Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen

Cellular Microbiology

Volumn 14, Issue 9, 2012, Pages 1319-1335

  Ene, Iuliana V ^a   Adya, Ashok K ^b   Wehmeier, Silvia ^a   Brand, Alexandra C ^a   Maccallum, Donna M ^a   Gow, Neil A R ^a   Brown, Alistair J P ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF ABERTAY DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMPHOTERICIN B; AMPHOTERICIN B LIPID COMPLEX; CASPOFUNGIN; CHITIN; FRUCTOSE; FUNGAL PROTEIN; GALACTOSE; GLUCAN; GLUCOSE; LACTIC ACID; MANNAN; MICONAZOLE; OLEIC ACID; PROTEIN HOG1; PROTEIN MKC1; PYRUVIC ACID; SORBITOL; TUNICAMYCIN; UNCLASSIFIED DRUG;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; ATOMIC FORCE MICROSCOPY; CANDIDA; CANDIDA ALBICANS; CANDIDA DUBLINIENSIS; CANDIDA GLABRATA; CANDIDA GUILLERMONDII; CANDIDA KRUSEI; CANDIDA TROPICALIS; CARBON SOURCE; CELL ADHESION; CELL ULTRASTRUCTURE; CELL VOLUME; CELL WALL; CELLULAR STRESS RESPONSE; CLAVISPORA LUSITANIAE; CONTROLLED STUDY; ELASTICITY; FEMALE; FUNGAL CELL; FUNGAL CELL WALL; FUNGAL VIRULENCE; FUNGUS GROWTH; HOST PATHOGEN INTERACTION; HYDROPHOBICITY; HYPEROSMOTIC STRESS; INTRACELLULAR SIGNALING; INVASIVE CANDIDIASIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; VAGINA CANDIDIASIS; WESTERN BLOTTING;

CANDIDA ALBICANS; CARBOHYDRATE METABOLISM; CARBON; CELL WALL; COLONY COUNT, MICROBIAL; CULTURE MEDIA; DRUG RESISTANCE, FUNGAL; HOST-PATHOGEN INTERACTIONS; MICROBIAL VIABILITY; STRESS, PHYSIOLOGICAL; VIRULENCE;

CANDIDA; CANDIDA ALBICANS;

EID: 84865309913     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01813.x     Document Type: Article

References (76)

1. Adya, A.K., and Canetta, E. (2011) Atomic force microscopic investigation of commercial pressure sensitive adhesives for forensic analysis. Forensic Sci Int 210: 16-25.
2. Aguilar-Uscanga, B., and François, J.M. (2003) A study of the yeast cell wall composition and structure in response to growth conditions and mode of cultivation. Lett Appl Microbiol 37: 268-274.
3. Alonso-Monge, R., Navarro-García, F., Román, E., Negredo, A.I., Eisman, B., Nombela, C., and Pla, J. (2003) The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans Eukaryot Cell 2: 351-361.
4. Amaral, P.F., Lehocky, M., Barros-Timmons, A.M., Rocha-Leão, M.H., Coelho, M.A., and Coutinho, J.A. (2006) Cell surface characterization of Yarrowia lipolytica IMUFRJ 50682. Yeast 23: 867-877.
5. Askew, C., Sellam, A., Epp, E., Hogues, H., Mullick, A., Nantel, A., and Whiteway, M. (2009) Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans PLoS Pathog 5: e1000612.
6. Bain, J.M., Stubberfield, C., and Gow, N.A. (2001) Ura-status-dependent adhesion of Candida albicans mutants. FEMS Microbiol Lett 204: 323-328.
7. Barelle, C.J., Priest, C.L., MacCallum, D.M., Gow, N.A., Odds, F.C., and Brown, A.J. (2006) Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell Microbiol 8: 961-971.
8. Bartizal, C., and Odds, F.C. (2003) Influences of methodological variables on susceptibility testing of caspofungin against Candida species and Aspergillus fumigatus Antimicrob Agents Chemother 47: 2100-2107.
9. Binning, G., Quate, C.F., and Gerber, C. (1986) Atomic force microscopy. Phys Rev Lett 56: 930-933.
10. Blankenship, J.R., Fanning, S., Hamaker, J.J., and Mitchell, A.P. (2010) An extensive circuitry for cell wall regulation in Candida albicans PLoS Pathog 6: e1000752.
11. Brown, A.J.P., Odds, F.C., and Gow, N.A. (2007) Infection-related gene expression in Candida albicans Curr Opin Microbiol 10: 307-313.
12. Buchalter, S.E., Crain, M.R., and Kreisberg, R. (1989) Regulation of lactate metabolism in vivo. Diabetes Metab Rev 5: 379-391.
13. Calderone, R.A. (2002) Candida and Candidiasis, 1st edn. Washington DC: ASM Press.
14. Calderone, R.A., and Clancy, C.J. (2011) Candida and Candidiasis, 2nd edn. Washington DC: ASM Press.
15. Cheetham, J., Smith, D.A., Dantas, A., Doris, K.S., Patterson, M.J., Bruce, C.R., and Quinn, J. (2007) A single MAPKKK regulates the Hog1 MAPK pathway in the pathogenic fungus Candida albicans Mol Biol Cell 18: 4603-4614.
16. Dague, E., Bitar, R., Ranchon, H., Durand, F., Yken, H.M., and François, J.M. (2010) An atomic force microscopy analysis of yeast mutants defective in cell wall architecture. Yeast 27: 673-684.
17. Dalle, F., Wächtler, B., L'Ollivier, C., Holland, G., Bannert, N., Wilson, D., etal. (2009) Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell Microbiol 12: 248-271.
18. De Nobel, J.G., Klis, F.M., Munnik, T., Priem, J., and Van den Ende, H. (1990) An assay of relative cell wall porosity in Saccharomyces cerevisiae, Kluyveromyces lactis and Schizosaccharomyces pombe Yeast 6: 483-490.
19. Eisman, B., Alonso-Monge, R., Román, E., Arana, D., Nombela, C., and Pla, J. (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: 347-358.
20. Enjalbert, B., Nantel, A., and Whiteway, M. (2003) Stress-induced gene expression in Candida albicans: absence of a general stress response. Mol Biol Cell 14: 1460-1467.
21. Enjalbert, B., Smith, D.A., Cornell, M.J., Alam, I., Nicholls, S., Brown, A.J., and Quinn, J. (2006) Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans Mol Biol Cell 17: 1018-1032.
22. Fidel, P.L., and Sobel, J.D. (1999) Murine models of Candida vaginal infections. In Handbook of Animal Models of Infection. Zak, O. (ed.). New York, NY, USA: Academic Press, pp. 741-748.
23. Gancedo, J.M. (2008) The early steps of glucose signalling in yeast. FEMS Microbiol Rev 32: 673-704.
24. Görner, W., Durchschlag, E., Wolf, J., Brown, E.L., Ammerer, G., Ruis, H., and Schüller, C. (2002) Acute glucose starvation activates the nuclear localization signal of a stress-specific yeast transcription factor. EMBO J 21: 135-144.
25. Gounalaki, N., and Thireos, G. (1994) Yap1p, a yeast transcriptional activator that mediates multidrug resistance, regulates the metabolic stress response. EMBO J 13: 4036-4041.
26. Hedbacker, K., and Carlson, M. (2008) SNF1/AMPK pathways in yeast. Front Biosci 13: 2408-2420.
27. Henriques, M., Azeredo, J., and Oliveira, R. (2007) The involvement of physico-chemical interactions in the adhesion of Candida albicans and Candida dubliniensis to epithelial cells. Mycoses 50: 391-396.
28. Hertz, H. (1986) In Miscellaneous Papers. London: MacMillian.
29. Ihmels, J., Bergmann, S., Gerami-Nejad, M., Yanai, I., McClellan, M., Berman, J., and Barkai, N. (2005) Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309: 938-940.
30. Johnston, M. (1999) Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet 15: 29-33.
31. Kawahata, M., Masaki, K., Fujii, T., and Iefuji, H. (2006) Yeast genes involved in response to lactic acid and acetic acid: acidic conditions caused by the organic acids in Saccharomyces cerevisiae cultures induce expression of intracellular metal metabolism genes regulated by Aft1p. FEMS Yeast Res 6: 924-936.
32. Kim, J.H., and Johnston, M. (2006) Two glucose-sensing pathways converge on Rgt1 to regulate expression of glucose transporter genes in Saccharomyces cerevisiae J Biol Chem 281: 26144-26149.
33. Koyama, T., Makita, M., Shibata, N., and Okawa, Y. (2009) Influence of oxidative and osmotic stresseson the structure of the cell wall mannan of Candida albicans serotype A. Carbohydr Res 44: 2195-2200.
34. Kruppa, M., Greene, R.R., Noss, I., Lowman, D.W., and Williams, D.L. (2011) C.albicans increases cell wall mannoprotein, but not mannan, in response to blood, serum and cultivation at physiological temperature. Glycobiology 21: 1173-1180.
35. Kulkarni, R.K., Hollingsworth, P.J., and Volz, P.A. (1980) Variation in cell surface features of Candida albicans with respect to carbon sources. Sabouraudia 18: 255-260.
36. Lavoie, H., Hogues, H., and Whiteway, M. (2009) Rearrangements of the transcriptional regulatory networks of metabolic pathways in fungi. Curr Opin Microbiol 12: 655-663.
37. Lee, K.K., MacCallum, D.M., Jacobsen, M.D., Walker, L.A., Odds, F.C., Gow, N.A., and Munro, C.A. (2011) Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrob Agents Chemother 56: 208-217.
38. Lorenz, M.C., and Fink, G.R. (2001) The glyoxylate cycle is required for fungal virulence. Nature 412: 83-86.
39. Lorenz, M.C., Bender, J.A., and Fink, G.R. (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3: 1076-1087.
40. MacCallum, D.M., Castillo, L., Nather, K., Munro, C.A., Brown, A.J., Gow, N.A., and Odds, F.C. (2009) Property differences among the four major Candida albicans strain clades. Eukaryot Cell 8: 373-387.
41. MacCallum, D.M., Coste, A., Ischer, F., Jacobsen, M.D., Odds, F.C., and Sanglard, D. (2010) Genetic dissection of azole resistance mechanisms in Candida albicans and their validation in a mouse model of disseminated infection. Antimicrob Agents Chemother 54: 1476-1483.
42. Martchenko, M., Levitin, A., Hogues, H., Nantel, A., and Whiteway, M. (2007) Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr Biol 17: 1007-1013.
43. Müller, D.J., and Dufrêne, Y.F. (2011) Force nanoscopy of living cells. Curr Biol 21: R212-R216.
44. 2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans Mol Microbiol 63: 1399-1413.
45. Navarro-Garcia, F., Alonso-Monge, R., Rico, H., Pla, J., Sentandreu, R., and Nombela, C. (1998) A role for the MAP kinase gene MKC1 in cell wall construction and morphological transitions in Candida albicans Microbiology 144: 411-424.
46. Navarro-Garcia, F., Eisman, B., Fiuza, S.M., Nombela, C., and Pla, J. (2005) The MAP kinase Mkc1p is activated under different stress conditions in Candida albicans Microbiology 151: 2737-2749.
47. Negredo, A., Monteoliva, L., Gil, C., Pla, J., and Nombela, C. (1997) Cloning, analysis and one-step disruption of the ARG5, 6 gene of Candida albicans Microbiology 143: 297-302.
48. Netea, M.G., Gow, N.A., Munro, C.A., Bates, S., Collins, C., Ferwerda, G., etal. (2006) Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 166: 1642-1650.
49. Niimi, M., Kamiyama, A., and Tokunaga, M. (1988) Respiration of medically important Candida species and Saccharomyces cerevisiae in relation to glucose effect. J Med Vet Mycol 26: 195-197.
50. O'Hanlon, D.E., Moench, T.R., and Cone, R.A. (2011) In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide. BMC Infect Dis 11: 200.
51. Odds, F.C., Van Nuffel, L., and Gow, N.A. (2000) Survival in experimental Candida albicans infections depends on inoculum growth conditions as well as animal host. Microbiology 146: 1881-1889.
52. Perlroth, J., Choi, B., and Spellberg, B. (2007) Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med Mycol 45: 321-346.
53. Pfaller, M.A., and Diekema, D.J. (2010) Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 36: 1-53.
54. Piekarska, K., Mol, E., van den Berg, M., Hardy, G., van den Burg, J., van Roermund, C., etal. (2006) Peroxisomal fatty acid beta-oxidation is not essential for virulence of Candida albicans Eukaryot Cell 5: 1847-1856.
55. Plaine, A., Walker, L., Da Costa, G., Mora-Montes, H.M., McKinnon, A., Gow, N.A., etal. (2008) Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol 45: 1404-1414.
56. Price, M.S., Betancourt-Quiroz, M., Price, J.L., Toffaletti, D.L., Vora, H., Hu, G., etal. (2011) Cryptococcus neoformans requires a functional glycolytic pathway for disease but not persistence in the host. mBio 2: e00103-e00111.
57. Ramsdale, M., Selway, L., Stead, D., Walker, J., Yin, Z., Nicholls, S.M., etal. (2008) MNL1 regulates weak acid induced stress responses of the fungal pathogen Candida albicans Mol Biol Cell 19: 4393-4403.
58. Rodaki, A., Bohovych, I.M., Enjalbert, B., Young, T., Odds, F.C., Gow, N.A., and Brown, A.J.P. (2009) Glucose promotes stress resistance in the fungal pathogen Candida albicans Mol Biol Cell 20: 4845-4855.
59. Sabina, J., and Brown, V. (2009) Glucose sensing network in Candida albicans: a sweet spot for fungal morphogenesis. Eukaryot Cell 8: 1314-1320.
60. San José, C., Monge, R.A., Pérez-Díaz, R., Pla, J., and Nombela, C. (1996) The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus Candida albicans J Bacteriol 178: 5850-5852.
61. Sanglard, D., Ischer, F., Parkinson, T., Falconer, D., and Bille, J. (2003) Candida albicans mutations in the ergosterol biosynthetic pathway and resistance to several antifungal agents. Antimicrob Agents Chemother 47: 2404-2412.
62. Sardi, J.C., Duque, C., Mariano, F.S., Marques, M.R., Höfling, J.F., and Gonçalves, R.B. (2011) Adhesion and invasion of Candida albicans from periodontal pockets of patients with chronic periodontitis and diabetes to gingival human fibroblasts. Med Mycol 50: 43-49.
63. Schaber, J., Adrover, M.A., Eriksson, E., Pelet, S., Petelenz-Kurdziel, E., Klein, D., etal. (2010) Biophysical properties of Saccharomyces cerevisiae and their relationship with HOG pathway activation. Eur Biophys J 39: 1547-1546.
64. Sexton, J.A., Brown, V., and Johnston, M. (2007) Regulation of sugar transport and metabolism by the Candida albicans Rgt1 transcriptional repressor. Yeast 24: 847-860.
65. Smith, D.A., Nicholls, S., Morgan, B.A., Brown, A.J., and Quinn, J. (2004) A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans Mol Biol Cell 15: 4179-4190.
66. Soumya, A., Mohamed, M., Fatimazahra, B., Hassan, L., Abdellah, H., Fatima, H., and Saad, I.K. (2011) Study of microbial adhesion on some wood species: theoretical prediction. Mikrobiologiia 80: 47-52.
67. Stanhill, A., Schick, N., and Engelberg, D. (1999) The yeast ras/cyclic AMP pathway induces invasive growth by suppressing the cellular stress response. Mol Biol Cell 19: 7529-7538.
68. Ueno, K., Matsumoto, Y., Uno, J., Sasamoto, K., Sekimizu, K., Kinjo, Y., and Chibaba, H. (2011) Intestinal resident yeast Candida glabrata requires Cyb2p-mediated lactate assimilation to adapt in mouse intestine. PLoS ONE 6: e24759.
69. Vieira, N., Casal, M., Johansson, B., MacCallum, D.M., Brown, A.J., and Paiva, S. (2010) Functional specialization and differential regulation of short-chain carboxylic acid transporters in the pathogen Candida albicans Mol Microbiol 75: 1337-1354.
70. Vylkova, S., Carman, A.J., Danhof, H.A., Collette, J.R., Zhou, H., and Lorenz, M.C. (2011) The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. mBio 2: e00055-e00011.
71. Walker, L.A., Munro, C.A., de Bruijn, I., Lenardon, M.D., McKinnon, A., and Gow, N.A. (2008) Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 4: e1000040.
72. Willis, A.M., Coulter, W.A., Hayes, J.R., Bell, P., and Lamey, P.J. (2000) Factors affecting the adhesion of Candida albicans to epithelial cells of insulin-using diabetes mellitus patients. J Med Microbiol 49: 291-293.
73. Wilson, D., Tutulan-Cunita, A., Jung, W., Hauser, N.C., Hernandez, R., Williamson, T., etal. (2007) Deletion of the high-affinity cAMP phosphodiesterase encoded by PDE2 affects stress responses and virulence in Candida albicans Mol Microbiol 65: 841-856.
74. Yin, Z., Smith, R.J., and Brown, A.J.P. (1996) Multiple signalling pathways trigger the exquisite sensitivity of yeast gluconeogenic mRNAs to glucose. Mol Microbiol 20: 751-761.
75. Yoshijima, Y., Murakami, K., Kayama, S., Liu, D., Hirota, K., Ichikawa, T., and Miyake, Y. (2010) Effect of substrate surface hydrophobicity on the adherence of yeast and hyphal Candida Mycoses 53: 221-226.
76. Zaman, S., Lippman, S.I., Zhao, X., and Broach, J.R. (2008) How Saccharomyces responds to nutrients. Annu Rev Genet 42: 27-81.