Niche-specific requirement for hyphal wall protein 1 in virulence of Candida albicans

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Staab, Janet F ^a   Datta, Kausik ^a   Rhee, Peter ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; HYPHAL WALL PROTEIN 1; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE BINDING PROTEIN; HWP1 PROTEIN, CANDIDA ALBICANS; MEMBRANE PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; TRANSGLUTAMINASE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; BIOFILM; BLOOD FLOW; C57BL 6 MOUSE; CANDIDA ALBICANS; CONTROLLED STUDY; FEMALE; FUNGAL VIRULENCE; GENE LOCUS; HOST PATHOGEN INTERACTION; INTESTINE; INVASIVE CANDIDIASIS; MOUSE; MOUSE MODEL; MOUSE STRAIN; MOUTH MUCOSA; NONHUMAN; NUCLEOTIDE SEQUENCE; OROPHARYNX CANDIDIASIS; WILD TYPE; ANIMAL; C57BL MOUSE; CANDIDIASIS; CELL WALL; CHEMISTRY; DEFICIENCY; ENZYMOLOGY; ESOPHAGUS; FUNGUS HYPHAE; GENE EXPRESSION REGULATION; GENETICS; HOST RANGE; METABOLISM; MICROBIOLOGY; MORTALITY; MOUTH; PATHOGENICITY; SURVIVAL; THRUSH; VIRULENCE;

ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; CANDIDIASIS, ORAL; CELL WALL; ESOPHAGUS; FEMALE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GTP-BINDING PROTEINS; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; HYPHAE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MOUTH; SURVIVAL ANALYSIS; TRANSGLUTAMINASES; VIRULENCE;

EID: 84892613008     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080842     Document Type: Article

References (87)

1. Staab JF, Bradway SD, Fidel PL, Sundstrom P (1999) Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283: 1535-1538. doi:10.1126/science.283.5407.1535. PubMed: 10066176.
2. Coleman DA, Oh SH, Zhao X, Zhao H, Hutchins JT et al. (2009) Monoclonal antibodies specific for Candida albicans Als3 that immunolabel fungal cells in vitro and in vivo and block adhesion to host surfaces. J Microbiol Methods 78: 71-78. doi:10.1016/j.mimet.2009.05.002. PubMed: 19427882.
3. Fanning S, Xu W, Solis N, Woolford CA, Filler SG et al. (2012) Divergent targets of Candida albicans biofilm regulator Bcr1 In vitro and In vivo. Eukaryot Cell 11: 896-904. doi:10.1128/EC.00103-12. PubMed: 22544909.
4. Fu Y, Rieg G, Fonzi WA, Belanger PH, Edwards JE Jr. et al. (1998) Expression of the Candida albicans gene ALS1 in Saccharomyces cerevisiae induces adherence to endothelial and epithelial cells. Infect Immun 66: 1783-1786. PubMed: 9529114.
5. Oh SH, Cheng G, Nuessen JA, Jajko R, Yeater KM et al. (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: 673-681. doi:10.1099/mic.0.27680-0. PubMed: 15758214.
6. Zhao X, Oh SH, Cheng G, Green CB, Nuessen JA et al. (2004) ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology 150: 2415-2428. doi:10.1099/mic.0.26943-0. PubMed: 15256583.
7. Ponniah G, Rollenhagen C, Bahn YS, Staab JF, Sundstrom P (2007) State of differentiation defines buccal epithelial cell affinity for crosslinking to Candida albicans Hwp1. J Oral Pathol Med 36: 456-467. doi:10.1111/j.1600-0714. 2007.00565.x. PubMed: 17686003.
8. Staab JF, Bahn YS, Tai CH, Cook PF, Sundstrom P (2004) Expression of transglutaminase substrate activity on Candida albicans germ tubes through a coiled, disulfide-bonded N-terminal domain of Hwp1 requires C-terminal glycosylphosphatidylinositol modification. J Biol Chem 279: 40737-40747. doi:10.1074/jbc.M406005200. PubMed: 15262971.
9. Lorand L, Conrad SM (1984) Transglutaminases. Mol Cell Biochem 58: 9-35. doi:10.1007/BF00240602. PubMed: 6143256.
10. Lorand L, Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4: 140-156. doi:10.1038/nrm1014. PubMed: 12563291.
11. Nemes Z, Steinert PM (1999) Bricks and mortar of the epidermal barrier. Exp Mol Med 31: 5-19. doi:10.1038/emm.1999.2. PubMed: 10231017.
12. Steinert PM, Chung SI, Kim SY (1996) Inactive zymogen and highly active proteolytically processed membrane-bound forms of the transglutaminase 1 enzyme in human epidermal keratinocytes. Biochem Biophys Res Commun 221: 101-106. doi:10.1006/bbrc.1996.0552. PubMed: 8660317.
13. Sundstrom P, Balish E, Allen CM (2002) Essential role of the Candida albicans transglutaminase substrate, hyphal wall protein 1, in lethal oroesophageal candidiasis in immunodeficient mice. J Infect Dis 185: 521-530. doi:10.1086/338836. PubMed: 11865405.
14. Matsuki M, Yamashita F, Ishida-Yamamoto A, Yamada K, Kinoshita C et al. (1998) Defective stratum corneum and early neonatal death in mice lacking the gene for transglutaminase 1 (keratinocyte transglutaminase). Proc Natl Acad Sci U S A 95: 1044-1049. doi:10.1073/pnas.95.3.1044. PubMed: 9448282.
15. Sundstrom P, Cutler JE, Staab JF (2002) Reevaluation of the role of HWP1 in systemic candidiasis by use of Candida albicans strains with selectable marker URA3 targeted to the ENO1 locus. Infect Immun 70: 3281-3283. doi:10.1128/IAI.70.6.3281-3283.2002. PubMed: 12011025.
16. Itoh M, Kawamoto T, Tatsukawa H, Kojima S, Yamanishi K et al. (2011) In situ detection of active transglutaminases for keratinocyte type (TGase 1) and tissue type (TGase 2) using fluorescence-labeled highly reactive substrate peptides. J Histochem Cytochem Off J Histochem Soc 59: 180-187. doi:10.1369/jhc.2010.957225. PubMed: 20876521.
17. Reuss O, Vik A, Kolter R, Morschhäuser J (2004) The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119-127. doi:10.1016/j.gene.2004.06.021. PubMed: 15474295.
18. Brand A, MacCallum DM, Brown AJ, Gow NA, Odds FC (2004) Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot Cell 3: 900-909. doi:10.1128/EC.3.4.900-909.2004. PubMed: 15302823.
19. Cheng S, Nguyen MH, Zhang Z, Jia H, Handfield M et al. (2003) Evaluation of the roles of four Candida albicans genes in virulence by using gene disruption strains that express URA3 from the native locus. Infect Immun 71: 6101-6103. doi:10.1128/IAI.71.10.6101-6103.2003. PubMed: 14500538.
20. Staab JF, Sundstrom P (2003) URA3 as a selectable marker for disruption and virulence assessment of Candida albicans genes. Trends Microbiol 11: 69-73. doi:10.1016/S0966-842X(02)00029-X. PubMed: 12598128.
21. Ene IV, Bennett RJ (2009) Hwp1 and related adhesins contribute to both mating and biofilm formation in Candida albicans. Eukaryot Cell 8: 1909-1913. doi:10.1128/EC.00245-09. PubMed: 19837954.
22. Nobile CJ, Nett JE, Andes DR, Mitchell AP (2006) Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot Cell 5: 1604-1610. doi:10.1128/EC.00194-06. PubMed: 17030992.
23. Solis NV, Filler SG (2012) Mouse model of oropharyngeal candidiasis. Nat Protoc 7: 637-642. doi:10.1038/nprot.2012.011. PubMed: 22402633.
24. Koh AY, Köhler JR, Coggshall KT, Van Rooijen N, Pier GB (2008) Mucosal damage and neutropenia are required for Candida albicans dissemination. PLOS Pathog 4: e35. doi:10.1371/journal.ppat.0040035. PubMed: 18282097.
25. Maccallum DM (2012) Hosting infection: experimental models to assay Candida virulence. International journal of microbiology 2012: 363764. PubMed: 22235206
26. Spellberg B (2008) Novel insights into disseminated candidiasis: pathogenesis research and clinical experience converge. PLOS Pathog 4: e38. doi:10.1371/journal.ppat.0040038. PubMed: 18282100.
27. Fonzi WA, Irwin MY (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717-728. PubMed: 8349105.
28. Gillum AM, Tsay EY, Kirsch DR (1984) Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Molecular General Genet MGG 198: 179-182. doi:10.1007/BF00328721.
29. Sharkey LL, Liao WL, Ghosh AK, Fonzi WA (2005) Flanking direct repeats of hisG alter URA3 marker expression at the HWP1 locus of Candida albicans. Microbiology 151: 1061-1071. doi:10.1099/mic.0.27487-0. PubMed: 15817775.
30. Rose MD, Winston F, Hieter P (1990) Method in yeast genetics: a laboratory course manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Publishing.
31. Morschhäuser J, Michel S, Staib P (1999) Sequential gene disruption in Candida albicans by FLP-mediated site-specific recombination. Mol Microbiol 32: 547-556. doi:10.1046/j.1365-2958.1999.01393.x. PubMed: 10320577.
32. Staab JF, Sundstrom P (1998) Genetic organization and sequence analysis of the hypha-specific cell wall protein gene HWP1 of Candida albicans. Yeast 14: 681-686. doi:10.1002/(SICI)1097-0061(199805)14:7. PubMed: 9639315.
33. Schmitt ME, Brown TA, Trumpower BL (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res 18: 3091-3092. doi:10.1093/nar/18.10.3091. PubMed: 2190191.
34. De Laurenzi V, Melino G (2001) Gene disruption of tissue transglutaminase. Mol Cell Biol 21: 148-155. doi:10.1128/MCB.21.1.148-155.2001. PubMed: 11113189.
35. MacCallum DM, Odds FC (2005) Temporal events in the intravenous challenge model for experimental Candida albicans infections in female mice. Mycoses 48: 151-161. doi:10.1111/j.1439-0507.2005.01121.x. PubMed: 15842329.
36. Wilson RB, Davis D, Mitchell AP (1999) Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J Bacteriol 181: 1868-1874. PubMed: 10074081.
37. Ahmad A, Kabir MA, Kravets A, Andaluz E, Larriba G et al. (2008) Chromosome instability and unusual features of some widely used strains of Candida albicans. Yeast 25: 433-448. doi:10.1002/yea.1597. PubMed: 18509849.
38. Arbour M, Epp E, Hogues H, Sellam A, Lacroix C et al. (2009) Widespread occurrence of chromosomal aneuploidy following the routine production of Candida albicans mutants. FEMS Yeast Res 9: 1070-1077. doi:10.1111/j.1567-1364.2009. 00563.x. PubMed: 19732157.
39. Selmecki A, Bergmann S, Berman J (2005) Comparative genome hybridization reveals widespread aneuploidy in Candida albicans laboratory strains. Mol Microbiol 55: 1553-1565. doi:10.1111/j.1365-2958.2005.04492.x. PubMed: 15720560.
40. Chen X, Magee BB, Dawson D, Magee PT, Kumamoto CA (2004) Chromosome 1 trisomy compromises the virulence of Candida albicans. Mol Microbiol 51: 551-565. doi:10.1046/j.1365-2958.2003.03852.x. PubMed: 14756793.
41. Ganguly S, Mitchell AP (2011) Mucosal biofilms of Candida albicans. Curr Opin Microbiol 14: 380-385. doi:10.1016/j.mib.2011.06.001. PubMed: 21741878.
42. Nobile CJ, Schneider HA, Nett JE, Sheppard DC, Filler SG et al. (2008) Complementary adhesin function in C. albicans biofilm formation. Curr Biol CB 18: 1017-1024. doi:10.1016/j.cub.2008.09.017.
43. Ramage G, Saville SP, Wickes BL, López-Ribot JL (2002) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68: 5459-5463. doi:10.1128/AEM.68.11.5459-5463.2002. PubMed: 12406738.
44. Kamai Y, Kubota M, Hosokawa T, Fukuoka T, Filler SG (2001) New model of oropharyngeal candidiasis in mice. Antimicrob Agents Chemother 45: 3195-3197. doi:10.1128/AAC.45.11.3195-3197.2001. PubMed: 11600377.
45. Naglik JR, Fidel PL Jr., Odds FC (2008) Animal models of mucosal Candida infection. FEMS Microbiol Lett 283: 129-139. doi:10.1111/j.1574-6968.2008.01160. x. PubMed: 18422625.
46. Costa AC, Pereira CA, Junqueira JC, Jorge AO (2013) Recent mouse and rat methods for the study of experimental oral candidiasis. Virulence 4.
47. Balish E (2009) A URA3 null mutant of Candida albicans (CAI-4) causes oro-oesophageal and gastric candidiasis and is lethal for gnotobiotic, transgenic mice (Tgepsilon26) that are deficient in both natural killer and T cells. J Med Microbiol 58: 290-295. doi:10.1099/jmm.0.004846-0. PubMed: 19208876.
48. Mattiuzzi G, Ostrosky-Zeichner L (2010) Fungal and Parasitic Infections. In: M Kleinberg. Comtemporay Hematology: Managing infections in patients with hematological malignancies. New York: Humana Press.
49. Falasca L, Farrace MG, Rinaldi A, Tuosto L, Melino G et al. (2008) Transglutaminase type II is involved in the pathogenesis of endotoxic shock. J Immunol 180: 2616-2624. PubMed: 18250473.
50. Falasca L, Iadevaia V, Ciccosanti F, Melino G, Serafino A et al. (2005) Transglutaminase type II is a key element in the regulation of the antiinflammatory response elicited by apoptotic cell engulfment. J Immunol 174: 7330-7340. PubMed: 15905580.
51. Kim SY (2006) Transglutaminase 2 in inflammation. Front Biosci J Virtual Libr 11: 3026-3035. doi:10.2741/2030.
52. Mohan K, Pinto D, Issekutz TB (2003) Identification of tissue transglutaminase as a novel molecule involved in human CD8+ T cell transendothelial migration. J Immunol 171: 3179-3186. PubMed: 12960346.
53. Park KS, Kim DS, Ko C, Lee SJ, Oh SH et al. (2011) TNF-alpha mediated NF-kappaB activation is constantly extended by transglutaminase 2. Front Biosci 3: 341-354. doi:10.2741/s155. PubMed: 21196314.
54. Romani L (2001) Animal models for candidiasis. Current Protocols in Immunology. John Wiley & Sons, Inc. p. 19.16.11-19.16.16.
55. Hector RF, Domer JE, Carrow EW (1982) Immune responses to Candida albicans in genetically distinct mice. Infect Immun 38: 1020-1028. PubMed: 6759403.
56. Ashman RB, Fulurija A, Papadimitriou JM (1996) Strain-dependent differences in host response to Candida albicans infection in mice are related to organ susceptibility and infectious load. Infect Immun 64: 1866-1869. PubMed: 8613406.
57. Ashman RB, Papadimitriou JM (1987) Murine candidiasis. Pathogenesis and host responses in genetically distinct inbred mice. Immunol Cell Biol 65 (2): 163-171. doi:10.1038/icb.1987.18.
58. Radovanovic I, Mullick A, Gros P (2011) Genetic control of susceptibility to infection with Candida albicans in mice. PLOS ONE 6: e18957. doi:10.1371/journal.pone.0018957. PubMed: 21533108.
59. Carvalho A, Giovannini G, De Luca A, D'Angelo C, Casagrande A et al. (2012) Dectin-1 isoforms contribute to distinct Th1/Th17 cell activation in mucosal candidiasis. Cell Mol Immunol 9: 276-286. doi:10.1038/cmi.2012.1. PubMed: 22543832.
60. Mosci P, Pietrella D, Ricci G, Pandey N, Monari C et al. (2013) Mouse strain-dependent differences in estrogen sensitivity during vaginal candidiasis. Mycopathologia 175: 1-11. doi:10.1007/s11046-012-9589-9. PubMed: 23054331.
61. Schofield DA, Westwater C, Balish E (2005) Divergent chemokine, cytokine and beta-defensin responses to gastric candidiasis in immunocompetent C57BL/6 and BALB/c mice. J Med Microbiol 54: 87-92. doi:10.1099/jmm.0.45755-0. PubMed: 15591261.
62. Wellington M, Dolan K, Krysan DJ (2009) Live Candida albicans suppresses production of reactive oxygen species in phagocytes. Infect Immun 77: 405-413. doi:10.1128/IAI.00860-08. PubMed: 18981256.
63. Zou Y, Zhang H, Li H, Chen H, Song W et al. (2012) Strain-dependent production of interleukin-17/interferon-gamma and matrix remodeling-associated genes in experimental Candida albicans keratitis. Mol Vis 18: 1215-1225. PubMed: 22665968.
64. Chibana H, Uno J, Cho T, Mikami Y (2005) Mutation in IRO1 tightly linked with URA3 gene reduces virulence of Candida albicans. Microbiol Immunol 49: 937-939. PubMed: 16237272.
65. Lay J, Henry LK, Clifford J, Koltin Y, Bulawa CE et al. (1998) Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect Immun 66: 5301-5306. PubMed: 9784536.
66. Correia A, Lermann U, Teixeira L, Cerca F, Botelho S et al. (2010) Limited role of secreted aspartyl proteinases Sap1 to Sap6 in Candida albicans virulence and host immune response in murine hematogenously disseminated candidiasis. Infect Immun 78: 4839-4849. doi:10.1128/IAI.00248-10. PubMed: 20679440.
67. Martin R, Albrecht-Eckardt D, Brunke S, Hube B, Hünniger K et al. (2013) A core filamentation response network in Candida albicans is restricted to eight genes. PLOS ONE 8: e58613. doi:10.1371/journal.pone.0058613. PubMed: 23516516.
68. Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F et al. (2006) Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLOS Pathog 2: e63. doi:10.1371/journal.ppat.0020063. PubMed: 16839200.
69. Braun BR, Head WS, Wang MX, Johnson AD (2000) Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156: 31-44. PubMed: 10978273.
70. Cleary IA, Reinhard SM, Miller CL, Murdoch C, Thornhill MH et al. (2011) Candida albicans adhesin Als3p is dispensable for virulence in the mouse model of disseminated candidiasis. Microbiology 157: 1806-1815. doi:10.1099/mic.0. 046326-0. PubMed: 21436220.
71. Park YN, Daniels KJ, Pujol C, Srikantha T, Soll DR (2013) Candida albicans forms a specialized "sexual" as well As " pathogenic" biofilm. Eukaryot Cell, 12: 1120-31. PubMed: 23771904.
72. Padovan AC, Chaves GM, Colombo AL, Briones MR (2009) A novel allele of HWP1, isolated from a clinical strain of Candida albicans with defective hyphal growth and biofilm formation, has deletions of Gln/Pro and Ser/Thr repeats involved in cellular adhesion. Med Mycol Off Publ International Society For Human Animal Mycology 47: 824-835. doi:10.3109/13693780802669574. PubMed: 19184714.
73. White SJ, Rosenbach A, Lephart P, Nguyen D, Benjamin A et al. (2007) Self-regulation of Candida albicans population size during GI colonization. PLOS Pathog 3: e184. doi:10.1371/journal.ppat.0030184. PubMed: 18069889.
74. Rosenbach A, Dignard D, Pierce JV, Whiteway M, Kumamoto CA (2010) Adaptations of Candida albicans for growth in the mammalian intestinal tract. Eukaryot Cell 9: 1075-1086. doi:10.1128/EC.00034-10. PubMed: 20435697.
75. Naglik JR, Fostira F, Ruprai J, Staab JF, Challacombe SJ et al. (2006) Candida albicans HWP1 gene expression and host antibody responses in colonization and disease. J Med Microbiol 55: 1323-1327. doi:10.1099/jmm.0. 46737-0. PubMed: 17005778.
76. Braun BR, Johnson AD (2000) TUP1, CPH1 and EFG1 make independent contributions to filamentation in Candida albicans. Genetics 155: 57-67. PubMed: 10790384.
77. Lane S, Birse C, Zhou S, Matson R, Liu H (2001) DNA array studies demonstrate convergent regulation of virulence factors by Cph1, Cph2, and Efg1 in Candida albicans. J Biol Chem 276: 48988-48996. doi:10.1074/jbc.M104484200. PubMed: 11595734.
78. Hube B, Hess D, Baker CA, Schaller M, Schäfer W et al. (2001) The role and relevance of phospholipase D1 during growth and dimorphism of Candida albicans. Microbiology 147: 879-889. PubMed: 11283284.
79. Jackson BE, Wilhelmus KR, Hube B (2007) The role of secreted aspartyl proteinases in Candida albicans keratitis. Invest Ophthalmol Vis Sci 48: 3559-3565. doi:10.1167/iovs.07-0114. PubMed: 17652724.
80. Lorenz MC, Fink GR (2001) The glyoxylate cycle is required for fungal virulence. Nature 412: 83-86. doi:10.1038/35083594. PubMed: 11452311.
81. Naglik JR, Moyes D, Makwana J, Kanzaria P, Tsichlaki E et al. (2008) Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology 154: 3266-3280. doi:10.1099/mic.0.2008/022293-0. PubMed: 18957581.
82. Naglik JR, Rodgers CA, Shirlaw PJ, Dobbie JL, Fernandes-Naglik LL et al. (2003) Differential expression of Candida albicans secreted aspartyl proteinase and phospholipase B genes in humans correlates with active oral and vaginal infections. J Infect Dis 188: 469-479. doi:10.1086/376536. PubMed: 12870130.
83. Samaranayake YH, Dassanayake RS, Cheung BP, Jayatilake JA, Yeung KW et al. (2006) Differential phospholipase gene expression by Candida albicans in artificial media and cultured human oral epithelium. APMIS Acta Pathol Microbiol Immunol Scand 114: 857-866. PubMed: 17207086.
84. Schaller M, Schackert C, Korting HC, Januschke E, Hube B (2000) Invasion of Candida albicans correlates with expression of secreted aspartic proteinases during experimental infection of human epidermis. J Invest Dermatol 114: 712-717. doi:10.1046/j.1523-1747.2000.00935.x. PubMed: 10733678.
85. Barelle CJ, Priest CL, Maccallum DM, Gow NA, Odds FC et al. (2006) Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell Microbiol 8: 961-971. doi:10.1111/j.1462-5822.2005.00676.x. PubMed: 16681837.
86. Staib P, Kretschmar M, Nichterlein T, Hof H, Morschhäuser J (2000) Differential activation of a Candida albicans virulence gene family during infection. Proc Natl Acad Sci U S A 97: 6102-6107. doi:10.1073/pnas.110031497. PubMed: 10811913.
87. Schofield DA, Westwater C, Warner T, Nicholas PJ, Paulling EE et al. (2003) Hydrolytic gene expression during oroesophageal and gastric candidiasis in immunocompetent and immunodeficient gnotobiotic mice. J Infect Dis 188: 591-599. doi:10.1086/377182. PubMed: 12898449.