Chapter 14 : The Cell Wall: Glycoproteins, Remodeling, and Regulation

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

The Cell Wall: Glycoproteins, Remodeling, and Regulation, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817176/9781555815394_Chap14-1.gif /docserver/preview/fulltext/10.1128/9781555817176/9781555815394_Chap14-2.gif


This chapter provides an update on cell wall structure and, in particular, cell wall glycoproteins (CWPs), cell wall remodeling, and cell wall regulation. Proteins associated with glycolysis, like enolase and alcohol dehydrogenase, are well-known cytoplasmic proteins but have also been identified at the cell surface; this dual location has led them to be termed “moonlighting” proteins. Glycosylphosphatidylinositol (GPI) anchoring is encountered in every eukaryotic cell, including unicellular yeast cells, several parasites, and highly specialized mammalian cells. Analyses of the and genomes to identify intragenic tandem repeats found a significant enrichment of putative CWPs. Mutants of GAS genes in , , , and had defects in cell wall organization and morphogenesis. Single and double disruption of the Gas orthologues and showed that the enzymatic activity was required for morphogenesis and virulence. The poor resolution of fungal glycoproteins through sodium dodecyl sulfate (SDS)-polyacrylamide gel electrophoresis has prompted alternative nongel technologies to study the complement of proteins in the cell wall. Transcript profiling of cells from in vivo models has identified a number of cell wall-associated genes whose expression is altered compared to those in in vitro-grown cells. As well as being exposed to different stimuli that are independently known to alter expression of cell wall-related genes, the invading fungus will also be under attack by the host’s enzymes and immune cells.

Citation: Munro C, Richard M. 2012. The Cell Wall: Glycoproteins, Remodeling, and Regulation, p 197-223. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch14

Key Concept Ranking

Cell Wall Proteins
Cell Wall Biosynthesis
Sodium Dodecyl Sulfate
Transmission Electron Microscopy
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Signaling pathways that regulate cell wall biogenesis and remodeling. The cross-section of a yeast cell prepared by high-pressure freeze substitution transmission electron microscopy demonstrates the outer fibrillar cell surface composed of highly glycosylated glycoproteins surrounding an electron transparent polysaccharide-rich matrix made mainly of glucan with some chitin. In , several integral membrane proteins with glycosylated extracellular domains (Wsc family, Mid2, Mtl1, Msb2, Hkr1, Sho1, and Sln1) act as sensors that respond to changes in cell wall integrity and activate downstream signaling pathways. Msb2, Hkr1, Sln1, and Sho1 also act as osmosensors. In , Msb2 and Sho1 signal to the CEK pathway and Sln1 signals to the HOG pathway. In , the Chk1 histidine kinase and the CEK pathway regulate cell wall biosynthesis, and Δ and Δ mutants have defects in mannan biosynthesis. The PKC pathway is the classical pathway that maintains cell integrity by regulating cell wall biogenesis and remodeling. In , the Wsc and Mid2 sensors signal to Rho1, which activates Pkc1 and the downstream MAP kinase cascade culminating in Slt2 phosphorylation, and in , the orthologous MAP kinase is Mkc1. In addition, in , Rho1 acts as a regulatory subunit of β(1,3)-glucan synthase and Pkc1 is involved in targeting Chs3 to the plasma membrane in response to heat shock. A number of transcription factors, outlined in black, have been identified in as regulating the expression of cell wall-related genes (). Cas5 and Sko1 are involved in the response to echinocandins, and Bcr1 regulates the expression of a number of important adhesins and functions downstream of the TOR signaling pathway. The role of Sko1 in the transcriptional response to caspofungin is dependent on the Psk1 PAS kinase. Crz1 is the transcription factor that lies downstream of the Ca+/calmodulin pathway. In response to elevated intracellular Ca levels, Crz1 becomes dephosphorylated by calcineurin, moves into the nucleus, and activates expression of genes with calcium-dependent response elements within their promoter sequences. In the genes encoding the Crh GPI-anchored protein family are examples of calcium-responsive genes. The PKC, HOG, and Ca signaling all contribute to the regulation of chitin synthesis in . The signaling pathways are based on the paradigm and are predicted to have homologous functions in In some cases rewiring of pathway components has been experimentally demonstrated in and is presented in the schematic. doi:10.1128/9781555817176.ch14.f1

Citation: Munro C, Richard M. 2012. The Cell Wall: Glycoproteins, Remodeling, and Regulation, p 197-223. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Analysis of the predicted O-glycosylation patterns of cell surface glycoproteins using the NetOGlyc 3.1 Server of the Danish Center for Biological Sequence Analysis (http://www.cbs.dtu.dk/services/NetOGlyc/). One representative pattern is used to illustrate the four different categories identified. Asterisks indicate the proteins of group 1 with neither O glycosylation nor N glycosylation predicted. doi:10.1128/9781555817176.ch14.f2

Citation: Munro C, Richard M. 2012. The Cell Wall: Glycoproteins, Remodeling, and Regulation, p 197-223. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Tandem repeats identified in cell surface glycoproteins. Cell surface glyco-proteins can be classified according to sequence conservation within their intragenic tandem repeats. Four major groups harboring tandem repeats that share common features have been identified: Als, Pir, CFEM, and CxCxYTTYCPL. Representative repeats extracted from the Genome Database (http://www.candidagenome.org/) are shown for the different proteins in each group. Additional sequences from other fungi have been added to some alignments to show the strong conservation between different fungal species. Maggr, G-coupled receptor Mac1; Sacce, ; Zygro, ; Lachth, ; Klula, ; Vanpo, ; Picpa, ; Cangl, . Adapted from references , and . doi:10.1128/9781555817176.ch14.f3

Citation: Munro C, Richard M. 2012. The Cell Wall: Glycoproteins, Remodeling, and Regulation, p 197-223. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

glycoprotein families. The proteins are represented by a rectangle (predicted to be GPI anchored) or an oval (not predicted to be GPI anchored). The large group encircled by the dashed and dotted line represents the putative GPI-anchored proteins. Within this group there are 11 families of genes composed only of GPI-anchored proteins (surrounded by solid lines). In addition, there are 10 mixed families (marked with dotted lines) composed of one or more predicted GPI-anchored proteins and one or more non-GPI-anchored proteins. The families are labeled according to the nomenclature in Table 2 . doi:10.1128/9781555817176.ch14.f4

Citation: Munro C, Richard M. 2012. The Cell Wall: Glycoproteins, Remodeling, and Regulation, p 197-223. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5

Domain organization of glycoprotein families of A common domain organization can be defined for each glycoprotein family. All families display a posttranslational modified domain that is O and/or N glycosylated. The black boxes at the N and the C termini are the signal peptide and the GPI anchor addition signal, respectively. Als proteins consist of tandem immunoglobulin (Ig)-like domains, a β-sheet-rich conserved 127-residue amyloid-forming T region, and a variable number of tandem repeats characteristic of the Als proteins. Iff proteins share a common N-terminal domain of 340 to 350 aa with no predicted specific function. Gas proteins share a GH72 domain (CaZY domain for β(1,3)-glucanosyltransglycosylase, EC 2.4.1) with two catalytic sites located on two glutamic acids at positions 152 and 254 for Pga4/Gas1. The Cys box is the cysteine-enriched module present in Phr1 and -2 and Pga5/Gas2 but not in Phr3 or Pga4/Gas1. Crh proteins share two functional domains, a GH16 domain (CaZY domain for endo-1,3-β-glucanase, EC, and a carbohydrate-binding module (CBM18) for binding chitin, but the last is present only in Utr2/Csf4 and not in Crh11 or Crh12. In the case of Sap proteins, after the propeptide, characteristic of this family, the proteins share an aspartyl protease catalytic domain with two aspartic acid catalytic residues at positions 83 and 380 in Sap9. Four cysteine residues may be responsible for the formation of two disulfide bridges within the catalytic domain. Adapted from references , and . doi:10.1128/9781555817176.ch14.f5

Citation: Munro C, Richard M. 2012. The Cell Wall: Glycoproteins, Remodeling, and Regulation, p 197-223. In Calderone R, Clancy C (ed), and Candidiasis, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817176.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Aimanianda, V.,, C. Clavaud,, C. Simenel,, T. Fontaine,, M. Delepierre, and, J. P. Latge. 2009. Cell wall beta-(1,6)-glucan of Saccharomyces cerevisiae: structural characterization and in situ synthesis. J. Biol. Chem. 284:1340113412.
2. Alberti-Segui, C.,, A. J. Morales,, H. Xing,, M. M. Kessler,, D. A. Willins,, K. G. Weinstock,, G. Cottarel,, K. Fechtel, and, B. Rogers. 2004. Identification of potential cellsurface proteins in Candida albicans and investigation of the role of a putative cell-surface glycosidase in adhesion and virulence. Yeast 21:285302.
3. Albrecht, A.,, A. Felk,, I. Pichova,, J. R. Naglik,, M. Schaller,, P. De Groot,, D. MacCallum,, F. C. Odds,, W. Schafer,, F. Klis,, M. Monod, and, B. Hube. 2006. Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J. Biol. Chem. 281:688694.
4. Almeida, R. S.,, S. Brunke,, A. Albrecht,, S. Thewes,, M. Laue,, J. E. Edwards,, S. G. Filler, and, B. Hube. 2008. The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog. 4:e1000217.
5. Alonso-Monge, R.,, E. Roman,, D. M. Arana,, J. Pla, and, C. Nombela. 2009. Fungi sensing environmental stress. Clin. Microbiol. Infect. 15(Suppl. 1):1719.
6. Angiolella, L.,, A. Vitali,, A. Stringaro,, G. Mignogna,, B. Maras,, M. Bonito,, M. Colone,, A. T. Palamara, and, A. Cassone. 2009. Localisation of Bgl2p upon antifungal drug treatment in Candida albicans. Int. J. Antimicrob. Agents 33:143148.
7. Arana, D. M.,, R. Alonso-Monge,, C. Du,, R. Calderone, and, J. Pla. 2007. Differential susceptibility of mitogen-activated protein kinase pathway mutants to oxidative-mediated killing by phagocytes in the fungal pathogen Candida albicans. Cell. Microbiol. 9:16471659.
8. Arroyo, J.,, C. Bermejo,, R. Garcia, and, J. M. Rodriguez-Pena. 2009. Genomics in the detection of damage in microbial systems: cell wall stress in yeast. Clin. Microbiol. Infect. 15(Suppl. 1):4446.
9. Arroyo, J.,, J. Sarfati,, M. T. Baixench,, E. Ragni,, M. Guillen,, J. M. Rodriguez-Pena,, L. Popolo, and, J. P. Latge. 2007. The GPI-anchored Gas and Crh families are fungal antigens. Yeast 24:289296.
10. Bader, O.,, Y. Krauke, and, B. Hube. 2008. Processing of predicted substrates of fungal Kex2 proteinases from Candida albicans, C. glabrata, Saccharomyces cerevisiae and Pichia pastoris. BMC Microbiol. 8:116.
11. Bailey, D. 1997. Cloning and characterisation of the HYR1 and UBI4 genes from Candida albicans. Ph.D. thesis. University of Aberdeen, Aberdeen, United Kingdom.
12. Bailey, D. A.,, P. J. F. Feldmann,, M. Bovey,, N. A. R. Gow, and, A. J. P. Brown. 1996. The Candida albicans HYR1 gene, which is activated in response to hyphal development, belongs to a gene family encoding yeast cell wall proteins. J. Bacteriol. 178:53535360.
13. Basco, R. D.,, R. Cueva,, E. Andaluz, and, G. Larriba. 1996. In vivo processing of the precursor of the major exoglucanase by KEX2 endoprotease in the Saccharomyces cerevisiae secretory pathway. Biochim. Biophys. Acta 1310:110118.
14. Bastidas, R. J.,, J. Heitman, and, M. E. Cardenas. 2009. The protein kinase Tor1 regulates adhesin gene expression in Candida albicans. PLoS Pathog. 5:e1000294.
15. Bates, S.,, J. M. de la Rosa,, D. M. MacCallum,, A. J. Brown,, N. A. Gow, and, F. C. Odds. 2007. Candida albicans Iff11, a secreted protein required for cell wall structure and virulence. Infect. Immun. 75:29222928.
16. Brand, A.,, S. Shanks,, V. M. Duncan,, M. Yang,, K. Mackenzie, and, N. A. Gow. 2007. Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr. Biol. 17:347352.
17. Braun, B. R.,, W. S. Head,, M. X. Wang, and, A. D. Johnson. 2000. Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156:3144.
18. Bromuro, C.,, M. Romano,, P. Chiani,, F. Berti,, M. Tontini,, D. Proietti,, E. Mori,, A. Torosantucci,, P. Costantino,, R. Rappuoli, and, A. Cassone. 2010. Beta-glucanCRM197 conjugates as candidates antifungal vaccines. Vaccine 28:26152623.
19. Brown, G. D.,, P. R. Taylor,, D. M. Reid,, J. A. Willment,, D. L. Williams,, L. Martinez-Pomares,, S. Y. Wong, and, S. Gordon. 2002. Dectin-1 is a major beta-glucan receptor on macrophages. J. Exp. Med. 196:407412.
20. Brown, J. A.,, and B. J. Catley. 1992. Monitoring polysaccharide synthesis in Candida albicans. Carbohydr. Res. 227:195202.
21. Butler, G.,, M. D. Rasmussen,, M. F. Lin,, M. A. Santos,, S. Sakthikumar,, C. A. Munro,, E. Rheinbay,, M. Grabherr,, A. Forche,, J. L. Reedy,, I. Agrafioti,, M. B. Arnaud,, S. Bates,, A. J. Brown,, S. Brunke,, M. C. Costanzo,, D. A. Fitzpatrick,, P. W. De Groot,, D. Harris,, L. L. Hoyer,, B. Hube,, F. M. Klis,, C. Kodira,, N. Lennard,, M. E. Logue,, R. Martin,, A. M. Neiman,, E. Nikolaou,, M. A. Quail,, J. Quinn,, M. C. Santos,, F. F. Schmitzberger,, G. Sherlock,, P. Shah,, K. A. Silverstein,, M. S. Skrzypek,, D. Soll,, R. Staggs,, I. Stansfield,, M. P. Stumpf,, P. E. Sudbery,, T. Srikantha,, Q. Zeng,, J. Berman,, M. Berriman,, J. Heitman,, N. A. Gow,, M. C. Lorenz,, B. W. Birren,, M. Kellis, and, C. A. Cuomo. 2009. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657662.
22. Cabezon, V.,, A. Llama-Palacios,, C. Nombela,, L. Monteoliva, and, C. Gil. 2009. Analysis of Candida albicans plasma membrane proteome. Proteomics 9:47704786.
23. Cabib, E. 2009. Two novel techniques for determination of polysaccharide cross-links show that Crh1p and Crh2p attach chitin to both β(1-6)- and β(1-3)glucan in the Saccharomyces cerevisiae cell wall. Eukaryot. Cell 8:16261636.
24. Cabib, E.,, N. Blanco,, C. Grau,, J. M. Rodriguez-Pena, and, J. Arroyo. 2007. Crh1p and Crh2p are required for the cross-linking of chitin to beta(1-6)glucan in the Saccharomyces cerevisiae cell wall. Mol. Microbiol. 63:921935.
25. Cabib, E.,, V. Farkas,, O. Kosik,, N. Blanco,, J. Arroyo, and, P. McPhie. 2008. Assembly of the yeast cell wall. Crh1p and Crh2p act as transglycosylases in vivo and in vitro. J. Biol. Chem. 283:2985929872.
26. Cantarel, B. L.,, P. M. Coutinho,, C. Rancurel,, T. Bernard,, V. Lombard, and, B. Henrissat. 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37:D233–D238.
27. Carotti, C.,, L. Ferrario,, C. Roncero,, M.-H. Valdivieso,, A. Duran, and, L. Popolo. 2002. Maintenance of cell integrity in the gas1 mutant of Saccharomyces cerevisiae requires the Chs3p-targeting and activation pathway and involves an unusual Chs3p localization. Yeast 19:11131124.
28. Carotti, C.,, E. Ragni,, O. Palomares,, T. Fontaine,, G. Tedeschi,, R. Rodriguez,, J. P. Latge,, M. Vai, and, L. Popolo. 2004. Characterization of recombinant forms of the yeast Gas1 protein and identification of residues essential for glucanosyltransferase activity and folding. Eur. J. Biochem. 271:36353645.
29. Cassone, A. 2008. Fungal vaccines: real progress from real challenges. Lancet Infect. Dis. 8:114124.
30. Castillo, L.,, E. Calvo,, A. I. Martinez,, J. Ruiz-Herrera,, E. Valentin,, J. A. Lopez, and, R. Sentandreu. 2008. A study of the Candida albicans cell wall proteome. Proteomics 8:38713881.
31. Chaffin, W. L. 2008. Candida albicans cell wall proteins. Microbiol. Mol. Biol. Rev. 72:495544.
32. Chaffin, W. L.,, J. L. Lopez-Ribot,, M. Casanova,, D. Gozalbo, and, J. P. Martinez. 1998. Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol. Mol. Biol. Rev. 62:130180.
33. Chattaway, F. W.,, M. R. Holmes, and, A. J. E. Barlow. 1968. Cell wall composition of the mycelial and blastospore forms of Candida albicans. J. Gen. Microbiol. 51:367376.
34. Cleves, A. E.,, D. N. Cooper,, S. H. Barondes, and, R. B. Kelly. 1996. A new pathway for protein export in Saccharomyces cerevisiae. J. Cell Biol. 133:10171026.
35. Copping, V. M.,, C. J. Barelle,, B. Hube,, N. A. Gow,, A. J. Brown, and, F. C. Odds. 2005. Exposure of Candida albicans to antifungal agents affects expression of SAP2 and SAP9 secreted proteinase genes. J. Antimicrob. Chemother. 55:645654.
36. Cote, P.,, and M. Whiteway. 2008. The role of Candida albicans FAR1 in regulation of pheromone-mediated mating, gene expression and cell cycle arrest. Mol. Microbiol. 68:392404.
37. Cutler, J. E.,, G. S. Deepe, Jr., and, B. S. Klein. 2007. Advances in combating fungal diseases: vaccines on the threshold. Nat. Rev. Microbiol. 5:1328.
38. De Bernardis, F.,, F. A. Muhlschlegel,, A. Cassone, and, W. A. Fonzi. 1998. The pH of the host niche controls gene expression in and virulence of Candida albicans. Infect. Immun. 66:33173325.
39. De Groot, P. W.,, B. W. Brandt, and, F. M. Klis. 2007. Cell wall biology of Candida, p. 291–323. In C. d’Enfert and, B. Hube (ed.), Candida: Comparative and Functional Genomics. Caister Academic Press, Norfolk, United Kingdom.
40. De Groot, P. W.,, A. D. de Boer,, J. Cunningham,, H. L. Dekker,, L. de Jong,, K. J. Hellingwerf,, C. de Koster, and, F. M. Klis. 2004. Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell 3:955965.
41. De Groot, P. W.,, K. J. Hellingwerf, and, F. M. Klis. 2003. Genome-wide identification of fungal GPI proteins. Yeast 20:781796.
42. De Groot, P. W.,, E. A. Kraneveld,, Q. Y. Yin,, H. L. Dekker,, U. Gross,, W. Crielaard,, C. G. De Koster,, O. Bader,, F. M. Klis, and, M. Weig. 2008. The cell wall of the human pathogen Candida glabrata: differential incorporation of novel adhesin-like wall proteins. Eukaryot. Cell 7:19511964.
43. De Groot, P. W.,, A. F. Ram, and, F. M. Klis. 2005. Features and functions of covalently linked proteins in fungal cell walls. Fungal Genet. Biol. 42:657675.
44. Douglas, C. M.,, J. A. D’Ippolito,, G. J. Shei,, M. Meinz,, J. Onishi,, J. A. Marrinan,, W. Li,, G. K. Abruzzo,, A. Flattery,, K. Bartizal,, A. Mitchell, and, M. B. Kurtz. 1997. Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-β-d-glucan synthase inhibitors. Anti-microb. Agents Chemother. 41:24712479.
45. Dupres, V.,, D. Alsteens,, S. Wilk,, B. Hansen,, J. J. Heinisch, and, Y. F. Dufrene. 2009. The yeast Wsc1 cell surface sensor behaves like a nanospring in vivo. Nat. Chem. Biol. 5:857862.
46. Ecker, M.,, R. Deutzmann,, L. Lehle,, V. Mrsa, and, W. Tanner. 2006. Pir proteins of Saccharomyces cerevisiae are attached to beta-1,3-glucan by a new protein-carbohydrate linkage. J. Biol. Chem. 281:1152311529.
47. Eckert, S. E.,, W. J. Heinz,, K. Zakikhany,, S. Thewes,, K. Haynes,, B. Hube, and, F. A. Muhlschlegel. 2006. PGA4, a GAS homologue from Candida albicans, is up-regulated early in infection processes. Fungal Genet. Biol. 44:368377.
48. Eisenhaber, B.,, G. Schneider,, M. Wildpaner, and, F. Eisenhaber. 2004. A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J. Mol. Biol. 337:243253.
49. Eisman, B.,, R. Alonso-Monge,, E. Roman,, D. Arana,, C. Nombela, and, J. Pla. 2006. The Cek1 and Hog1 mitogen-activated protein kinases play complementary roles in cell wall biogenesis and chlamydospore formation in the fungal pathogen Candida albicans. Eukaryot. Cell 5:347358.
50. Felk, A.,, M. Kretschmar,, A. Albrecht,, M. Schaller,, S. Beinhauer,, T. Nichterlein,, D. Sanglard,, H. C. Korting,, W. Schafer, and, B. Hube. 2002. Candida albicans hyphal formation and the expression of the Efg1-regulated proteinases Sap4 to Sap6 are required for the invasion of parenchymal organs. Infect. Immun. 70:36893700.
51. Ferguson, M. A.,, S. W. Homans,, R. A. Dwek, and, T. W. Rademacher. 1988. Glycosyl-phosphatidylinositol moiety that anchors Trypanosoma brucei variant surface glycoprotein to the membrane. Science 239:753759.
52. Fonzi, W. A. 1999. PHR1 and PHR2 of Candida albicans encode putative glycosidases required for proper cross-linking of β-1,3- and β-1,6-glucans. J. Bacteriol. 181:70707079.
53. Fradin, C.,, P. De Groot,, D. MacCallum,, M. Schaller,, F. Klis,, F. C. Odds, and, B. Hube. 2005. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 56:397415.
54. Frank, A. T.,, C. B. Ramsook,, H. N. Otoo,, C. Tan,, G. Soybelman,, J. M. Rauceo,, N. K. Gaur,, S. A. Klotz, and, P. N. Lipke. 2010. Structure and function of glycosylated tandem repeats from Candida albicans Als adhesins. Eukaryot. Cell 9:405414.
55. Frieman, M. B.,, and B. P. Cormack. 2003. The omega-site sequence of glycosylphosphatidylinositol-anchored proteins in Saccharomyces cerevisiae can determine distribution between the membrane and the cell wall. Mol. Microbiol. 50:883896.
56. Frieman, M. B.,, and B. P. Cormack. 2004. Multiple sequence signals determine the distribution of glycosylphosphatidylinositol proteins between the plasma membrane and cell wall in Saccharomyces cerevisiae. Microbiology 150:31053114.
57. Frohner, I. E.,, C. Bourgeois,, K. Yatsyk,, O. Majer, and, K. Kuchler. 2009. C. albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol. Microbiol. 71:240252.
58. Fu, Y.,, A. S. Ibrahim,, D. C. Sheppard,, Y. C. Chen,, S. W. French,, J. E. Cutler,, S. G. Filler, and, J. E. Edwards. 2002. Candida albicans Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol. Microbiol. 44:6172.
59. Fu, Y.,, G. Luo,, B. J. Spellberg,, J. E. Edwards, Jr., and, A. S. Ibrahim. 2008. Gene overexpression/suppression analysis of candidate virulence factors of Candida albicans. Eukaryot. Cell 7:483492.
60. Gagnon-Arsenault, I.,, L. Parise,, J. Tremblay, and, Y. Bourbonnais. 2008. Activation mechanism, functional role and shedding of glycosylphosphatidylinositol-anchored Yps1p at the Saccharomyces cerevisiae cell surface. Mol. Microbiol. 69:982993.
61. Gagnon-Arsenault, I.,, J. Tremblay, and, Y. Bourbonnais. 2006. Fungal yapsins and cell wall: a unique family of aspartic peptidases for a distinctive cellular function. FEMS Yeast Res. 6:966978.
62. Galan-Diez, M.,, D. M. Arana,, D. Serrano-Gomez,, L. Kremer,, J. M. Casasnovas,, M. Ortega,, A. Cuesta-Dominguez,, A. L. Corbi,, J. Pla, and, E. Fernandez-Ruiz. 2010. Candida albicans β-glucan exposure is controlled by the fungal CEK1-mediated mitogen-activated protein kinase pathway that modulates immune responses triggered through dectin-1. Infect. Immun. 78:14261436.
63. Garcera, A.,, L. Castillo,, A. I. Martinez,, M. V. Elorza,, E. Valentin, and, R. Sentandreu. 2005. Anchorage of Candida albicans Ssr1 to the cell wall, and transcript profiling of the null mutant. Res. Microbiol. 156:911920.
64. Garcia, R.,, J. M. Rodriguez-Pena,, C. Bermejo,, C. Nom-bela, and, J. Arroyo. 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. 284:1090110911.
65. Reference deleted.
66. Garcia-Sanchez, S.,, S. Aubert,, I. Iraqui,, G. Janbon,, J. M. Ghigo, and, C. d’Enfert. 2004. Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot. Cell 3:536545.
67. Gastebois, A.,, I. Mouyna,, C. Simenel,, C. Clavaud,, B. Coddeville,, M. Delepierre,, J. P. Latge, and, T. Fontaine. 2010. Characterization of a new beta (1-3)-glucan branching activity of Aspergillus fumigatus. J. Biol. Chem. 285:23862396.
68. Gaur, N. K.,, S. A. Klotz, and, R. L. Henderson. 1999. Overexpression of the Candida albicans ALA1 gene in Saccharomyces cerevisiae results in aggregation following attachment of yeast cells to extracellular matrix proteins, adherence properties similar to those of Candida albicans. Infect. Immun. 67:60406047.
69. Gil-Navarro, I.,, M. L. Gil,, M. Casanova,, J. E. O’Connor,, J. P. Martinez, and, D. Gozalbo. 1997. The glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is a surface antigen. J. Bacteriol. 179:49924999.
70. Gomez, M. J.,, A. Torosantucci,, S. Arancia,, B. Maras,, L. Parisi, and, A. Cassone. 1996. Purification and biochemical characterization of a 65-kilodalton mannoprotein (MP65), a main target of anti-Candida cell-mediated immune responses in humans. Infect. Immun. 64:25772584.
71. Granger, B. L.,, M. L. Flenniken,, D. A. Davis,, A. P. Mitchell, and, J. E. Cutler. 2005. Yeast wall protein 1 of Candida albicans. Microbiology 151:16311644.
72. Hamada, K.,, H. Terashima,, M. Arisawa, and, K. Kitada. 1998. Amino acid sequence requirement for efficient incorporation of glycosylphosphatidylinositol-associated proteins into the cell wall of Saccharomyces cerevisiae. J. Biol. Chem. 273:2694626953.
73. Hartland, R. P.,, T. Fontaine,, J. P. Debeaupuis,, C. Simenel,, M. Delepierre, and, J. P. Latge. 1996. A novel beta-(1-3)-glucanosyltransferase from the cell wall of Aspergillus fumigatus. J. Biol. Chem. 271:2684326849.
74. Hong, Z.,, P. Mann,, K. J. Shaw, and, B. J. Di Domenico. 1994. Analysis of beta-glucans and chitin in a Saccharomyces cerevisiae cell wall mutant using high-performance liquid chromatography. Yeast 10:10831092.
75. Hornbach, A.,, A. Heyken,, L. Schild,, B. Hube,, J. Loffler, and, O. Kurzai. 2009. The glycosylphosphatidylinositol-anchored protease Sap9 modulates the interaction of Candida albicans with human neutrophils. Infect. Immun. 77:52165224.
76. Hoyer, L. L. 2001. The ALS gene family of Candida albicans. Trends Microbiol. 9:176180.
77. Hoyer, L. L.,, C. B. Green,, S. H. Oh, and, X. Zhao. 2008. Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family—a sticky pursuit. Med. Mycol. 46:115.
78. Hoyer, L. L.,, T. L. Payne,, M. Bell,, A. M. Myers, and, S. Scherer. 1998. Candida albicans ALS3 and insights into the nature of the ALS gene family. Curr. Genet. 33:451459.
79. Hube, B. 2004. From commensal to pathogen: stage- and tissue-specific gene expression of Candida albicans. Curr. Opin. Microbiol. 7:336341.
80. Hube, B.,, and J. Naglik. 2001. Candida albicans proteinases: resolving the mystery of a gene family. Microbiology 147:19972005.
81. Inoue, N.,, Y. Murakami, and, T. Kinoshita. 2003. Molecular genetics of paroxysmal nocturnal hemoglobinuria. Int. J. Hematol. 77:107112.
82. Iorio, E.,, A. Torosantucci,, C. Bromuro,, P. Chiani,, A. Ferretti,, M. Giannini,, A. Cassone, and, F. Podo. 2008. Candida albicans cell wall comprises a branched β-d-(1→6)-glucan with β-d-(1→3)-side chains. Carbohydr. Res. 343:10501061.
83. Ishihara, S.,, A. Hirata,, S. Nogami,, A. Beauvais,, J. P. Latge, and, Y. Ohya. 2007. Homologous subunits of 1,3-beta-glucan synthase are important for spore wall assembly in Saccharomyces cerevisiae. Eukaryot. Cell 6:143156.
84. Jaafar, L.,, I. Moukadiri, and, J. Zueco. 2003. Characterization of a disulphide-bound Pir-cell wall protein (Pir-CWP) of Yarrowia lipolytica. Yeast 20:417426.
85. Kalebina, T. S.,, D. K. Laurinavichiute,, A. N. Packeiser,, O. S. Morenkov,, M. D. Ter Avanesyan, and, I. S. Kulaev. 2002. Correct GPI-anchor synthesis is required for the incorporation of endoglucanase/glucanosyltransferase Bgl2p into the Saccharomyces cerevisiae cell wall. FEMS Microbiol. Lett. 210:8185.
86. Kapteyn, J. C.,, G. J. Dijkgraaf,, R. C. Montijn, and, F. M. Klis. 1995. Glucosylation of cell wall proteins in regenerating spheroplasts of Candida albicans. FEMS Microbiol. Lett. 128:271277.
87. Kapteyn, J. C.,, L. L. Hoyer,, J. E. Hecht,, W. H. Muller,, A. Andel,, A. J. Verkleij,, M. Makarow,, H. Van den Ende, and, F. M. Klis. 2000. The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol. Microbiol. 35:601611.
88. Kapteyn, J. C.,, R. C. Montijn,, G. J. Dijkgraaf, and, F. M. Klis. 1994. Identification of beta-1,6-glucosylated cell wall proteins in yeast and hyphal forms of Candida albicans. Eur. J. Cell Biol. 65:402407.
89. Karababa, M.,, E. Valentino,, G. Pardini,, A. T. Coste,, J. Bille, and, D. Sanglard. 2006. CRZ1, a target of the calcineurin pathway in Candida albicans. Mol. Microbiol. 59:14291451.
90. Kempf, M.,, V. Apaire-Marchais,, P. Saulnier,, P. Licznar,, C. Lefrancois,, R. Robert, and, J. Cottin. 2007. Disruption of Candida albicans IFF4 gene involves modifications of the cell electrical surface properties. Colloids Surf. B Biointer-faces 58:250255.
91. Kempf, M.,, J. Cottin,, P. Licznar,, C. Lefrancois,, R. Robert, and, V. Apaire-Marchais. 2009. Disruption of the GPI protein-encoding gene IFF4 of Candida albicans results in decreased adherence and virulence. Mycopathologia 168:7377.
92. Kim, K. Y.,, A. W. Truman, and, D. E. Levin. 2008. Yeast Mpk1 mitogen-activated protein kinase activates transcription through Swi4/Swi6 by a noncatalytic mechanism that requires upstream signal. Mol. Cell. Biol. 28:25792589.
93. Klis, F. M.,, P. De Groot, and, K. Hellingwerf. 2001. Molecular organisation of the cell wall of Candida albicans. Med. Mycol. 39(Suppl. 1):18.
94. Klis, F. M.,, M. de Jong,, S. Brul, and, P. W. De Groot. 2007. Extraction of cell surface-associated proteins from living yeast cells. Yeast 24:253258.
95. Klis, F. M.,, G. J. Sosinska,, P. W. De Groot, and, S. Brul. 2009. Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. FEMS Yeast Res. 9:10131028.
96. Klotz, S. A.,, N. K. Gaur,, R. De Armond,, D. Sheppard,, N. Khardori,, J. E. Edwards, Jr.,, P. N. Lipke, and, M. El Azizi. 2007. Candida albicans Als proteins mediate aggregation with bacteria and yeasts. Med. Mycol. 45:363370.
97. Klotz, S. A.,, N. K. Gaur,, D. F. Lake,, V. Chan,, J. Rauceo, and, P. N. Lipke. 2004. Degenerate peptide recognition by Candida albicans adhesins Als5p and Als1p. Infect. Immun. 72:20292034.
98. Kollar, R.,, E. Petrakova,, G. Ashwell,, P. W. Robbins, and, E. Cabib. 1995. Architecture of the yeast cell wall. The linkage between chitin and beta(1-3)-glucan. J. Biol. Chem. 270:11701178.
99. Kollar, R.,, B. B. Reinhold,, E. Petrakova,, H. J. C. Yeh,, G. Ashwell,, J. Drgonova,, J. C. Kapteyn,, F. M. Klis, and, E. Cabib. 1997. Architecture of the yeast cell wall: beta(1-6)-glucan interconnects mannoprotein, beta(1-3)-glucan, and chitin. J. Biol. Chem. 272:1776217775.
100. Kondoh, O.,, Y. Tachibana,, Y. Ohya,, M. Arisawa, and, T. Watanabe. 1997. Cloning of the RHO1 gene from Candida albicans and its regulation of beta-1,3-glucan synthesis. J. Bacteriol. 179:77347741.
101. Kruppa, M.,, T. Goins,, J. E. Cutler,, D. Lowman,, D. Williams,, N. Chauhan,, V. Menon,, P. Singh,, D. Li, and, R. Calderone. 2003. The role of the Candida albicans histi-dine kinase (CHK1) gene in the regulation of cell wall mannan and glucan biosynthesis. FEMS Yeast Res. 3:289299.
102. Krysan, D. J.,, E. L. Ting,, C. Abeijon,, L. Kroos, and, R. S. Fuller. 2005. Yapsins are a family of aspartyl proteases required for cell wall integrity in Saccharomyces cerevisiae. Eukaryot. Cell 4:13641374.
103. Kulkarni, R. D.,, H. S. Kelkar, and, R. A. Dean. 2003. An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends Biochem. Sci. 28:118121.
104. Kulkarni, R. D.,, M. R. Thon,, H. Pan, and, R. A. Dean. 2005. Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol. 6:R24.
105. Lamarre, C.,, N. Deslauriers, and, Y. Bourbonnais. 2000. Expression cloning of the Candida albicans CSA1 gene encoding a mycelial surface antigen by sorting of Saccharomyces cerevisiae transformants with monoclonal antibody-coated magnetic beads. Mol. Microbiol. 35:444453.
106. Lee, S. A.,, S. Wormsley,, S. Kamoun,, A. F. Lee,, K. Joiner, and, B. Wong. 2003. An analysis of the Candida albicans genome database for soluble secreted proteins using computer-based prediction algorithms. Yeast 20:595610.
107. Lenardon, M. D.,, S. A. Milne,, H. M. Mora-Montes,, F. A. Kaffarnik,, S. C. Peck,, A. J. P. Brown,, C. A. Munro, and, N. A. Gow. 2010. Phosphorylation regulates polarisation of chitin synthesis in Candida albicans. J. Cell Sci. 123(Pt. 1):21992206.
108. Lenardon, M. D.,, C. A. Munro, and, N. A. Gow. 2010. Chitin synthesis and fungal pathogenesis. Curr. Opin. Microbiol. 13:416423.
109. Lenardon, M. D.,, R. K. Whitton,, C. A. Munro,, D. Marshall, and, N. A. R. Gow. 2007. Individual chitin synthase enzymes synthesize microfibrils of differing structure at specific locations in Candida albicans cell wall. Mol. Microbiol. 66:11641173.
110. Lesage, G.,, A. M. Sdicu,, P. Menard,, J. Shapiro,, S. Hussein, and, H. Bussey. 2004. Analysis of beta-1,3-glucan assembly in Saccharomyces cerevisiae using a synthetic interaction network and altered sensitivity to caspofungin. Genetics 167:3549.
111. Lesage, G.,, J. Shapiro,, C. A. Specht,, A. M. Sdicu,, P. Menard,, S. Hussein,, A. H. Tong,, C. Boone, and, H. Bussey. 2005. An interactional network of genes involved in chitin synthesis in Saccharomyces cerevisiae. BMC Genet. 6:8.
112. Levin, D. E. 2005. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69:262291.
113. Li, D.,, D. Williams,, D. Lowman,, M. A. Monteiro,, X. Tan,, M. Kruppa,, W. Fonzi,, E. Roman,, J. Pla, and, R. Calderone. 2009. The Candida albicans histidine kinase Chk1p: signaling and cell wall mannan. Fungal Genet. Biol. 46:731741.
114. Li, F.,, and S. P. Palecek. 2003. EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryot. Cell 2:12661273.
115. Li, F.,, and S. P. Palecek. 2008. Distinct domains of the Candida albicans adhesin Eap1p mediate cell-cell and cell-substrate interactions. Microbiology 154:11931203.
116. Li, F.,, M. J. Svarovsky,, A. J. Karlsson,, J. P. Wagner,, K. Marchillo,, P. Oshel,, D. Andes, and, S. P. Palecek. 2007. Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot. Cell 6:931939.
117. Li, X. S.,, M. S. Reddy,, D. Baev, and, M. Edgerton. 2003. Candida albicans Ssa1/2p is the cell envelope binding protein for human salivary histatin 5. J. Biol. Chem. 278:2855328561.
118. Lopez-Ribot, J. L.,, M. Casanova,, A. Murgui, and, J. P. Martinez. 2004. Antibody response to Candida albicans cell wall antigens. FEMS Immunol. Med. Microbiol. 41:187196.
119. Lopez-Villar, E.,, L. Monteoliva,, M. R. Larsen,, E. Sachon,, M. Shabaz,, M. Pardo,, J. Pla,, C. Gil,, P. Roepstorff, and, C. Nombela. 2006. Genetic and proteomic evidences support the localization of yeast enolase in the cell surface. Proteomics 6(Suppl. 1):S107S118.
120. Lorenz, M. C.,, J. A. Bender, and, G. R. Fink. 2004. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3:10761087.
121. Lott, T. J.,, B. P. Holloway,, D. A. Logan,, R. Fundyga, and, J. Arnold. 1999. Towards understanding the evolution of the human commensal yeast Candida albicans. Microbiology 145:11371143.
122. Loza, L.,, Y. Fu,, A. S. Ibrahim,, D. C. Sheppard,, S. G. Filler, and, J. E. Edwards, Jr. 2004. Functional analysis of the Candida albicans ALS1 gene product. Yeast 21:473482.
123. Lu, C. F.,, R. C. Montijn,, J. L. Brown,, F. Klis,, J. Kurjan,, H. Bussey, and, P. N. Lipke. 1995. Glycosyl phosphatidylinositol-dependent cross-linking of alpha-agglutinin and beta 1,6-glucan in the Saccharomyces cerevisiae cell wall. J. Cell Biol. 128:333340.
124. MacCallum, D. M.,, L. Castillo,, K. Nather,, C. A. Munro,, A. J. Brown,, N. A. Gow, and, F. C. Odds. 2009. Property differences among the four major Candida albicans strain clades. Eukaryot. Cell 8:373387.
125. Maddi, A.,, S. M. Bowman, and, S. J. Free. 2009. Trifluoromethanesulfonic acid-based proteomic analysis of cell wall and secreted proteins of the ascomycetous fungi Neurospora crassa and Candida albicans. Fungal Genet. Biol. 46:768781.
126. Mao, Y.,, Z. Zhang,, C. Gast, and, B. Wong. 2008. C-terminal signals regulate targeting of the GPI-anchored proteins to the cell wall or the plasma membrane in Candida albicans. Eukaryot. Cell 7:19061915.
127. Mao, Y.,, Z. Zhang, and, B. Wong. 2003. Use of green fluorescent protein fusions to analyse the N- and C-terminal signal peptides of GPI-anchored cell wall proteins in Candida albicans. Mol. Microbiol. 50:16171628.
128. Marcil, A.,, C. Gadoury,, J. Ash,, J. Zhang,, A. Nantel, and, M. Whiteway. 2008. Analysis of PRA1 and its relationship to Candida albicans-macrophage interactions. Infect. Immun. 76:43454358.
129. Martchenko, M.,, A. M. Alarco,, D. Harcus, and, M. Whiteway. 2004. Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol. Biol. Cell 15:456467.
130. Martinez, A. I.,, L. Castillo,, A. Garcera,, M. V. Elorza,, E. Valentin, and, R. Sentandreu. 2004. Role of Pir1 in the construction of the Candida albicans cell wall. Microbiology 150:31513161.
131. Martinez-Lopez, R.,, L. Monteoliva,, R. Diez-Orejas,, C. Nombela, and, C. Gil. 2004. The GPI-anchored protein CaEcm33p is required for cell wall integrity, morphogenesis and virulence in Candida albicans. Microbiology 150:33413354.
132. Martin-Yken, H.,, A. Dagkessamanskaia,, F. Basmaji,, A. Lagorce, and, J. Francois. 2003. The interaction of Slt2 MAP kinase with Knr4 is necessary for signalling through the cell wall integrity pathway in Saccharomyces cerevisiae. Mol. Microbiol. 49:2335.
133. Mazan, M.,, K. Mazanova, and, V. Farkas. 2008. Pheno-type analysis of Saccharomyces cerevisiae mutants with deletions in Pir cell wall glycoproteins. Antonie Leeuwenhoek 94:335342.
134. Mazur, P.,, and W. Baginsky. 1996. In vitro activity of 1,3-beta-d-glucan synthase requires the GTP-binding protein Rho1. J. Biol. Chem. 271:1460414609.
135. Moreno-Ruiz, E.,, G. Ortu,, P. W. J. de Groot,, F. Cottier,, C. Loussert,, M. C. Prevost,, C. de Koster,, F. M. Klis,, S. Goyard, and, C. d’Enfert. 2009. The GPI-modified proteins Pga59 and Pga62 of Candida albicans are required for cell wall integrity. Microbiology 155:20042020.
136. Mormeneo, S.,, H. Rico,, M. Iranzo,, C. Aguado, and, R. Sentandreu. 1996. Study of supramolecular structures released from the cell wall of Candida albicans by ethylenediamine treatment. Arch. Microbiol. 166:327335.
137. Mormeneo, S.,, R. Zazueta-Sandoval, and, A. Flores-Carreon. 1995. Isolation and partial characterization of uronic acid-containing glycoproteins from Mucor rouxii. Curr. Microbiol. 30:237241.
138. Moukadiri, I.,, and J. Zueco. 2001. Evidence for the attachment of Hsp150/Pir2 to the cell wall of Saccharomyces cerevisiae through disulfide bridges. FEMS Yeast Res. 1:241245.
139. Mouyna, I.,, T. Fontaine,, M. Vai,, M. Monod,, W. A. Fonzi,, M. Diaquin,, L. Popolo,, R. P. Hartland, and, J. P. Latge. 2000. Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J. Biol. Chem. 275:1488214889.
140. Mouyna, I.,, W. Morelle,, M. Vai,, M. Monod,, B. Lechenne,, T. Fontaine,, A. Beauvais,, J. Sarfati,, M. C. Prevost,, C. Henry, and, J. P. Latge. 2005. Deletion of GEL2 encoding for a beta(1-3)glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Mol. Microbiol. 56:16751688.
141. Mrsa, V.,, T. Seidl,, M. Gentzsch, and, W. Tanner. 1997. Specific labelling of cell wall proteins by biotinylation. Identification of four covalently linked O-mannosylated proteins of Saccharomyces cerevisiae. Yeast 13:11451154.
142. Mrsa, V.,, and W. Tanner. 1999. 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. Yeast 15:813820.
143. Muhlschlegel, F. A.,, and W. A. Fonzi. 1997. PHR2 of Candida albicans encodes a functional homolog of the pH-regulated gene PHR1 with an inverted pattern of pH-dependent expression. Mol. Cell. Biol. 17:59605967.
144. Munro, C. A. 2009. Candida albicans cell wall mediated virulence, p. 69–95. In R. Ashbee and, E. Bignell (ed.), Handbook of Pathogenic Yeasts. Springer-Verlag, Berlin, Germany.
145. Munro, C. A.,, and N. A. Gow. 2001. Chitin synthesis in human pathogenic fungi. Med. Mycol. 39(Suppl. 1):4153.
146. Munro, C. A.,, D. A. Schofield,, G. W. Gooday, and, N. A. R. Gow. 1998. Regulation of chitin synthesis during dimorphic growth of Candida albicans. Microbiology 144:391401.
147. Munro, C. A.,, S. Selvaggini,, I. de Bruijn,, L. Walker,, M. D. Lenardon,, B. Gerssen,, S. Milne,, A. J. Brown, and, N. A. Gow. 2007. The PKC, HOG and Ca2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans. Mol. Microbiol. 63:13991413.
148. Naglik, J.,, A. Albrecht,, O. Bader, and, B. Hube. 2004. Candida albicans proteinases and host/pathogen interactions. Cell. Microbiol. 6:915926.
149. Naglik, J. R.,, D. Moyes,, J. Makwana,, P. Kanzaria,, E. Tsichlaki,, G. Weindl,, A. R. Tappuni,, C. A. Rodgers,, A. J. Woodman,, S. J. Challacombe,, M. Schaller, and, B. Hube. 2008. Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology 154:32663280.
150. Nailis, H.,, D. Vandenbosch,, D. Deforce,, H. J. Nelis, and, T. Coenye. 2010. Transcriptional response to fluconazole and amphotericin B in Candida albicans biofilms. Res. Microbiol. 161:284292.
151. Nantel, A.,, D. Dignard,, C. Bachewich,, D. Harcus,, A. Marcil,, A. P. Bouin,, C. W. Sensen,, H. Hogues,, H. M. van het,, P. Gordon,, T. Rigby,, F. Benoit,, D. C. Tessier,, D. Y. Thomas, and, M. Whiteway. 2002. Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13:34523465.
152. Nather, K.,, and C. A. Munro. 2008. Generating cell surface diversity in Candida albicans and other fungal pathogens. FEMS Microbiol. Lett. 285:137145.
153. Navarro-Garcia, F.,, B. Eisman,, S. M. Fiuza,, C. Nom-bela, and, J. Pla. 2005. The MAP kinase Mkc1p is activated under different stress conditions in Candida albicans. Microbiology 151:27372749.
154. Nobile, C. J.,, D. R. Andes,, J. E. Nett,, F. J. Smith,, F. Yue,, Q. T. Phan,, J. E. Edwards,, S. G. Filler, and, A. P. Mitchell. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2:e63.
155. Nobile, C. J.,, H. A. Schneider,, J. E. Nett,, D. C. Sheppard,, S. G. Filler,, D. R. Andes, and, A. P. Mitchell. 2008. Complementary adhesin function in C. albicans biofilm formation. Curr. Biol. 18:10171024.
156. Nombela, C.,, C. Gil, and, W. L. Chaffin. 2006. Non-conventional protein secretion in yeast. Trends Microbiol. 14:1521.
157. Oh, S. H.,, G. Cheng,, J. A. Nuessen,, R. Jajko,, K. M. Yeater,, X. Zhao,, C. Pujol,, D. R. Soll, and, L. L. Hoyer. 2005. Functional specificity of Candida albicans Als3p proteins and clade specificity of ALS3 alleles discriminated by the number of copies of the tandem repeat sequence in the central domain. Microbiology 151:673681.
158. Ostrosky-Zeichner, L.,, B. D. Alexander,, D. H. Kett,, J. Vazquez,, P. G. Pappas,, F. Saeki,, P. A. Ketchum,, J. Wingard,, R. Schiff,, H. Tamura,, M. A. Finkelman, and, J. H. Rex. 2005. Multicenter clinical evaluation of the (1→3) beta-d-glucan assay as an aid to diagnosis of fungal infections in humans. Clin. Infect. Dis. 41:654659.
159. Otoo, H. N.,, K. G. Lee,, W. Qiu, and, P. N. Lipke. 2007. Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot. Cell 7:776782.
160. Pardini, G.,, P. W. De Groot,, A. T. Coste,, M. Karababa,, F. M. Klis,, C. G. De Koster, and, D. Sanglard. 2006. The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. J. Biol. Chem. 281:4039940411.
161. Perez, A.,, B. Pedros,, A. Murgui,, M. Casanova,, J. L. Lopez-Ribot, and, J. P. Martinez. 2006. Biofilm formation by Candida albicans mutants for genes coding fungal proteins exhibiting the eight-cysteine-containing CFEM domain. FEMS Yeast Res. 6:10741084.
162. Perlin, D. S. 2007. Resistance to echinocandin-class antifungal drugs. Drug Resist. Updat. 10:121130.
163. Pietrella, D.,, A. Rachini,, A. Torosantucci,, P. Chiani,, A. J. Brown,, F. Bistoni,, P. Costantino,, P. Mosci,, C. d’Enfert,, R. Rappuoli,, A. Cassone, and, A. Vecchiarelli. 2010. A beta-glucan-conjugate vaccine and anti-beta-glucan antibodies are effective against murine vaginal candidiasis as assessed by a novel in vivo imaging technique. Vaccine 28:17171725.
164. Pitarch, A.,, R. Diez-Orejas,, G. Molero,, M. Pardo,, M. Sanchez,, C. Gil, and, C. Nombela. 2001. Analysis of the serologic response to systemic Candida albicans infection in a murine model. Proteomics 1:550559.
165. Pitarch, A.,, A. Jimenez,, C. Nombela, and, C. Gil. 2006. Decoding serological response to Candida cell wall immunome into novel diagnostic, prognostic, and therapeutic candidates for systemic candidiasis by proteomic and bioinformatic analyses. Mol. Cell. Proteomics 5:7996.
166. Pitarch, A.,, M. Pardo,, A. Jimenez,, J. Pla,, C. Gil,, M. Sanchez, and, C. Nombela. 1999. Two-dimensional gel electrophoresis as analytical tool for identifying Candida albicans immunogenic proteins. Electrophoresis 20:10011010.
167. Pitoniak, A.,, B. Birkaya,, H. M. Dionne,, N. Vadaie, and, P. J. Cullen. 2009. The signaling mucins Msb2 and Hkr1 differentially regulate the filamentation mitogen-activated protein kinase pathway and contribute to a multi-modal response. Mol. Biol. Cell 20:31013114.
168. Popolo, L.,, D. Gilardelli,, P. Bonfante, and, M. Vai. 1997. Increase in chitin as an essential response to defects in assembly of cell wall polymers in the ggp1Δ mutant of Saccharomyces cerevisiae. J. Bacteriol. 179:463469.
169. Popolo, L.,, E. Ragni,, C. Carotti,, O. Palomares,, R. Aardema,, J. W. Back,, H. L. Dekker,, L. J. de Koning,, L. de Jong, and, C. G. De Koster. 2008. Disulfide bond structure and domain organization of yeast beta(1,3)-glucanosyltransferases involved in cell wall biogenesis. J. Biol. Chem. 283:1855318565.
170. Popolo, L.,, and M. Vai. 1999. The Gas1 glycoprotein, a putative wall polymer cross-linker. Biochim. Biophys. Acta 1426:385400.
171. Qadota, H.,, C. P. Python,, S. B. Inoue,, M. Arisawa,, Y. Anraku,, Y. Zheng,, T. Watanabe,, D. E. Levin, and, Y. Ohya. 1996. Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-beta-glucan synthase. Science 272:279281.
172. Ragni, E.,, A. Coluccio,, E. Rolli,, J. M. Rodriguez-Pena,, G. Colasante,, J. Arroyo,, A. M. Neiman, and, L. Popolo. 2007. GAS2 and GAS4, a pair of developmentally regulated genes required for spore wall assembly in Saccharomyces cerevisiae. Eukaryot. Cell 6:302316.
173. Ragni, E.,, T. Fontaine,, C. Gissi,, J. P. Latge, and, L. Popolo. 2007. The Gas family of proteins of Saccharomyces cerevisiae: characterization and evolutionary analysis. Yeast 24:297308.
174. Ramsook, C. B.,, C. Tan,, M. C. Garcia,, R. Fung,, G. Soybelman,, R. Henry,, A. Litewka,, S. O’Meally,, H. N. Otoo,, R. A. Khalaf,, A. M. Dranginis,, N. K. Gaur,, S. A. Klotz,, J. M. Rauceo,, C. K. Jue, and, P. N. Lipke. 2010. Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot. Cell 9:393404.
175. Rauceo, J. M.,, R. Dearmond,, H. Otoo,, P. C. Kahn,, S. A. Klotz,, N. K. Gaur, and, P. N. Lipke. 2006. Threo-nine-rich repeats increase fibronectin binding in the C. albicans adhesin Als5p. Eukaryot. Cell 5:16641673.
176. Reid, D. M.,, N. A. Gow, and, G. D. Brown. 2009. Pattern recognition: recent insights from Dectin-1. Curr. Opin. Immunol. 21:3037.
177. Richard, M.,, S. Ibata-Ombetta,, F. Dromer,, F. Bordon-Pallier,, T. Jouault, and, C. Gaillardin. 2002. Complete glycosylphosphatidylinositol anchors are required in Candida albicans for full morphogenesis, virulence and resistance to macrophages. Mol. Microbiol. 44:841853.
178. Richard, M. L.,, and A. Plaine. 2007. Comprehensive analysis of glycosylphosphatidylinositol-anchored proteins in Candida albicans. Eukaryot. Cell 6:119133.
179. Ripeau, J. S.,, M. Fiorillo,, F. Aumont,, P. Belhumeur, and, L. De Repentigny. 2002. Evidence for differential expression of Candida albicans virulence genes during oral infection in intact and human immunodeficiency virus type 1-transgenic mice. J. Infect. Dis. 185:10941102.
180. Rodriguez-Pena, J. M.,, V. J. Cid,, J. Arroyo, and, C. Nombela. 2000. A novel family of cell wall-related proteins regulated differently during the yeast life cycle. Mol. Cell. Biol. 20:32453255.
181. Rodriguez-Pena, J. M.,, C. Rodriguez,, A. Alvarez,, C. Nombela, and, J. Arroyo. 2002. Mechanisms for targeting of the Saccharomyces cerevisiae GPI-anchored cell wall protein Crh2p to polarised growth sites. J. Cell Sci. 115:25492558.
182. Roman, E.,, R. Alonso-Monge,, Q. Gong,, D. Li,, R. Calderone, and, J. Pla. 2009. The Cek1 MAPK is a short-lived protein regulated by quorum sensing in the fungal pathogen Candida albicans. FEMS Yeast Res. 9:942955.
183. Roman, E.,, F. Cottier,, J. F. Ernst, and, J. Pla. 2009. Msb2 signaling mucin controls activation of Cek1 mitogen-activated protein kinase in Candida albicans. Eukaryot. Cell 8:12351249.
184. Russo, P.,, N. Kalkkinen,, H. Sareneva,, J. Paakkola, and, M. Makarow. 1992. A heat shock gene from Saccharomyces cerevisiae encoding a secretory glycoprotein. Proc. Natl. Acad. Sci. USA 89:36713675.
185. Sandini, S.,, R. La Valle,, F. De Bernardis,, C. Macri, and, A. Cassone. 2007. The 65 kDa mannoprotein gene of Candida albicans encodes a putative beta-glucanase adhesin required for hyphal morphogenesis and experimental pathogenicity. Cell. Microbiol. 9:12231238.
186. Saporito-Irwin, S. M.,, C. E. Birse,, P. S. Sypherd, and, W. A. Fonzi. 1995. PHR1, a pH-regulated gene of Candida albicans, is required for morphogenesis. Mol. Cell. Biol. 15:601613.
187. Sarthy, A. V.,, T. McGonigal,, M. Coen,, D. J. Frost,, J. A. Meulbroek, and, R. C. Goldman. 1997. Phenotype in Candida albicans of a disruption of the BGL2 gene encoding a 1,3-β-glucosyltransferase. Microbiology 143:367376.
188. Schaller, M.,, U. Boeld,, S. Oberbauer,, G. Hamm,, B. Hube, and, H. C. Korting. 2004. Polymorphonuclear leukocytes (PMNs) induce protective Th1-type cytokine epithelial responses in an in vitro model of oral candidosis. Microbiology 150:28072813.
189. Senn, L.,, J. O. Robinson,, S. Schmidt,, M. Knaup,, N. Asahi,, S. Satomura,, S. Matsuura,, B. Duvoisin,, J. Bille,, T. Calandra, and, O. Marchetti. 2008. 1,3-Beta-d-glucan antigenemia for early diagnosis of invasive fungal infections in neutropenic patients with acute leukemia. Clin. Infect. Dis. 46:878885.
190. Shahinian, S.,, and H. Bussey. 2000. β-1,6-Glucan synthesis in Saccharomyces cerevisiae. Mol. Microbiol. 35:477489.
191. Sheppard, D. C.,, M. R. Yeaman,, W. H. Welch,, Q. T. Phan,, Y. Fu,, A. S. Ibrahim,, S. G. Filler,, M. Zhang,, A. J. Waring, and, J. E. Edwards, Jr. 2004. Functional and structural diversity in the Als protein family of Candida albicans. J. Biol. Chem. 279:3048030489.
192. Sosinska, G. J.,, P. W. De Groot,, M. J. Teixeira de Mattos,, H. L. Dekker,, C. G. De Koster,, K. J. Hellingwerf, and, F. M. Klis. 2008. Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology 154:510520.
193. Spellberg, B. J.,, A. S. Ibrahim,, V. Avanesian,, Y. Fu,, C. Myers,, Q. T. Phan,, S. G. Filler,, M. R. Yeaman, and, J. E. Edwards, Jr. 2006. Efficacy of the anti-Candida rAls3p-N or rAls1p-N vaccines against disseminated and mucosal candidiasis. J. Infect. Dis. 194:256260.
194. Spreghini, E.,, D. A. Davis,, R. Subaran,, M. Kim, and, A. P. Mitchell. 2003. Roles of Candida albicans Dfg5p and Dcw1p cell surface proteins in growth and hypha formation. Eukaryot. Cell 2:746755.
195. Staab, J. F.,, S. D. Bradway,, P. L. Fidel, and, P. Sund-strom. 1999. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283:15351538.
196. Staab, J. F.,, C. A. Ferrer, and, P. Sundstrom. 1996. Developmental expression of a tandemly repeated, proline and glutamine rich amino acid motif on hyphal surfaces of Candida albicans. J. Biol. Chem. 271:62986305.
197. Sullivan, P. A.,, C. Y. Yin,, C. Molloy,, M. D. Templeton, and, M. G. Shepherd. 1983. An analysis of the metabolism and cell wall composition of Candida albicans during germ tube formation. Can. J. Microbiol. 29:15141525.
198. Takeda, J.,, and T. Kinoshita. 1995. GPI-anchor biosynthesis. Trends Biochem. Sci. 20:367371.
199. Tatebayashi, K.,, K. Tanaka,, H. Y. Yang,, K. Yamamoto,, Y. Matsushita,, T. Tomida,, M. Imai, and, H. Saito. 2007. Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J. 26:35213533.
200. Teparic, R.,, I. Stuparevic, and, V. Mrsa. 2007. Binding assay for incorporation of alkali-extractable proteins in the Saccharomyces cerevisiae cell wall. Yeast 24:259266.
201. Theiss, S.,, G. Ishdorj,, A. Brenot,, M. Kretschmar,, C. Y. Lan,, T. Nichterlein,, J. Hacker,, S. Nigam,, N. Agabian, and, G. A. Kohler. 2006. Inactivation of the phospholipase B gene PLB5 in wild-type Candida albicans reduces cell-associated phospholipase A2 activity and attenuates virulence. Int. J. Med. Microbiol. 296:405420.
202. Tiede, A.,, I. Bastisch,, J. Schubert,, P. Orlean, and, R. E. Schmidt. 1999. Biosynthesis of glycosylphosphatidylinositols in mammals and unicellular microbes. Biol. Chem. 380:503523.
203. Toh-e, A.,, S. Yasunaga,, H. Nisogi,, K. Tanaka,, T. Oguchi, and, Y. Matsui. 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 9:481494.
204. Torosantucci, A.,, M. J. Gomez,, C. Bromuro,, I. Casalinuovo, and, A. Cassone. 1991. Biochemical and antigenic characterization of mannoprotein constituents released from yeast and mycelial forms of Candida albicans. J. Med. Vet. Mycol. 29:361372.
205. Umeyama, T.,, A. Kaneko,, H. Watanabe,, A. Hirai,, Y. Uehara,, M. Niimi, and, M. Azuma. 2006. Deletion of the CaBIG1 gene reduces β-1,6-glucan synthesis, filamentation, adhesion, and virulence in Candida albicans. Infect. Immun. 74:23732381.
206. Vadaie, N.,, H. Dionne,, D. S. Akajagbor,, S. R. Nicker-son,, D. J. Krysan, and, P. J. Cullen. 2008. Cleavage of the signaling mucin Msb2 by the aspartyl protease Yps1 is required for MAPK activation in yeast. J. Cell Biol. 181:10731081.
207. Valdivieso, M. H.,, L. Ferrario,, M. Vai,, A. Duran, and, L. Popolo. 2000. Chitin synthesis in a gas1 mutant of Saccharomyces cerevisiae. J. Bacteriol. 182:47524757.
208. Verstrepen, K. J.,, and G. R. Fink. 2009. Genetic and epigenetic mechanisms underlying cell-surface variability in protozoa and fungi. Annu. Rev. Genet. 43:124.
209. Verstrepen, K. J.,, A. Jansen,, F. Lewitter, and, G. R. Fink. 2005. Intragenic tandem repeats generate functional variability. Nat. Genet. 37:986990.
210. Walker, L. A.,, N. A. Gow, and, C. A. Munro. 2009. Fungal echinocandin resistance. Fungal Genet. Biol. 47:117126.
211. Walker, L. A.,, C. A. Munro,, I. de Bruijn,, M. D. Lenardon,, A. McKinnon, and, N. A. R. Gow. 2008. Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog. 4:e1000040.
212. Weig, M.,, K. Haynes,, T. R. Rogers,, O. Kurzai,, M. Frosch, and, F. A. Muhlschlegel. 2001. A GAS-like gene family in the pathogenic fungus Candida glabrata. Microbiology 147:20072019.
213. Weissman, Z.,, and D. Kornitzer. 2004. A family of Candida cell surface haem-binding proteins involved in haemin and haemoglobin-iron utilization. Mol. Microbiol. 53:12091220.
214. Weissman, Z.,, R. Shemer,, E. Conibear, and, D. Kornitzer. 2008. An endocytic mechanism for haemoglobin-iron acquisition in Candida albicans. Mol. Microbiol. 69:201217.