Advertisement

Carbon Metabolism in Pathogenic Yeasts (Especially Candida): The Role of Cell Wall Metabolism in Virulence

Chapter
  • 2k Downloads

Abstract

Fungal pathogens are found in the natural environment and associated with living organisms including humans. The major life-threatening human fungal pathogens are Cryptococcus, Aspergillus, and Candida species (spp.). Among Candida spp., C. albicans is the most prevalent human pathogen responsible for a range of infections that differ in their severity according to the host’s immune status.

Keywords

Fungal Cell Wall Cell Wall Protein Cell Wall Biosynthesis Cell Wall Integrity Alternative Carbon Source 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aebi M (2013) N-linked protein glycosylation in the ER. Biochimica et Biophysica Acta dol 1833(11):2430--2437Google Scholar
  2. Almeida RS, Brunke S, Albrecht A, Thewes S, Laue M, Edwards JE Jr, Filler SG, Hube B (2008) The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog 4:e1000217PubMedCentralPubMedGoogle Scholar
  3. Alvarez FJ, Konopka JB (2007) Identification of an N-acetylglucosamine transporter that mediates hyphal induction in Candida albicans. Mol Biol Cell 18:965–975PubMedCentralPubMedGoogle Scholar
  4. Askew C, Sellam A, Epp E, Hogues H, Mullick A, Nantel A, Whiteway M (2009) Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans. PLoS Pathog 5:e1000612PubMedCentralPubMedGoogle Scholar
  5. Baek YU, Martin SJ, Davis DA (2006) Evidence for novel pH-dependent regulation of Candida albicans Rim101, a direct transcriptional repressor of the cell wall β-glycosidase Phr2. Eukaryot Cell 5:1550–1559PubMedCentralPubMedGoogle Scholar
  6. Bahnan W, Koussa J, Younes S, Rizk MA, Khalil B, Sitt SE, Hanna S, El-Sibai M, Khalaf RA (2012) Deletion of the Candida albicans PIR32 results in increased virulence, stress response, and upregulation of cell call chitin deposition. Mycopathologia 174:107–119PubMedGoogle Scholar
  7. Baker LG, Specht CA, Lodge JK (2011) Cell wall chitosan is necessary for virulence in the opportunistic pathogen Cryptococcus neoformans. Eukaryot Cell 10:1264–1268PubMedCentralPubMedGoogle Scholar
  8. Barelle CJ, Priest CL, MacCallum DM, Gow NAR, Odds FC, Brown AJP (2006) Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell Microbiol 8:961–971PubMedCentralPubMedGoogle Scholar
  9. Bates S, Hughes HB, Munro CA, Thomas WP, MacCallum DM, Bertram G, Atrih A, Ferguson MA, Brown AJ, Odds FC, Gow NA (2006) Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem 281:90–98PubMedGoogle Scholar
  10. Bates S, MacCallum DM, Bertram G, Munro CA, Hughes HB, Buurman ET, Brown AJ, Odds FC, Gow NA (2005) Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+-ATPase, is required for glycosylation and virulence. J Biol Chem 280:23408–23415PubMedGoogle Scholar
  11. Becker JM, Kauffman SJ, Hauser M, Huang L, Lin M, Sillaots S, Jiang B, Xu D, Roemer T (2010) Pathway analysis of Candida albicans survival and virulence determinants in a murine infection model. Proc Natl Acad Sci USA 107:22044–22049PubMedCentralPubMedGoogle Scholar
  12. Ben-Ami R, Garicia-Effron G, Lewis RE, Gamarra S, Leventakos K, Perlin DS, Kontoyiannis P (2011) Fitness and virulence costs of Candida albicans FKS1 hot spot mutations associated with echinocandin resistance. J Infec Dis 204:626–635Google Scholar
  13. Ben-Ami R, Kontoyiannis DP (2012) Resistance to echinocandins comes at a cost: the impact of FKS1 hotspot mutations on Candida albicans fitness and virulence. Virulence 3:95–98PubMedCentralPubMedGoogle Scholar
  14. Bowman SM, Free SJ (2006) The structure and synthesis of the fungal cell wall. BioEssays 28:799–808PubMedGoogle Scholar
  15. Brown DH Jr, Giusani AD, Chen X, Kumamoto CA (1999) Filamentous growth of Candida albicans in response to physical environmental cues and its regulation by the unique CZF1 gene. Mol Microbiol 34:651–662PubMedGoogle Scholar
  16. Bruno VM, Kalachikov S, Subaran R, Nobile CJ, Kyratsous C, Mitchell AP (2006) Control of the Candida albicans cell wall damage response by transcriptional regulator Cas5. PLoS Pathog 2:0204–0210Google Scholar
  17. Bulawa CE, Miller DW, Henry LK, Becker JM (1995) Attenuated virulence of chitin-deficient mutants of Candida albicans. Proc Natl Acad Sci USA 92:10570–10574PubMedCentralPubMedGoogle Scholar
  18. Bulik DA, Olczak M, Lucero HA, Osmond BC, Robbins PW, Specht CA (2003) Chitin synthesis in Saccharomyces cerevisiae in response to supplementation of growth medium with glucosamine and cell wall stress. Eukaryot Cell 2:886–900PubMedCentralPubMedGoogle Scholar
  19. Buurman ET, Westwater C, Hube B, Brown AJP, Odds FC, Gow NAR (1998) Molecular analysis of CaMnt1p, a mannosyl transferase important for adhesion and virulence of Candida albicans. Proc Natl Acad Sci USA 95:7670–7675PubMedCentralPubMedGoogle Scholar
  20. 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 8:1626–1636PubMedCentralPubMedGoogle Scholar
  21. Cabib E, Farkas V, Kosík O, Blanco N, Arroyo J, McPhie P (2008) Assembly of the yeast cell wall: Crh1p and Crh2p act as transglycosylases in vivo and in vitro. J Biol Chem 283:29859–29872PubMedCentralPubMedGoogle Scholar
  22. Cabib E, Blanco N, Grau C, Rodríguez-Peña JM, Arroyo J (2007) Crh1p and Crh2p are required for the cross-linking of chitin to β(1-6)glucan in the Saccharomyces cerevisiae cell wall. Mol Microbiol 63:921–935PubMedGoogle Scholar
  23. Campbell RN, Leverentz MK, Ryan LA, Reece RJ (2008) Metabolic control of transcription: paradigms and lessons from Saccharomyces cerevisiae. Biochem J 414:177–187PubMedGoogle Scholar
  24. Chaffin WL (2008) Candida albicans cell wall proteins. Microbiol Mol Biol Rev 72:495–544PubMedCentralPubMedGoogle Scholar
  25. Chaffin WL, López-Ribot JL, Casanova M, Gozalbo D, Martínez JP (1998) Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev 62:130–180PubMedCentralPubMedGoogle Scholar
  26. Chen H, Fujita M, Feng Q, Clardy J, Fink GR (2004) Tyrosol is a quorum-sensing molecule in Candida albicans. Proc Natl Acad Sci USA 101:5048–5052PubMedCentralPubMedGoogle Scholar
  27. Copping VMS, Barelle CJ, Hube B, Gow NAR, Brown AJP, Odds FC (2005) Exposure of Candida albicans to antifungal agents affects expression of SAP2 and SAP9 secreted proteinase genes. J Antimicrob Chemother 55:645–654PubMedGoogle Scholar
  28. de Groot PWJ, Hellingwerf KJ, Klis FM (2003) Genome-wide identification of fungal GPI proteins. Yeast 20:781–796PubMedGoogle Scholar
  29. Denning DW (2002) Echinocandins: a new class of antifungal. J Antimicrob Chemother 49:889–891PubMedGoogle Scholar
  30. Douglas CM, D’Ippolito JA, Shei GJ, Meinz M, Onishi J, Marrinan JA, Li W, Abruzzo GK, Flattery A, Bartizal K, Mitchell A, Kurtz MB (1997) Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-D-glucan synthase inhibitors. Antimicrob Agents Chemother 41:2471–2479PubMedCentralPubMedGoogle Scholar
  31. Ene IV, Cheng S-, Netea MG, Brown AJP (2013) Growth of Candida albicans cells on the physiologically relevant carbon source lactate affects their recognition and phagocytosis by immune cells. Infect Immun 81:238–248PubMedCentralPubMedGoogle Scholar
  32. Ene IV, Adya AK, Wehmeier S, Brand AC, Maccallum DM, Gow NAR, Brown AJP (2012a) Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cell Microbiol 14:1319–1335PubMedCentralPubMedGoogle Scholar
  33. Ene IV, Heilmann CJ, Sorgo AG, Walker LA, De Koster CG, Munro CA, Klis FM, Brown AJP (2012b) Carbon source-induced reprogramming of the cell wall proteome and secretome modulates the adherence and drug resistance of the fungal pathogen Candida albicans. Proteomics 12:3164–3179PubMedCentralPubMedGoogle Scholar
  34. Ene IV, Bennett RJ (2009) Hwp1 and related adhesins contribute to both mating and biofilm formation in Candida albicans. Eukaryot Cell 8:1909–1913PubMedCentralPubMedGoogle Scholar
  35. Ener B, Douglas LJ (1992) Correlation between cell-surface hydrophobicity of Candida albicans and adhesion to buccal epithelial cells. FEMS Microbiol Lett 99:37–42Google Scholar
  36. Fan J, Chaturvedi V, Shen S (2002) Identification and phylogenetic analysis of a glucose transporter gene family from the human pathogenic yeast Candida albicans. J Mol Evol 55:336–346PubMedGoogle Scholar
  37. Fanning S, Xu W, Solis N, Woolford CA, Filler SG, Mitchell AP (2012) Divergent targets of Candida albicans biofilm regulator Bcr1 in vitro and in vivo. Eukaryot Cell 11:896–904PubMedCentralPubMedGoogle Scholar
  38. Fleck CB, Schöbel F, Brock M (2011) Nutrient acquisition by pathogenic fungi: nutrient availability, pathway regulation, and differences in substrate utilization. Int J Med Microbiol 301:400–407PubMedGoogle Scholar
  39. Fonzi WA (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 181:7070–7079PubMedCentralPubMedGoogle Scholar
  40. Fradin C, Hube B (2006) Transcriptional profiling of Candida albicans in human blood. Microbe 1:76–80Google Scholar
  41. Fradin C, Thewes S, Zakikhany K, Albrecht A, Bader O, Kunze D, Hube B (2004) Transcriptional profiling of Candida albicans during infections. Mikologia Lekarska 11:157–163Google Scholar
  42. Free SJ (2013) Fungal cell wall organization and biosynthesis. Adv Genet 81:33–82PubMedGoogle Scholar
  43. Fujita M, Kinoshita T (2012) GPI-anchor remodeling: potential functions of GPI-anchors in intracellular trafficking and membrane dynamics. Biochim Biophys Acta 1821:1050–1058PubMedGoogle Scholar
  44. Fukuda Y, Tsai H-, Myers TG, Bennett JE (2013) Transcriptional profiling of Candida glabrata during phagocytosis by neutrophils and in the infected mouse spleen. Infect Immun 81:1325–1333PubMedCentralPubMedGoogle Scholar
  45. Gelis S, de Groot PWJ, Castillo L, Moragues M-, Sentandreu R, Gómez M-, Valentín E (2012) Pga13 in Candida albicans is localized in the cell wall and influences cell surface properties, morphogenesis and virulence. Fungal Genet Biol 49:322–331PubMedGoogle Scholar
  46. Gow NA, Hube B (2012) Importance of the Candida albicans cell wall during commensalism and infection. Curr Opin Microbiol 15:406–412PubMedGoogle Scholar
  47. Gow NA, Netea MG, Munro CA, Ferwerda G, Bates S, Mora-Montes HM, Walker L, Jansen T, Jacobs L, Tsoni V, Brown GD, Odds FC, Van der Meer JW, Brown AJ, Kullberg BJ (2007) Immune recognition of Candida albicans beta-glucan by dectin-1. J Infect Dis 196:1565–1571PubMedCentralPubMedGoogle Scholar
  48. Gregori C, Glaser W, Frohner IE, Reinoso-Martín C, Rupp S, Schüller C, Kuchler K (2011) Efg1 controls caspofungin-induced cell aggregation of Candida albicans through the adhesin Als1. Eukaryot Cell 10:1694–1704PubMedCentralPubMedGoogle Scholar
  49. Gunasekera A, Alvarez FJ, Douglas LM, Wang HX, Rosebrock AP, Konopka JB (2010) Identification of GIG1, a GlcNAc-induced gene in Candida albicans needed for normal sensitivity to the chitin synthase inhibitor nikkomycin Z. Eukaryot Cell 9:1476–1483PubMedCentralPubMedGoogle Scholar
  50. Hall RA, Bates S, Lenardon MD, Maccallum DM, Wagener J, Lowman DW, Kruppa MD, Williams DL, Odds FC, Brown AJ, Gow NA (2013) The Mnn2 mannosyltransferase family modulates mannoprotein fibril length, immune recognition and virulence of Candida albicans. PLoS Pathog 9:e1003276PubMedCentralPubMedGoogle Scholar
  51. Hayek P, Dib L, Yazbeck P, Beyrouthy B, Khalaf RA (2010) Characterization of Hwp2, a Candida albicans putative GPI-anchored cell wall protein necessary for invasive growth. Microbiol Res 165:250–258PubMedGoogle Scholar
  52. Heilmann CJ, Sorgo AG, Siliakus AR, Dekker HL, Brul S, Koster CG, de Koning LJ, Klis FM (2011) Hyphal induction in the human fungal pathogen Candida albicans reveals a characteristic wall protein profile. Microbiology 157:2297–2307PubMedGoogle Scholar
  53. Herrero AB, Magnelli P, Mansour MK, Levitz SM, Bussey H, Abeijon C (2004) KRE5 gene null mutant strains of Candida albicans are avirulent and have altered cell wall composition and hypha formation properties. Eukaryot Cell 3:1423–1432PubMedCentralPubMedGoogle Scholar
  54. Hoehamer CF, Cummings ED, Hilliard GM, Rogers PD (2010) Changes in the proteome of Candida albicans in response to azole, polyene, and echinocandin antifungal agents. Antimicrob Agents Chemother 54:1655–1664PubMedCentralPubMedGoogle Scholar
  55. Hoyer LL, Green CB, Oh SH, Zhao X (2008) Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family—A sticky pursuit. Med Mycol 46:1–15PubMedCentralPubMedGoogle Scholar
  56. Hoyer LL (2001) The ALS gene family of Candida albicans. Trends Microbiol 9:176–180PubMedGoogle Scholar
  57. Huang G (2012) Regulation of phenotypic transitions in the fungal pathogen Candida albicans. Virulence 3:6Google Scholar
  58. Huang G, Yi S, Sahni N, Daniels KJ, Srikantha T, Soll DR (2010) N-acetylglucosamine induces white to opaque switching, a mating prerequisite in Candida albicans. PLoS Pathog 6:e1000806PubMedCentralPubMedGoogle Scholar
  59. Hube B (2006) Infection-associated genes of Candida albicans. Future Microbiol 1:209–218PubMedGoogle Scholar
  60. Jyothi Kumar M, Jamaluddin MS, Natarajan K, Kaur D, Datta A (2000) The inducible N-acetylglucosamine catabolic pathway gene cluster in Candida albicans: discrete N-acetylglucosamine-inducible factors interact at the promoter of NAG1. Proc Natl Acad Sci USA 97:14218–14223PubMedCentralGoogle Scholar
  61. Kamai Y, Kubota M, Kamai Y, Hosokawa T, Fukuoka T, Filler SG (2002) Contribution of Candida albicans ALS1 to the pathogenesis of experimental oropharyngeal candidiasis. Infect Immun 70:5256–5258PubMedCentralPubMedGoogle Scholar
  62. Kamthan M, Kamthan A, Ruhela D, Maiti P, Bhavesh NS, Datta A (2013) Upregulation of galactose metabolic pathway by N-acetylglucosamine induced endogenous synthesis of galactose in Candida albicans. Fungal Genet Biol 54:15–24PubMedGoogle Scholar
  63. Kamthan M, Mukhopadhyay G, Chakraborty N, Chakraborty S, Datta A (2012) Quantitative proteomics and metabolomics approaches to demonstrate N-acetyl-d-glucosamine inducible amino acid deprivation response as morphological switch in Candida albicans. Fungal Genet Biol 49:369–378PubMedGoogle Scholar
  64. Kapteyn JC, Hoyer LL, Hecht JE, Muller WH, Andel A, Verkleij AJ, Makarow M, Van Den Ende H, Klis FM (2000) The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol Microbiol 35:601–611PubMedGoogle Scholar
  65. Kitamura A, Someya K, Hata M, Nakajima R, Takemura M (2009) Discovery of a small-molecule inhibitor of β-1,6-glucan synthesis. Antimicrob Agents Chemother 53:670–677PubMedCentralPubMedGoogle Scholar
  66. Klis FM, Sosinska GJ, De Groot PWJ, Brul S (2009) Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. FEMS Yeast Res 9:1013–1028PubMedGoogle Scholar
  67. Klis FM, de Groot P, Hellingwerf K (2001) Molecular organization of the cell wall of Candida albicans. Med Mycol 39(Suppl 1):1–8PubMedGoogle Scholar
  68. Kollar R, Petrakova E, Ashwell G, Robbins PW, Cabib E (1995) Architecture of the yeast cell wall. The linkage between chitin and β(1 → 3)-glucan. J Biol Chem 270:1170–1178PubMedGoogle Scholar
  69. Kollár R, Reinhold BB, Petráková E, Yeh HJC, Ashwell G, Drgonová J, Kapteyn JC, Klis FM, Cabib E (1997) Architecture of the yeast cell wall: β(1 → 6)glucan interconnects mannoprotein, β(1 → 3)-glucan, and chitin. J Biol Chem 272:17762–17775PubMedGoogle Scholar
  70. Konopka JB (2012) N-acetylglucosamine (GlcNAc) functions in cell signaling. Scientifica (Cairo) 2012:489208Google Scholar
  71. Kvaal C, Lachke SA, Srikantha T, Daniels K, Mccoy J, Soll DR (1999) Misexpression of the opaque-phase-specific gene PEP1 (SAP1) in the white phase of Candida albicans confers increased virulence in a mouse model of cutaneous infection. Infect Immun 67:6652–6662PubMedCentralPubMedGoogle Scholar
  72. Lagorce A, Berre-Anton VL, Aguilar-Uscanga B, Martin-Yken H, Dagkessamanskaia A, François J (2002) Involvement of GFA1, which encodes glutamine-fructose-6-phosphate amidotransferase, in the activation of the chitin synthesis pathway in response to cell-wall defects in Saccharomyces cerevisiae. European J Biochem 269:1697–1707Google Scholar
  73. Lan C-, Newport G, Murillo LA, Jones T, Scherer S, Davis RW, Agabian N (2002) Metabolic specialization associated with phenotypic switching in Candida albicans. Proc Natl Acad Sci USA 99:14907–14912PubMedCentralPubMedGoogle Scholar
  74. Latgé JP (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66:279–290PubMedGoogle Scholar
  75. Lee CG (2009) Chitin, chitinases and chitinase-like proteins in allergic inflammation and tissue remodeling. Yonsei Med J 50:22–30PubMedCentralPubMedGoogle Scholar
  76. Lee CG, Da Silva CA, Lee JY, Hartl D, Elias JA (2008) Chitin regulation of immune responses: an old molecule with new roles. Curr Opin Immunol 20:684–689PubMedCentralPubMedGoogle Scholar
  77. Lee KK, MacCallum DM, Jacobsen MD, Walker LA, Odds FC, Gow NAR, Munro CA (2012) Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrob Agents Chemother 56:208–217PubMedCentralPubMedGoogle Scholar
  78. Lenardon MD, Munro CA, Gow NAR (2010) Chitin synthesis and fungal pathogenesis. Curr Opin Microbiol 13:416–423PubMedCentralPubMedGoogle Scholar
  79. Lipinski T, Wu X, Sadowska J, Kreiter E, Yasui Y, Cheriaparambil S, Rennie R, Bundle DR (2012) A β-mannan trisaccharide conjugate vaccine aids clearance of Candida albicans in immunocompromised rabbits. Vaccine 30:6263–6269PubMedGoogle Scholar
  80. Liu TT, Lee REB, Barker KS, Lee RE, Wei L, Homayouni R, Rogers PD (2005) Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob Agents Chemother 49:2226–2236PubMedCentralPubMedGoogle Scholar
  81. Liu Y, Filler SG (2011) Candida albicans Als3, a multifunctional adhesin and invasin. Eukaryot Cell 10:168–173PubMedCentralPubMedGoogle Scholar
  82. Lorenz MC, Bender JA, Fink GR (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3:1076–1087PubMedCentralPubMedGoogle Scholar
  83. Lussier M, Sdicu AM, Shahinian S, Bussey H (1998) The Candida albicans KRE9 gene is required for cell wall β-1,6-glucan synthesis and is essential for growth on glucose. Proc Natl Acad Sci USA 95:9825–9830PubMedCentralPubMedGoogle Scholar
  84. Marcil A, Gadoury C, Ash J, Zhang J, Nantel A, Whiteway M (2008) Analysis of PRA1 and its relationship to Candida albicans-macrophage interactions. Infec Immun 76:4345–4358Google Scholar
  85. Martchenko M, Levitin A, Hogues H, Nantel A, Whiteway M (2007) Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr Biol 17:1007–1013PubMedGoogle Scholar
  86. Martin R, Albrecht-Eckardt D, Brunke S, Hube B, Hünniger K, Kurzai O (2013) A core filamentation response network in Candida albicans is restricted to eight genes. PLoS ONE 8:e58613PubMedCentralPubMedGoogle Scholar
  87. Martínez AI, Castillo L, Garcerá A, Elorza MV, Valentín E, Sentandreu R (2004) Role of Pir1 in the construction of the Candida albicans cell wall. Microbiology 150:3151–3161PubMedGoogle Scholar
  88. Mattia E, Carruba G, Angiolella L, Cassone A (1982) Induction of germ tube formation by N-acetyl-D-glucosamine in Candida albicans: uptake of inducer and germinative response. J Bacteriol 152:555–562PubMedCentralPubMedGoogle Scholar
  89. McKenzie CGJ, Koser U, Lewis LE, Bain JM, Mora-Montes HM, Barker RN, Gow NAR, Erwig LP (2010) Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect Immun 78:1650–1658PubMedCentralPubMedGoogle Scholar
  90. Milewski S, Gabriel I, Olchowy J (2006) Enzymes of UDP-GlcNAc biosynthesis in yeast. Yeast 23:1–14PubMedGoogle Scholar
  91. Mille C, Bobrowicz P, Trinel P-, Li H, Maes E, Guerardel Y, Fradin C, Martínez-Esparza M, Davidson RC, Janbon G, Poulain D, Wildt S (2008) Identification of a new family of genes involved in β-1,2- mannosylation of glycans in Pichia pastoris and Candida albicans. J Biol Chem 283:9724–9736PubMedGoogle Scholar
  92. Mio T, Kokado M, Arisawa M, Yamada-Okabe H (2000) Reduced virulence of Candida albicans mutants lacking the GNA1 gene encoding glucosamine-6-phosphate acetyltransferase. Microbiology 146:1753–1758PubMedGoogle Scholar
  93. Mio T, Adachi-Shimizu M, Tachibana Y, Tabuchi H, Inoue SB, Yabe T, Yamada-Okabe T, Arisawa M, Watanabe T, Yamada-Okabe H (1997a) Cloning of the Candida albicans homolog of Saccharomyces cerevisiae GSC1/FKS1 and its involvement in β-1,3-glucan synthesis. J Bacteriol 179:4096–4105PubMedCentralPubMedGoogle Scholar
  94. Mio T, Yamada-Okabe T, Yabe T, Nakajima T, Arisawa M, Yamada-Okabe H (1997b) Isolation of the Candida albicans homologs of Saccharomyces cerevisiae KRE6 and SKN1: expression and physiological function. J Bacteriol 179:2363–2372PubMedCentralPubMedGoogle Scholar
  95. Miramón P, Dunker C, Windecker H, Bohovych IM, Brown AJP, Kurzai O, Hube B (2012) Cellular responses of Candida albicans to phagocytosis and the extracellular activities of neutrophils are critical to counteract carbohydrate starvation, oxidative and nitrosative stress. PLoS ONE 7:e52850PubMedCentralPubMedGoogle Scholar
  96. Mora-Montes HM, Netea MG, Ferwerda G, Lenardon MD, Brown GD, Misura AS, Kullberg BJ, O’Callaghan CA, Sheth CC, Odds FC, Brown AJP, Munro CA, Gow NAR (2011) Recognition and blocking of innate immunity cells by Candida albicans chitin. Infect Immun 79:1961–1970PubMedCentralPubMedGoogle Scholar
  97. Mora-Montes HM, Ponce-Noyola P, Villagómez-Castro JC, Gow NAR, Flores-Carreón A, López-Romero E (2009) Protein glycosylation in Candida. Future Microbiol 4:1167–1183PubMedGoogle Scholar
  98. Munro CA (2013) Chitin and glucan, the yin and yang of the fungal cell wall, implications for antifungal drug discovery and therapy. Adv Appl Microbiol 83:145–172PubMedGoogle Scholar
  99. Munro CA, Richard ML (2012) The cell wall: glycoproteins, remodeling, and regulation. In: Calderone RA, Clancy CJ (eds) Candida and Candidiasis, 2nd edn. ASM Press, Washington D.C, pp 197–223Google Scholar
  100. Munro CA, Selvaggini S, de Bruijn I, Walker L, Lenardon MD, Gerssen B, Milne S, Brown AJ, Gow NA (2007) The PKC, HOG and Ca2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans. Mol Microbiol 63:1399–1413PubMedCentralPubMedGoogle Scholar
  101. Munro CA, Bates S, Buurman ET, Hughes HB, Maccallum DM, Bertram G, Atrih A, Ferguson MA, Bain JM, Brand A, Hamilton S, Westwater C, Thomson LM, Brown AJ, Odds FC, Gow NA (2005) Mnt1p and Mnt2p of Candida albicans are partially redundant alpha-1,2-mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence. J Biol Chem 280:1051–1060PubMedCentralPubMedGoogle Scholar
  102. Munro CA, Winter K, Buchan A, Henry K, Becker JM, Brown AJ, Bulawa CE, Gow NA (2001) Chs1 of Candida albicans is an essential chitin synthase required for synthesis of the septum and for cell integrity. Mol Microbiol 39:1414–1426PubMedGoogle Scholar
  103. Munro CA, Schofield DA, Gooday GW, Gow NA (1998) Regulation of chitin synthesis during dimorphic growth of Candida albicans. Microbiology 144:391–401PubMedGoogle Scholar
  104. Murciano C, Moyes DL, Runglall M, Tobouti P, Islam A, Hoyer LL, Naglik JR (2012) Evaluation of the role of Candida albicans agglutinin-like sequence (ALS) proteins in human oral epithelial cell interactions. PLoS ONE 7:e33362PubMedCentralPubMedGoogle Scholar
  105. Nagatani K, Wang S, Llado V, Lau CW, Li Z, Mizoguchi A, Nagler CR, Shibata Y, Reinecker HC, Mora JR, Mizoguchi E (2012) Chitin microparticles for the control of intestinal inflammation. Inflamm Bowel Dis 18:1698–1710PubMedCentralPubMedGoogle Scholar
  106. Naseem S, Gunasekera A, Araya E, Konopka JB (2011) N-acetylglucosamine (GlcNAc) induction of hyphal morphogenesis and transcriptional responses in Candida albicans are not dependent on its metabolism. J Biol Chem 286:28671–28680PubMedCentralPubMedGoogle Scholar
  107. Natarajan K, Datta A (1993) Molecular cloning and analysis of the NAG1 cDNA coding for glucosamine-6-phosphate deaminase from Candida albicans. J Biol Chem 268:9206–9214PubMedGoogle Scholar
  108. Netea MG, Brown GD, Kullberg BJ, Gow NAR (2008) An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol 6:67–78PubMedGoogle Scholar
  109. Netea MG, Gow NAR, Munro CA, Bates S, Collins C, Ferwerda G, Hobson RP, Bertram G, Hughes HB, Jansen T, Jacobs L, Buurman ET, Gijzen K, Williams DL, Torensma R, McKinnon A, MacCallum DM, Odds FC, Van Der Meer JWM, Brown AJP, Kullberg BJ (2006) Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 116:1642–1650PubMedCentralPubMedGoogle Scholar
  110. Nett J, Lincoln L, Marchillo K, Massey R, Holoyda K, Hoff B, VanHandel M, Andes D (2007) Putative role of beta-1,3 glucans in Candida albicans biofilm resistance. Antimicrob Agents Chemother 51:510–520PubMedCentralPubMedGoogle Scholar
  111. Nett JE, Crawford K, Marchillo K, Andes DR (2010) Role of Fks1p and matrix glucan in Candida albicans biofilm resistance to an echinocandin, pyrimidine, and polyene. Antimicrob Agents Chemother 54:3505–3508PubMedCentralPubMedGoogle Scholar
  112. Odds FC (ed) (1988) Candida and Candidosis 2nd edn. Bailliere Tindall, LondonGoogle Scholar
  113. Onishi A, Sugiyama D, Kogata Y, Saegusa J, Sugimoto T, Kawano S, Morinobu A, Nishimura K, Kumagaia S (2012) Diagnostic accuracy of serum 1,3-ß-D-glucan for Pneumocystis jiroveci pneumonia, invasive candidiasis, and invasive aspergillosis: systematic review and meta-analysis. J Clin Microbiol 50:7–15PubMedCentralPubMedGoogle Scholar
  114. Ostrosky-Zeichner L (2012) Invasive mycoses: diagnostic challenges. Am J Med 125:S14–S24PubMedGoogle Scholar
  115. Pardini G, De Groot PWJ, Coste AT, Karababa M, Klis FM, De Koster CG, Sanglard D (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 281:40399–40411PubMedGoogle Scholar
  116. Phan QT, Myers CL, Fu Y, Sheppard DC, Yeaman MR, Welch WH, Ibrahim AS, Edwards JE Jr, Filler SG (2007) Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 5:0543–0557Google Scholar
  117. Plaine A, Walker L, Da Costa G, Mora-Montes HM, McKinnon A, Gow NA, Gaillardin C, Munro CA, Richard ML (2008) Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol 45:1404–1414PubMedCentralPubMedGoogle Scholar
  118. Plumbridge JA (1989) Sequence of the nagBACD operon in Escherichia coli K12 and pattern of transcription within the nag regulon. Mol Microbiol 3:505–515PubMedGoogle Scholar
  119. Popolo L, Gualtieri T, Ragni E (2001) The yeast cell-wall salvage pathway. Med Mycol 39:111–121PubMedGoogle Scholar
  120. Prill SK, Klinkert B, Timpel C, Gale CA, Schroppel K, Ernst JF (2005) PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol Microbiol 55:546–560PubMedGoogle Scholar
  121. Qadota H, Python CP, Inoue SB, Arisawa M, Anraku Y, Zheng Y, Watanabe T, Levin DE, Ohya Y (1996) Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-β-glucan synthase. Science 272:279–281PubMedGoogle Scholar
  122. Ram AFJ, Arentshorst M, Damveld RA, vanKuyk PA, Klis FM, van den Hondel CAMJJ (2004) The cell wall stress response in Aspergillus niger involves increased expression of the glutamine: fructose-6-phosphate amidotransferase-encoding gene (gfaA) and increased deposition of chitin in the cell wall. Microbiology 150:3315–3326PubMedGoogle Scholar
  123. Rao KH, Ghosh S, Natarajan K, Datta A (2013) N-acetylglucosamine kinase, HXK1 is involved in morphogenetic transition and metabolic gene expression in Candida albicans. PLoS ONE 8:e53638PubMedCentralPubMedGoogle Scholar
  124. Richard ML, Plaine A (2007) Comprehensive analysis of glycosylphosphatidylinositol-anchored proteins in Candida albicans. Eukaryot Cell 6:119–133PubMedCentralPubMedGoogle Scholar
  125. Rubin-Bejerano I, Abeijon C, Magnelli P, Grisafi P, Fink GR (2007) Phagocytosis by human neutrophils is stimulated by a unique fungal cell wall component. Cell Host Microbe 2:55–67PubMedCentralPubMedGoogle Scholar
  126. Rubin-Bejerano I, Fraser I, Grisafi P, Fink GR (2003) Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans. Proc Natl Acad Sci USA 100:11007–11012PubMedCentralPubMedGoogle Scholar
  127. Sandai D, Yin Z, Selway L, Stead D, Walker J, Leach MD, Bohovych I, Ene IV, Kastora S, Budge S, Munro CA, Odds FC, Gow NA, Brown AJ (2012) The evolutionary rewiring of ubiquitination targets has reprogrammed the regulation of carbon assimilation in the pathogenic yeast Candida albicans. MBio 3:e00495–12PubMedCentralPubMedGoogle Scholar
  128. Sardi JCO, Scorzoni L, Bernardi T, Fusco-Almeida AM, Mendes Giannini MJS (2013) Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol 62:10–24Google Scholar
  129. Sengupta M, Datta A (2003) Two membrane proteins located in the Nag regulon of Candida albicans confer multidrug resistance. Biochem Biophys Res Commun 301:1099–1108PubMedGoogle Scholar
  130. Shepardson KM, Cramer RA (2013) Fungal cell wall dynamics and infection site microenvironments: signal integration and infection outcome. Curr Opin Microbiol S1369–5274(13):00035. doi: 10.1016/j.mib.2013.03.003 Google Scholar
  131. Shibata N, Kobayashi H, Suzuki S (2012) Immunochemistry of pathogenic yeast, Candida species, focusing on Mannan. Proc Jpn Acad Ser B Phys Biol Sci 88:250–265PubMedCentralPubMedGoogle Scholar
  132. Singh B, Datta A (1979) Induction of N-acetylglucosamine-catabolic pathway in spheroplasts of Candida albicans. Biochem J 178:427–431PubMedCentralPubMedGoogle Scholar
  133. Singh P, Ghosh S, Datta A (2001) Attenuation of virulence and changes in morphology in Candida albicans by disruption of the N-acetylglucosamine catabolic pathway. Infect Immun 69:7898–7903PubMedCentralPubMedGoogle Scholar
  134. Singh V, Satheesh SV, Raghavendra ML, Sadhale PP (2007) The key enzyme in galactose metabolism, UDP-galactose-4-epimerase, affects cell-wall integrity and morphology in Candida albicans even in the absence of galactose. Fungal Genet Biol 44:563–574PubMedGoogle Scholar
  135. Smith RJ, Milewski S, Brown AJP, Gooday GW (1996) Isolation and characterization of the GFA1 gene encoding the glutamine: fructose-6-phosphate amidotransferase of Candida albicans. J Bacteriol 178:2320–2327PubMedCentralPubMedGoogle Scholar
  136. Smith TL, Rutter J (2007) Regulation of glucose partitioning by PAS Kinase and Ugp1 phosphorylation. Mol Cell 26:491–499PubMedGoogle Scholar
  137. Sohn K, Urban C, Brunner H, Rupp S (2003) EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol Microbiol 47:89–102PubMedGoogle Scholar
  138. Soll DR (2009) Why does Candida albicans switch? FEMS Yeast Res 9:973–989PubMedGoogle Scholar
  139. Spellberg B, Ibrahim AS, Lin L, Avanesian V, Fu Y, Lipke P, Otoo H, Ho T, Edwards JE Jr (2008) Antibody titer threshold predicts anti-candidal vaccine efficacy even though the mechanism of protection is induction of cell-mediated immunity. J Infect Dis 197:967–971PubMedCentralPubMedGoogle Scholar
  140. Staab JF, Bradway SD, Fidel PL, Sundstrom P (1999) Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283:1535–1538PubMedGoogle Scholar
  141. Stoldt VR, Sonneborn A, Leuker CE, Ernst JF (1997) Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J 16:1982–1991PubMedCentralPubMedGoogle Scholar
  142. Sudbery PE (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9:737–748PubMedGoogle Scholar
  143. Taff HT, Nett JE, Zarnowski R, Ross KM, Sanchez H, Cain MT, Hamaker J, Mitchell AP, Andes DR (2012) A Candida biofilm-induced pathway for matrix glucan delivery: implications for drug resistance. PLoS Pathog 8:e1002848PubMedCentralPubMedGoogle Scholar
  144. Ueno K, Okawara A, Yamagoe S, Naka T, Umeyama T, Utena-Abe Y, Tarumoto N, Niimi M, Ohno H, Doe M, Fujiwara N, Kinjo Y, Miyazaki Y (2013) The mannan of Candida albicans lacking beta-1,2-linked oligomannosides increases the production of inflammatory cytokines by dendritic cells. Med Mycol 51:385–395PubMedGoogle Scholar
  145. Umeyama T, Kaneko A, Watanabe H, Hirai A, Uehara Y, Niimi M, Azuma M (2006) Deletion of the CaBIG1 gene reduces β-1,6-glucan synthesis, filamentation, adhesion, and virulence in Candida albicans. Infect Immun 74:2373–2381PubMedCentralPubMedGoogle Scholar
  146. Vautier S, MacCallum DM, Brown GD (2012) C-type lectin receptors and cytokines in fungal immunity. Cytokine 58:89–99PubMedGoogle Scholar
  147. Vega K, Kalkum M (2012) Chitin, chitinase responses, and invasive fungal infections. Int J Microbiol 2012:920459PubMedCentralPubMedGoogle Scholar
  148. Walker LA, MacCallum DM, Bertram G, Gow NAR, Odds FC, Brown AJP (2009) Genome-wide analysis of Candida albicans gene expression patterns during infection of the mammalian kidney. Fungal Genet Biol 46:210–219PubMedCentralPubMedGoogle Scholar
  149. Walker LA, Munro CA, de Bruijn I, Lenardon MD, McKinnon A, Gow NA (2008) Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 4:e1000040PubMedCentralPubMedGoogle Scholar
  150. Wendland J, Schaub Y, Walther A (2009) N-acetylglucosamine utilization by Saccharomyces cerevisiae based on expression of Candida albicans NAG genes. Appl Environ Microbiol 75:5840–5845PubMedCentralPubMedGoogle Scholar
  151. Wheeler RT, Kombe D, Agarwala SD, Fink GR (2008) Dynamic, morphotype-specific Candida albicans β-glucan exposure during infection and drug treatment. PLoS Pathog 4:e1000227PubMedCentralPubMedGoogle Scholar
  152. Wheeler RT, Fink GR (2006) A drug-sensitive genetic network masks fungi from the immune system. PLoS Pathog 2:e35PubMedCentralPubMedGoogle Scholar
  153. Yamada-Okabe T, Yamada-Okabe H (2002) Characterization of the CaNAG3, CaNAG4, and CaNAG6 genes of the pathogenic fungus Candida albicans: possible involvement of these genes in the susceptibilities of cytotoxic agents. FEMS Microbiol Lett 212:15–21PubMedGoogle Scholar
  154. Yamada-Okabe T, Sakamori Y, Mio T, Yamada-Okabe H (2001) Identification and characterization of the genes for N-acetylglucosamine kinase and N-acetylglucosamine-phosphate deacetylase in the pathogenic fungus Candida albicans. European J Biochem 268:2498–2505Google Scholar
  155. Zhao X, Oh S-, Cheng G, Green CB, Nuessen JA, Yeater K, Leng RP, Brown AJP, Hoyer LL (2004) ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology 150:2415–2428PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Institute of Medical SciencesUniversity of AberdeenAberdeenUK

Personalised recommendations