐β‐D‐glucan synthesis in Saccharomyces cerevisiae , 2004, Yeast.

[58]  F. Klis,et al.  beta-Glucosylated proteins in the cell wall of the black yeast Exophiala (Wangiella) dermatitidis. , 1997, Microbiology.

[59]  M. Tokunaga,et al.  Ultrastructure of outermost layer of cell wall in Candida albicans observed by rapid-freezing technique. , 1986, Journal of electron microscopy.

[60]  Bernard Henrissat,et al.  Localization of Synthesis of β1,6-Glucan inSaccharomyces cerevisiae , 1999, Journal of bacteriology.

[61]  U. Jung,et al.  Regulation of the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP kinase , 2002, Molecular microbiology.

[62]  R. Kuroki,et al.  Region of Flo1 Proteins Responsible for Sugar Recognition , 1998, Journal of bacteriology.

[63]  J. Hoheisel,et al.  Sed1p and Srl1p are required to compensate for cell wall instability in Saccharomyces cerevisiae mutants defective in multiple GPI‐anchored mannoproteins , 2004, Molecular microbiology.

[64]  F. Klis,et al.  Features and functions of covalently linked proteins in fungal cell walls. , 2005, Fungal genetics and biology : FG & B.

[65]  H. Kitagaki,et al.  Two homologous genes, DCW1 (YKL046c) and DFG5, are essential for cell growth and encode glycosylphosphatidylinositol (GPI)‐anchored membrane proteins required for cell wall biogenesis in Saccharomyces cerevisiae , 2002, Molecular microbiology.

[66]  H. Yoshimoto,et al.  Analysis of the genes activated by the FLO8 gene in Saccharomyces cerevisiae , 1999, Current Genetics.

[67]  Michelle E. Kim,et al.  Roles of Candida albicans Dfg5p and Dcw1p Cell Surface Proteins in Growth and Hypha Formation , 2003, Eukaryotic Cell.

[68]  R. Bressan,et al.  Overexpression of a cell wall glycoprotein in Fusarium oxysporum increases virulence and resistance to a plant PR-5 protein. , 2003, The Plant journal : for cell and molecular biology.

[69]  J. C. Kapteyn,et al.  Cell wall dynamics in yeast. , 1999, Current opinion in microbiology.

[70]  M. Ueda,et al.  Yeast cell-surface display—applications of molecular display , 2004, Applied Microbiology and Biotechnology.

[71]  Javier Arroyo,et al.  The Global Transcriptional Response to Transient Cell Wall Damage in Saccharomyces cerevisiae and Its Regulation by the Cell Integrity Signaling Pathway* , 2004, Journal of Biological Chemistry.

[72]  J. McCaffery,et al.  Modular domain structure in the Candida glabrata adhesin Epa1p, a β1,6 glucan‐cross‐linked cell wall protein , 2002, Molecular microbiology.

[73]  P. Lipke,et al.  Cell Wall Architecture in Yeast: New Structure and New Challenges , 1998, Journal of bacteriology.

[74]  M. Osumi.  The ultrastructure of yeast: cell wall structure and formation. , 1998, Micron.

[75]  H. Kitagaki,et al.  Identification and analysis of a static culture-specific cell wall protein, Tir1p/Srp1p in Saccharomyces cerevisiae. , 1997, European journal of biochemistry.

[76]  F. Klis,et al.  Transcription of multiple cell wall protein-encoding genes in Saccharomyces cerevisiae is differentially regulated during the cell cycle. , 1998, FEMS microbiology letters.

[77]  D. Manners,et al.  The structure of a β-(1→3)-d-glucan from yeast cell walls , 1973 .

[78]  Nicola J. Rinaldi,et al.  Transcriptional regulatory code of a eukaryotic genome , 2004, Nature.

[79]  Javier Arroyo,et al.  A Novel Family of Cell Wall-Related Proteins Regulated Differently during the Yeast Life Cycle , 2000, Molecular and Cellular Biology.

[80]  K. Davies,et al.  Induction and repression of DAN1 and the family of anaerobic mannoprotein genes in Saccharomyces cerevisiae occurs through a complex array of regulatory sites. , 2001, Nucleic acids research.

[81]  K. J. Clarke,et al.  Effect of osmotic stress on the ultrastructure and viability of the yeast Saccharomyces cerevisiae. , 1986, Journal of general microbiology.

[82]  L. Johnston,et al.  Coordinated regulation of gene expression by the cell cycle transcription factor Swi4 and the protein kinase C MAP kinase pathway for yeast cell integrity. , 1996, The EMBO journal.

[83]  J. Zueco,et al.  Characterization of a glycosylphosphatidylinositol-bound cell-wall protein (GPI-CWP) in Yarrowia lipolytica. , 2004, Microbiology.

[84]  X. L. Zhou,et al.  A mechanosensitive ion channel in the yeast plasma membrane. , 1988, Science.

[85]  C. Selitrennikoff,et al.  Neurospora crassa FKS Protein Binds to the (1,3)β-Glucan Synthase Substrate, UDP-Glucose , 2003, Current Microbiology.

[86]  H. Bussey,et al.  Cell Wall Assembly in Saccharomyces cerevisiae , 2006, Microbiology and Molecular Biology Reviews.

[87]  H. Bussey,et al.  β‐1,6‐Glucan synthesis in Saccharomyces cerevisiae , 2000 .

[88]  B. Berk,et al.  Flow Activates ERK1/2 and Endothelial Nitric Oxide Synthase via a Pathway Involving PECAM1, SHP2, and Tie2* , 2005, Journal of Biological Chemistry.

[89]  S. Blad,et al.  Low external pH induces HOG1‐dependent changes in the organization of the Saccharomyces cerevisiae cell wall , 2001, Molecular microbiology.

[90]  Daniel J. Vis,et al.  T-profiler: scoring the activity of predefined groups of genes using gene expression data , 2005, Nucleic Acids Res..

[91]  C. Nombela,et al.  The GPI-anchored protein CaEcm33p is required for cell wall integrity, morphogenesis and virulence in Candida albicans. , 2004, Microbiology.

[92]  J. A. Barnett,et al.  Passage of molecules through yeast cell walls: A brief essay‐review , 1991, Yeast.

[93]  M. Zupancic,et al.  A yeast by any other name: Candida glabrata and its interaction with the host. , 2005, Current opinion in microbiology.

[94]  K. Hellingwerf,et al.  Molecular organization of the cell wall of Candida albicans. , 2001, Medical mycology.

[95]  H. Bussey,et al.  The KNH1 gene of Saccharomyces cerevisiae is a functional homolog of KRE9 , 1996, Yeast.

[96]  I. Imhof,et al.  Glycosylphosphatidylinositol (GPI) Proteins of Saccharomyces cerevisiae Contain Ethanolamine Phosphate Groups on the α1,4-linked Mannose of the GPI Anchor* , 2004, Journal of Biological Chemistry.

[97]  F. Klis,et al.  Targeting of a heterologous protein to the cell wall of Saccharomyces cerevisiae , 1993, Yeast.

[98]  W. Tanner,et al.  Role of NaOH‐extractable cell wall proteins Ccw5p, Ccw6p, Ccw7p and Ccw8p (members of the Pir protein family) in stability of the Saccharomyces cerevisiae cell wall , 1999, Yeast.

[99]  Ismaïl Moukadiri,et al.  Identification of Two Mannoproteins Released from Cell Walls of a Saccharomyces cerevisiae mnn1 mnn9 Double Mutant by Reducing Agents , 1999, Journal of bacteriology.

[100]  Pedro M. Coutinho,et al.  Carbohydrate-active enzymes : an integrated database approach , 1999 .

[101]  K. Iwashita,et al.  The AWA1 Gene Is Required for the Foam-Forming Phenotype and Cell Surface Hydrophobicity of Sake Yeast , 2002, Applied and Environmental Microbiology.

[102]  S. Barondes,et al.  A new pathway for protein export in Saccharomyces cerevisiae , 1996, The Journal of cell biology.

[103]  K. Hauser,et al.  Saccharomyces cerevisiae a‐ and alpha‐agglutinin: characterization of their molecular interaction. , 1991, The EMBO journal.

[104]  A. Verkleij,et al.  The cell wall architecture of Candida albicans wild‐type cells and cell wall‐defective mutants , 2000, Molecular microbiology.

[105]  J. Douwes,et al.  Loss of the Plasma Membrane-Bound Protein Gas1p inSaccharomyces cerevisiae Results in the Release of β1,3-Glucan into the Medium and Induces a Compensation Mechanism To Ensure Cell Wall Integrity , 1998, Journal of bacteriology.

[106]  Y. Noda,et al.  A Novel Endoplasmic Reticulum Membrane Protein Rcr1 Regulates Chitin Deposition in the Cell Wall of Saccharomyces cerevisiae* , 2005, Journal of Biological Chemistry.

[107]  R. Sentandreu,et al.  Functional analysis of the cysteine residues and the repetitive sequence of Saccharomyces cerevisiae Pir4/Cis3: the repetitive sequence is needed for binding to the cell wall β‐1,3‐glucan , 2003, Yeast.

[108]  A. Conzelmann,et al.  YLL031c Belongs to a Novel Family of Membrane Proteins Involved in the Transfer of Ethanolaminephosphate onto the Core Structure of Glycosylphosphatidylinositol Anchors in Yeast* , 2000, The Journal of Biological Chemistry.

[109]  J. Heinisch.  Baker's yeast as a tool for the development of antifungal kinase inhibitors--targeting protein kinase C and the cell integrity pathway. , 2005, Biochimica et biophysica acta.

[110]  Ronald W. Davis,et al.  Genome-Wide Transcriptional Analysis of Aerobic and Anaerobic Chemostat Cultures of Saccharomyces cerevisiae , 1999, Journal of bacteriology.

[111]  H. Tettelin,et al.  In silicio identification of glycosyl‐phosphatidylinositol‐anchored plasma‐membrane and cell wall proteins of Saccharomyces cerevisiae , 1997, Yeast.

[112]  James C Liao,et al.  Inferring yeast cell cycle regulators and interactions using transcription factor activities , 2005, BMC Genomics.

[113]  G. Fink,et al.  Bakers' yeast, a model for fungal biofilm formation. , 2001, Science.

[114]  J. C. Kapteyn,et al.  Altered extent of cross-linking of beta1,6-glucosylated mannoproteins to chitin in Saccharomyces cerevisiae mutants with reduced cell wall beta1,3-glucan content , 1997, Journal of bacteriology.

[115]  A. Svoboda,et al.  Sporothrix schenckii — a freeze‐fracture study , 1990, Journal of basic microbiology.

[116]  K. Hamada,et al.  Proteins Glycosylphosphatidylinositol-Attached of Yeast Region Participate in Cellular Localization-Minus ω Amino Acid Residues in the , 1999 .

[117]  P. Gerhardt,et al.  Porosity of the Yeast Cell Wall and Membrane , 1974, Journal of bacteriology.

[118]  David J Adams,et al.  Fungal cell wall chitinases and glucanases. , 2004, Microbiology.

[119]  M. Cyert.  Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. , 2003, Biochemical and biophysical research communications.

[120]  H. Bussey,et al.  The Candida albicans KRE9 gene is required for cell wall beta-1, 6-glucan synthesis and is essential for growth on glucose. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[121]  T. Hughes,et al.  Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles. , 2000, Science.

[122]  J. Latgé,et al.  Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. , 2000, The Journal of biological chemistry.

[123]  Shinichi Morishita,et al.  Data mining tools for the Saccharomyces cerevisiae morphological database , 2005, Nucleic Acids Res..

[124]  Thierry Fontaine,et al.  Glycosylphosphatidylinositol-anchored Glucanosyltransferases Play an Active Role in the Biosynthesis of the Fungal Cell Wall* , 2000, The Journal of Biological Chemistry.

[125]  H. Bussey,et al.  The yeast KRE9 gene encodes an O glycoprotein involved in cell surface beta-glucan assembly , 1993, Molecular and cellular biology.

[126]  P. Bonfante,et al.  Increase in chitin as an essential response to defects in assembly of cell wall polymers in the ggp1delta mutant of Saccharomyces cerevisiae , 1997, Journal of bacteriology.

[127]  F. Klis,et al.  Glucosylation of fungal cell wall proteins as a potential target for novel antifungal agents , 1996 .

[128]  H. Shimoi,et al.  Molecular cloning of CWP1: a gene encoding a Saccharomyces cerevisiae cell wall protein solubilized with Rarobacter faecitabidus protease I. , 1995, Journal of biochemistry.

[129]  J. C. Kapteyn,et al.  The contribution of the O‐glycosylated protein Pir2p/Hsp150 to the construction of the yeast cell wall in wild‐type cells and β1,6‐glucan‐deficient mutants , 1999, Molecular microbiology.

[130]  F. Klis,et al.  Glucosylation of chimeric proteins in the cell wall of Saccharomyces cerevisiae , 1994, FEBS letters.

[131]  J. Zueco,et al.  Characterization of a disulphide‐bound Pir‐cell wall protein (Pir‐CWP) of Yarrowia lipolytica , 2003, Yeast.

[132]  F. Klis,et al.  Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood , 2005, Molecular microbiology.

[133]  S. Reed,et al.  MCD4 encodes a conserved endoplasmic reticulum membrane protein essential for glycosylphosphatidylinositol anchor synthesis in yeast. , 1999, Molecular biology of the cell.

[134]  J. Latgé,et al.  Structures of the glycosylphosphatidylinositol membrane anchors from Aspergillus fumigatus membrane proteins. , 2003, Glycobiology.

[135]  Sapna Mehta,et al.  Reciprocal Regulation of Anaerobic and Aerobic Cell Wall Mannoprotein Gene Expression in Saccharomyces cerevisiae , 2001, Journal of bacteriology.

[136]  F. Klis,et al.  The Aspergillus niger MADS‐box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress , 2005, Molecular microbiology.

[137]  F. Klis,et al.  A new strategy for inhibition of the spoilage yeasts Saccharomyces cerevisiae and Zygosaccharomyces bailii based on combination of a membrane-active peptide with an oligosaccharide that leads to an impaired glycosylphosphatidylinositol (GPI)-dependent yeast wall protein layer. , 2001, FEMS yeast research.

[138]  P. Robbins,et al.  Architecture of the Yeast Cell Wall , 1995, The Journal of Biological Chemistry.

[139]  Y. Ohya,et al.  Dynactin is involved in a checkpoint to monitor cell wall synthesis in Saccharomyces cerevisiae , 2004, Nature Cell Biology.

[140]  D. Botstein,et al.  Genomic expression programs in the response of yeast cells to environmental changes. , 2000, Molecular biology of the cell.

[141]  C. D. de Koster,et al.  Systematic identification in silico of covalently bound cell wall proteins and analysis of protein-polysaccharide linkages of the human pathogen Candida glabrata. , 2004, Microbiology.

[142]  Andre Boorsma,et al.  Transcriptional Response of Saccharomyces cerevisiae to the Plasma Membrane-Perturbing Compound Chitosan , 2005, Eukaryotic Cell.

[143]  F. Klis,et al.  A Genomic Approach for the Identification and Classification of Genes Involved in Cell Wall Formation and its Regulation in Saccharomyces Cerevisiae , 2001, Comparative and functional genomics.

[144]  Y. Jigami,et al.  GPI7 Involved in Glycosylphosphatidylinositol Biosynthesis Is Essential for Yeast Cell Separation* , 2004, Journal of Biological Chemistry.

[145]  J. Berman,et al.  Candida albicans hyphae have a Spitzenkörper that is distinct from the polarisome found in yeast and pseudohyphae , 2005, Journal of Cell Science.

[146]  R. Schekman,et al.  Export of major cell surface proteins is blocked in yeast secretory mutants , 1983, The Journal of cell biology.

[147]  J. Pronk,et al.  Two-dimensional Transcriptome Analysis in Chemostat Cultures , 2005, Journal of Biological Chemistry.

[148]  B. Reinhold,et al.  Architecture of the Yeast Cell Wall , 1997, The Journal of Biological Chemistry.

[149]  V. Lundblad,et al.  Yeast , 2008 .

[150]  F. Klis,et al.  Identification of two cell cycle regulated genes affecting the β1,3‐glucan content of cell walls in Saccharomyces cerevisiae , 1995, FEBS letters.

[151]  H. Moor,et al.  FINE STRUCTURE IN FROZEN-ETCHED YEAST CELLS , 1963, The Journal of cell biology.

[152]  J. François,et al.  A study of the yeast cell wall composition and structure in response to growth conditions and mode of cultivation , 2003, Letters in applied microbiology.

[153]  Stanley Brul,et al.  Activation of the Protein Kinase C1 Pathway upon Continuous Heat Stress in Saccharomyces cerevisiae Is Triggered by an Intracellular Increase in Osmolarity due to Trehalose Accumulation , 2005, Applied and Environmental Microbiology.

[154]  W. E. Scott,et al.  Polysaccharide conformation. Part VI. Computer model-building for linear and branched pyranoglycans. Correlations with biological function. Preliminary assessment of inter-residue forces in aqueous solution. Further interpretation of optical rotation in terms of chain conformation , 1971 .

[155]  D. Manners,et al.  The structure of a beta-(1 leads to 3)-D-glucan from yeast cell walls. , 1973, The Biochemical journal.

[156]  J. Latgé,et al.  Glycosylphosphatidylinositol-anchored Fungal Polysaccharide in Aspergillus fumigatus* , 2005, Journal of Biological Chemistry.

[157]  J. Douwes,et al.  Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked beta-1,3-/beta-1,6-glucan heteropolymer. , 1996, Glycobiology.

[158]  U. Jung,et al.  Yeast Rpi1 Is a Putative Transcriptional Regulator That Contributes to Preparation for Stationary Phase , 2002, Eukaryotic Cell.

[159]  M. Gentzsch,et al.  Specific Labelling of Cell Wall Proteins by Biotinylation. Identification of Four Covalently Linked O‐mannosylated Proteins of Saccharomyces cerevisiae , 1997, Yeast.

[160]  E. Cabib,et al.  The Yeast Cell Wall and Septum as Paradigms of Cell Growth and Morphogenesis* , 2001, The Journal of Biological Chemistry.

[161]  J. Pérez-Ortín,et al.  Stress response and expression patterns in wine fermentations of yeast genes induced at the diauxic shift , 2000, Yeast.

[162]  F. Klebl,et al.  Molecular cloning of a cell wall exo-beta-1,3-glucanase from Saccharomyces cerevisiae , 1989, Journal of bacteriology.

[163]  M. Muzard,et al.  Iminosugars as glycosyltransferase inhibitors: synthesis of polyhydroxypyrrolidines and their evaluation on chitin synthase activity. , 2005, European journal of medicinal chemistry.

[164]  C. Mazzoni,et al.  The SLT2(MPK1) MAP kinase is activated during periods of polarized cell growth in yeast. , 1996, The EMBO journal.

[165]  C. Nombela,et al.  PST1 and ECM33 encode two yeast cell surface GPI proteins important for cell wall integrity. , 2004, Microbiology.

[166]  C. D. de Koster,et al.  Comprehensive Proteomic Analysis of Saccharomyces cerevisiae Cell Walls , 2005, Journal of Biological Chemistry.

[167]  Fran Lewitter,et al.  Intragenic tandem repeats generate functional variability , 2005, Nature Genetics.

[168]  D. A. Yphantis,et al.  Effect of Some Proteins on the Yeast Cell Membrane , 1967, Journal of bacteriology.

[169]  R C Montijn,et al.  Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked beta-1,3-/beta-1,6-glucan heteropolymer. , 1996, Glycobiology.

[170]  P. Orlean,et al.  Glycosylphosphatidylinositol biosynthesis defects in Gpi11p- and Gpi13p-deficient yeast suggest a branched pathway and implicate gpi13p in phosphoethanolamine transfer to the third mannose. , 2000, Molecular biology of the cell.

[171]  J. Pronk,et al.  The Genome-wide Transcriptional Responses of Saccharomyces cerevisiae Grown on Glucose in Aerobic Chemostat Cultures Limited for Carbon, Nitrogen, Phosphorus, or Sulfur* , 2003, The Journal of Biological Chemistry.