Skip to main content
Top
Published in: European Journal of Clinical Microbiology & Infectious Diseases 5/2014

01-05-2014 | Review

Candida glabrata: a review of its features and resistance

Authors: C. F. Rodrigues, S. Silva, M. Henriques

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 5/2014

Login to get access

Abstract

Candida species belong to the normal microbiota of the oral cavity and gastrointestinal and vaginal tracts, and are responsible for several clinical manifestations, from mucocutaneous overgrowth to bloodstream infections. Once believed to be non-pathogenic, Candida glabrata was rapidly blamable for many human diseases. Year after year, these pathological circumstances are more recurrent and problematic to treat, especially when patients reveal any level of immunosuppression. These difficulties arise from the capacity of C. glabrata to form biofilms and also from its high resistance to traditional antifungal therapies. Thus, this review intends to present an excerpt of the biology, epidemiology, and pathology of C. glabrata, and detail an approach to its resistance mechanisms based on studies carried out up to the present.
Literature
1.
go back to reference Lass-Flörl C (2009) The changing face of epidemiology of invasive fungal disease in Europe. Mycoses 52:197–205PubMed Lass-Flörl C (2009) The changing face of epidemiology of invasive fungal disease in Europe. Mycoses 52:197–205PubMed
2.
go back to reference Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J (2012) Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev 36(2):288–305. doi:10.1111/j.1574-6976.2011.00278.x PubMed Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J (2012) Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev 36(2):288–305. doi:10.​1111/​j.​1574-6976.​2011.​00278.​x PubMed
3.
go back to reference Odds FC (1988) Candida and candidosis, 2nd edn. Bailliere Tindall, London, UK Odds FC (1988) Candida and candidosis, 2nd edn. Bailliere Tindall, London, UK
4.
go back to reference Calderone RA (2002) Introduction and historical perspectives. In: Calderone RA (ed) Candida and candidiasis. ASM Press, Washington D.C., pp 15–25 Calderone RA (2002) Introduction and historical perspectives. In: Calderone RA (ed) Candida and candidiasis. ASM Press, Washington D.C., pp 15–25
5.
go back to reference Pfaller MA, Diekema DJ (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133–163PubMedCentralPubMed Pfaller MA, Diekema DJ (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133–163PubMedCentralPubMed
6.
go back to reference Bassetti M, Righi E, Costa A et al (2006) Epidemiological trends in nosocomial candidemia in intensive care. BMC Infect Dis 6:21PubMedCentralPubMed Bassetti M, Righi E, Costa A et al (2006) Epidemiological trends in nosocomial candidemia in intensive care. BMC Infect Dis 6:21PubMedCentralPubMed
7.
go back to reference Colombo AL, Guimarães T, Silva LR et al (2007) Prospective observational study of candidemia in São Paulo, Brazil: incidence rate, epidemiology, and predictors of mortality. Infect Control Hosp Epidemiol 28:570–576PubMed Colombo AL, Guimarães T, Silva LR et al (2007) Prospective observational study of candidemia in São Paulo, Brazil: incidence rate, epidemiology, and predictors of mortality. Infect Control Hosp Epidemiol 28:570–576PubMed
8.
go back to reference Chakrabarti A, Chatterjee SS, Rao KLN et al (2009) Recent experience with fungaemia: change in species distribution and azole resistance. Scand J Infect Dis 41:275–284PubMed Chakrabarti A, Chatterjee SS, Rao KLN et al (2009) Recent experience with fungaemia: change in species distribution and azole resistance. Scand J Infect Dis 41:275–284PubMed
9.
go back to reference Hasan F, Xess I, Wang X, Jain N, Fries BC (2009) Biofilm formation in clinical Candida isolates and its association with virulence. Microbes Infect 11:753–761PubMedCentralPubMed Hasan F, Xess I, Wang X, Jain N, Fries BC (2009) Biofilm formation in clinical Candida isolates and its association with virulence. Microbes Infect 11:753–761PubMedCentralPubMed
10.
go back to reference Krcmery V (1999) Torulopsis glabrata: an emerging yeast pathogen in cancer patients. Int J Antimicrob Agents 11:1–6PubMed Krcmery V (1999) Torulopsis glabrata: an emerging yeast pathogen in cancer patients. Int J Antimicrob Agents 11:1–6PubMed
11.
go back to reference Krcmery V, Barnes AJ (2002) Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect 50:243–260PubMed Krcmery V, Barnes AJ (2002) Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect 50:243–260PubMed
12.
go back to reference Kaur R, Domergue R, Zupancic ML, Cormack BP (2005) A yeast by any other name: Candida glabrata and its interaction with the host. Curr Opin Microbiol 8:378–384PubMed Kaur R, Domergue R, Zupancic ML, Cormack BP (2005) A yeast by any other name: Candida glabrata and its interaction with the host. Curr Opin Microbiol 8:378–384PubMed
13.
go back to reference Pfaller MA, Diekema DJ (2004) Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect 10(Suppl 1):11–23PubMed Pfaller MA, Diekema DJ (2004) Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect 10(Suppl 1):11–23PubMed
14.
go back to reference Bethea EK, Carver BJ, Montedonico AE, Reynolds TB (2010) The inositol regulon controls viability in Candida glabrata. Microbiology 156:452–462PubMedCentralPubMed Bethea EK, Carver BJ, Montedonico AE, Reynolds TB (2010) The inositol regulon controls viability in Candida glabrata. Microbiology 156:452–462PubMedCentralPubMed
15.
go back to reference 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 62:10–24PubMed 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 62:10–24PubMed
16.
go back to reference Kim J, Sudbery P (2011) Candida albicans, a major human fungal pathogen. J Microbiol 49:171–177PubMed Kim J, Sudbery P (2011) Candida albicans, a major human fungal pathogen. J Microbiol 49:171–177PubMed
17.
go back to reference Lim CS, Rosli R, Seow HF, Chong PP (2012) Candida and invasive candidiasis: back to basics. Eur J Clin Microbiol Infect Dis 31:21–31PubMed Lim CS, Rosli R, Seow HF, Chong PP (2012) Candida and invasive candidiasis: back to basics. Eur J Clin Microbiol Infect Dis 31:21–31PubMed
18.
go back to reference Vincent JL, Rello J, Marshall J et al (2009) International study of the prevalence and outcomes of infection in intensive care units. JAMA 302:2323–2329PubMed Vincent JL, Rello J, Marshall J et al (2009) International study of the prevalence and outcomes of infection in intensive care units. JAMA 302:2323–2329PubMed
19.
go back to reference Wisplinghoff H, Seifert H, Wenzel RP, Edmond MB (2006) Inflammatory response and clinical course of adult patients with nosocomial bloodstream infections caused by Candida spp. Clin Microbiol Infect 12:170–177PubMed Wisplinghoff H, Seifert H, Wenzel RP, Edmond MB (2006) Inflammatory response and clinical course of adult patients with nosocomial bloodstream infections caused by Candida spp. Clin Microbiol Infect 12:170–177PubMed
20.
go back to reference Vazquez JA, Dembry LM, Sanchez V et al (1998) Nosocomial Candida glabrata colonization: an epidemiologic study. J Clin Microbiol 36:421–426PubMedCentralPubMed Vazquez JA, Dembry LM, Sanchez V et al (1998) Nosocomial Candida glabrata colonization: an epidemiologic study. J Clin Microbiol 36:421–426PubMedCentralPubMed
21.
go back to reference Vazquez JA, Sanchez V, Dmuchowski C, Dembry LM, Sobel JD, Zervos MJ (1993) Nosocomial acquisition of Candida albicans: an epidemiologic study. J Infect Dis 168:195–201PubMed Vazquez JA, Sanchez V, Dmuchowski C, Dembry LM, Sobel JD, Zervos MJ (1993) Nosocomial acquisition of Candida albicans: an epidemiologic study. J Infect Dis 168:195–201PubMed
22.
go back to reference Reagan DR, Pfaller MA, Hollis RJ, Wenzel RP (1990) Characterization of the sequence of colonization and nosocomial candidemia using DNA fingerprinting and a DNA probe. J Clin Microbiol 28:2733–2738PubMedCentralPubMed Reagan DR, Pfaller MA, Hollis RJ, Wenzel RP (1990) Characterization of the sequence of colonization and nosocomial candidemia using DNA fingerprinting and a DNA probe. J Clin Microbiol 28:2733–2738PubMedCentralPubMed
23.
go back to reference Hagerty JA, Ortiz J, Reich D, Manzarbeitia C (2003) Fungal infections in solid organ transplant patients. Surg Infect (Larchmt) 4:263–271 Hagerty JA, Ortiz J, Reich D, Manzarbeitia C (2003) Fungal infections in solid organ transplant patients. Surg Infect (Larchmt) 4:263–271
25.
go back to reference Samaranayake LP, Fidel PL, Naglik JR et al (2002) Fungal infections associated with HIV infection. Oral Dis 8:151–160PubMed Samaranayake LP, Fidel PL, Naglik JR et al (2002) Fungal infections associated with HIV infection. Oral Dis 8:151–160PubMed
26.
go back to reference Rajendran R, Robertson DP, Hodge PJ, Lappin DF, Ramage G (2010) Hydrolytic enzyme production is associated with Candida albicans biofilm formation from patients with type 1 diabetes. Mycopathologia 170:229–235PubMed Rajendran R, Robertson DP, Hodge PJ, Lappin DF, Ramage G (2010) Hydrolytic enzyme production is associated with Candida albicans biofilm formation from patients with type 1 diabetes. Mycopathologia 170:229–235PubMed
27.
go back to reference Kuhn DM, Ghannoum MA (2004) Candida biofilms: antifungal resistance and emerging therapeutic options. Curr Opin Investig Drugs 5:186–197PubMed Kuhn DM, Ghannoum MA (2004) Candida biofilms: antifungal resistance and emerging therapeutic options. Curr Opin Investig Drugs 5:186–197PubMed
28.
go back to reference de Almeida AA, Mesquita CS, Svidzinski TI, de Oliveira KM (2013) Antifungal susceptibility and distribution of Candida spp. isolates from the University Hospital in the municipality of Dourados, State of Mato Grosso do Sul, Brazil. Rev Soc Bras Med Trop 46(3):335–339. doi:10.1590/0037-8682-0074-2012 PubMed de Almeida AA, Mesquita CS, Svidzinski TI, de Oliveira KM (2013) Antifungal susceptibility and distribution of Candida spp. isolates from the University Hospital in the municipality of Dourados, State of Mato Grosso do Sul, Brazil. Rev Soc Bras Med Trop 46(3):335–339. doi:10.​1590/​0037-8682-0074-2012 PubMed
29.
go back to reference Fidel PL Jr, Vazquez JA, Sobel JD (1999) Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin Microbiol Rev 12:80–96PubMedCentralPubMed Fidel PL Jr, Vazquez JA, Sobel JD (1999) Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin Microbiol Rev 12:80–96PubMedCentralPubMed
30.
go back to reference Dujon B, Sherman D, Fischer G et al (2004) Genome evolution in yeasts. Nature 430:35–44PubMed Dujon B, Sherman D, Fischer G et al (2004) Genome evolution in yeasts. Nature 430:35–44PubMed
31.
go back to reference Wolfe KH, Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–713PubMed Wolfe KH, Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–713PubMed
32.
go back to reference Butler G, Rasmussen MD, Lin MF et al (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657–662PubMedCentralPubMed Butler G, Rasmussen MD, Lin MF et al (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657–662PubMedCentralPubMed
33.
go back to reference Brunke S, Hube B (2013) Two unlike cousins: Candida albicans and C. glabrata infection strategies. Cell Microbiol 15(5):701–708PubMedCentralPubMed Brunke S, Hube B (2013) Two unlike cousins: Candida albicans and C. glabrata infection strategies. Cell Microbiol 15(5):701–708PubMedCentralPubMed
35.
go back to reference Butler G, Kenny C, Fagan A, Kurischko C, Gaillardin C, Wolfe KH (2004) Evolution of the MAT locus and its Ho endonuclease in yeast species. Proc Natl Acad Sci U S A 101:1632–1637PubMedCentralPubMed Butler G, Kenny C, Fagan A, Kurischko C, Gaillardin C, Wolfe KH (2004) Evolution of the MAT locus and its Ho endonuclease in yeast species. Proc Natl Acad Sci U S A 101:1632–1637PubMedCentralPubMed
36.
go back to reference Hittinger CT, Rokas A, Carroll SB (2004) Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts. Proc Natl Acad Sci U S A 101:14144–14149PubMedCentralPubMed Hittinger CT, Rokas A, Carroll SB (2004) Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts. Proc Natl Acad Sci U S A 101:14144–14149PubMedCentralPubMed
37.
go back to reference Roetzer A, Gabaldón T, Schüller C (2011) From Saccharomyces cerevisiae to Candida glabrata in a few easy steps: important adaptations for an opportunistic pathogen. FEMS Microbiol Lett 314:1–9PubMedCentralPubMed Roetzer A, Gabaldón T, Schüller C (2011) From Saccharomyces cerevisiae to Candida glabrata in a few easy steps: important adaptations for an opportunistic pathogen. FEMS Microbiol Lett 314:1–9PubMedCentralPubMed
38.
go back to reference Kramer A, Schwebke I, Kampf G (2006) How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis 6:130PubMedCentralPubMed Kramer A, Schwebke I, Kampf G (2006) How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis 6:130PubMedCentralPubMed
39.
go back to reference Cox GM, Harrison TS, Mcdade HC et al (2003) Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect Immun 71(1):173–180PubMedCentralPubMed Cox GM, Harrison TS, Mcdade HC et al (2003) Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect Immun 71(1):173–180PubMedCentralPubMed
40.
go back to reference Nicola AM, Casadevall A, Goldman DL (2008) Fungal killing by mammalian phagocytic cells. Curr Opin Microbiol 11(4):313–317PubMedCentralPubMed Nicola AM, Casadevall A, Goldman DL (2008) Fungal killing by mammalian phagocytic cells. Curr Opin Microbiol 11(4):313–317PubMedCentralPubMed
42.
go back to reference Nakagawa Y, Kanbe T, Mizuguchi I (2003) Disruption of the human pathogenic yeast Candida albicans catalase gene decreases survival in mouse-model infection and elevates susceptibility to higher temperature and to detergents. Microbiol Immunol 47(6):395–403PubMed Nakagawa Y, Kanbe T, Mizuguchi I (2003) Disruption of the human pathogenic yeast Candida albicans catalase gene decreases survival in mouse-model infection and elevates susceptibility to higher temperature and to detergents. Microbiol Immunol 47(6):395–403PubMed
43.
go back to reference Roetzer A, Gratz N, Kovarik P, Schüller C (2010) Autophagy supports Candida glabrata survival during phagocytosis. Cell Microbiol 12(2):199–216PubMedCentralPubMed Roetzer A, Gratz N, Kovarik P, Schüller C (2010) Autophagy supports Candida glabrata survival during phagocytosis. Cell Microbiol 12(2):199–216PubMedCentralPubMed
44.
go back to reference Saijo T, Miyazaki T, Izumikawa K et al (2010) Skn7p is involved in oxidative stress response and virulence of Candida glabrata. Mycopathologia 169(2):81–90PubMed Saijo T, Miyazaki T, Izumikawa K et al (2010) Skn7p is involved in oxidative stress response and virulence of Candida glabrata. Mycopathologia 169(2):81–90PubMed
45.
go back to reference Lee J, Godon C, Lagniel G et al (1999) Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J Biol Chem 274(23):16040–16046PubMed Lee J, Godon C, Lagniel G et al (1999) Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J Biol Chem 274(23):16040–16046PubMed
46.
go back to reference Gulshan K, Lee SS, Moye-Rowley WS (2011) Differential oxidant tolerance determined by the key transcription factor Yap1 is controlled by levels of the Yap1-binding protein, Ybp1. J Biol Chem 286(39):34071–34081PubMedCentralPubMed Gulshan K, Lee SS, Moye-Rowley WS (2011) Differential oxidant tolerance determined by the key transcription factor Yap1 is controlled by levels of the Yap1-binding protein, Ybp1. J Biol Chem 286(39):34071–34081PubMedCentralPubMed
47.
go back to reference Roetzer A, Klopf E, Gratz N et al (2011) Regulation of Candida glabrata oxidative stress resistance is adapted to host environment. FEBS Lett 585(2):319–327PubMedCentralPubMed Roetzer A, Klopf E, Gratz N et al (2011) Regulation of Candida glabrata oxidative stress resistance is adapted to host environment. FEBS Lett 585(2):319–327PubMedCentralPubMed
48.
go back to reference Kaur R, Ma B, Cormack BP (2007) A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci U S A 104(18):7628–7633PubMedCentralPubMed Kaur R, Ma B, Cormack BP (2007) A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci U S A 104(18):7628–7633PubMedCentralPubMed
49.
go back to reference Lorenz MC, Bender JA, Fink GR (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3(5):1076–1087PubMedCentralPubMed Lorenz MC, Bender JA, Fink GR (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3(5):1076–1087PubMedCentralPubMed
50.
go back to reference Roetzer A, Gregori C, Jennings AM et al (2008) Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol Microbiol 69(3):603–620PubMedCentralPubMed Roetzer A, Gregori C, Jennings AM et al (2008) Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol Microbiol 69(3):603–620PubMedCentralPubMed
51.
go back to reference Seider K, Brunke S, Schild L et al (2011) The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J Immunol 187(6):3072–3086PubMed Seider K, Brunke S, Schild L et al (2011) The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J Immunol 187(6):3072–3086PubMed
52.
go back to reference Klionsky DJ (2004) Cell biology: regulated self-cannibalism. Nature 431(7004):31–32PubMed Klionsky DJ (2004) Cell biology: regulated self-cannibalism. Nature 431(7004):31–32PubMed
53.
54.
go back to reference Xie Z, Klionsky DJ (2007) Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9(10):1102–1109PubMed Xie Z, Klionsky DJ (2007) Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9(10):1102–1109PubMed
55.
go back to reference Verstrepen KJ, Jansen A, Lewitter F, Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37(9):986–990PubMedCentralPubMed Verstrepen KJ, Jansen A, Lewitter F, Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37(9):986–990PubMedCentralPubMed
56.
go back to reference Sundstrom P (2002) Adhesion in Candida spp. Cell Microbiol 4(8):461–469PubMed Sundstrom P (2002) Adhesion in Candida spp. Cell Microbiol 4(8):461–469PubMed
57.
go back to reference Ruan SY, Hsueh PR (2009) Invasive candidiasis: an overview from Taiwan. J Formos Med Assoc 108(6):443–451PubMed Ruan SY, Hsueh PR (2009) Invasive candidiasis: an overview from Taiwan. J Formos Med Assoc 108(6):443–451PubMed
58.
go back to reference Kraneveld EA, De Soet JJ, Deng DM et al (2011) Identification and differential gene expression of adhesin-like wall proteins in Candida glabrata biofilms. Mycopathologia 172:415–427. doi:10.1007/ s11046-011-9446-2 PubMed Kraneveld EA, De Soet JJ, Deng DM et al (2011) Identification and differential gene expression of adhesin-like wall proteins in Candida glabrata biofilms. Mycopathologia 172:415–427. doi:10.​1007/​ s11046-011-9446-2 PubMed
59.
go back to reference De Groot PW, Kraneveld EA, Yin QY et al (2008) The cell wall of the human pathogen Candida glabrata: differential incorporation of novel adhesin-like wall proteins. Eukaryot Cell 7(11):1951–1964PubMedCentralPubMed De Groot PW, Kraneveld EA, Yin QY et al (2008) The cell wall of the human pathogen Candida glabrata: differential incorporation of novel adhesin-like wall proteins. Eukaryot Cell 7(11):1951–1964PubMedCentralPubMed
60.
go back to reference Domergue R, Castaño I, De Las Peñas A et al (2005) Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308(5723):866–870PubMed Domergue R, Castaño I, De Las Peñas A et al (2005) Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308(5723):866–870PubMed
61.
go back to reference Castaño I, Pan SJ, Zupancic M, Hennequin C, Dujon B, Cormack BP (2005) Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol Microbiol 55(4):1246–1258PubMed Castaño I, Pan SJ, Zupancic M, Hennequin C, Dujon B, Cormack BP (2005) Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol Microbiol 55(4):1246–1258PubMed
62.
go back to reference Jandric Z, Schüller C (2011) Stress response in Candida glabrata: pieces of a fragmented picture. Future Microbiol 6(12):1475–1484PubMed Jandric Z, Schüller C (2011) Stress response in Candida glabrata: pieces of a fragmented picture. Future Microbiol 6(12):1475–1484PubMed
64.
go back to reference Jayatilake JA, Samaranayake YH, Cheung LK, Samaranayake LP (2006) Quantitative evaluation of tissue invasion by wild type, hyphal and SAP mutants of Candida albicans, and non-albicans Candida species in reconstituted human oral epithelium. J Oral Pathol Med 35(8):484–491PubMed Jayatilake JA, Samaranayake YH, Cheung LK, Samaranayake LP (2006) Quantitative evaluation of tissue invasion by wild type, hyphal and SAP mutants of Candida albicans, and non-albicans Candida species in reconstituted human oral epithelium. J Oral Pathol Med 35(8):484–491PubMed
65.
go back to reference Tamura NK, Negri MF, Bonassoli LA, Svidzinski TI (2007) Virulence factors for Candida spp recovered from intravascular catheters and hospital workers hands. Rev Soc Bras Med Trop 40:91–93PubMed Tamura NK, Negri MF, Bonassoli LA, Svidzinski TI (2007) Virulence factors for Candida spp recovered from intravascular catheters and hospital workers hands. Rev Soc Bras Med Trop 40:91–93PubMed
66.
go back to reference Silva S, Henriques M, Martins A, Oliveira R, Williams D, Azeredo J (2009) Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. Med Mycol 47:681–689PubMed Silva S, Henriques M, Martins A, Oliveira R, Williams D, Azeredo J (2009) Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. Med Mycol 47:681–689PubMed
67.
go back to reference Iraqui I, Garcia-Sanchez S, Aubert S et al (2005) The Yak1p kinase controls expression of adhesins and biofilm formation in Candida glabrata in a Sir4p-dependent pathway. Mol Microbiol 55:1259–1271PubMed Iraqui I, Garcia-Sanchez S, Aubert S et al (2005) The Yak1p kinase controls expression of adhesins and biofilm formation in Candida glabrata in a Sir4p-dependent pathway. Mol Microbiol 55:1259–1271PubMed
68.
go back to reference De Las Peñas A, Pan SJ, Castaño I, Alder J, Cregg R, Cormack BP (2003) Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1- and SIR-dependent transcriptional silencing. Genes Dev 17:2245–2258 De Las Peñas A, Pan SJ, Castaño I, Alder J, Cregg R, Cormack BP (2003) Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1- and SIR-dependent transcriptional silencing. Genes Dev 17:2245–2258
69.
go back to reference Cormack BP, Ghori N, Falkow S (1999) An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 285:578–582PubMed Cormack BP, Ghori N, Falkow S (1999) An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 285:578–582PubMed
71.
go back to reference van Dyk D, Pretorius IS, Bauer FF (2005) Mss11p is a central element of the regulatory network that controls FLO11 expression and invasive growth in Saccharomyces cerevisiae. Genetics 169:91–106PubMedCentralPubMed van Dyk D, Pretorius IS, Bauer FF (2005) Mss11p is a central element of the regulatory network that controls FLO11 expression and invasive growth in Saccharomyces cerevisiae. Genetics 169:91–106PubMedCentralPubMed
72.
go back to reference Riera M, Mogensen E, d’Enfert C, Janbon G (2012) New regulators of biofilm development in Candida glabrata. Res Microbiol 163:297–307PubMed Riera M, Mogensen E, d’Enfert C, Janbon G (2012) New regulators of biofilm development in Candida glabrata. Res Microbiol 163:297–307PubMed
73.
go back to reference Guo B, Styles CA, Feng Q, Fink GR (2000) A Saccharomyces gene family involved in invasive growth, cell–cell adhesion, and mating. Proc Natl Acad Sci U S A 97:12158–12163PubMedCentralPubMed Guo B, Styles CA, Feng Q, Fink GR (2000) A Saccharomyces gene family involved in invasive growth, cell–cell adhesion, and mating. Proc Natl Acad Sci U S A 97:12158–12163PubMedCentralPubMed
74.
go back to reference Sheppard DC, Yeaman MR, Welch WH et al (2004) Functional and structural diversity in the Als protein family of Candida albicans. J Biol Chem 279:30480–30489PubMed Sheppard DC, Yeaman MR, Welch WH et al (2004) Functional and structural diversity in the Als protein family of Candida albicans. J Biol Chem 279:30480–30489PubMed
77.
go back to reference Chakrabarti A, Nayak N, Talwar P (1991) In vitro proteinase production by Candida species. Mycopathologia 114:163–168PubMed Chakrabarti A, Nayak N, Talwar P (1991) In vitro proteinase production by Candida species. Mycopathologia 114:163–168PubMed
79.
go back to reference Mohan das V, Ballal M (2008) Proteinase and phospholipase activity as virulence factors in Candida species isolated from blood. Rev Iberoam Micol 25(4):208–210PubMed Mohan das V, Ballal M (2008) Proteinase and phospholipase activity as virulence factors in Candida species isolated from blood. Rev Iberoam Micol 25(4):208–210PubMed
80.
go back to reference Kalkanci A, Güzel AB, Khalil II, Aydin M, Ilkit M, Kuştimur S (2012) Yeast vaginitis during pregnancy: susceptibility testing of 13 antifungal drugs and boric acid and the detection of four virulence factors. Med Mycol 50(6):585–593. doi:10.3109/13693786.2012.662597 PubMed Kalkanci A, Güzel AB, Khalil II, Aydin M, Ilkit M, Kuştimur S (2012) Yeast vaginitis during pregnancy: susceptibility testing of 13 antifungal drugs and boric acid and the detection of four virulence factors. Med Mycol 50(6):585–593. doi:10.​3109/​13693786.​2012.​662597 PubMed
81.
go back to reference Ueno K, Matsumoto Y, Uno J et al (2011) Intestinal resident yeast Candida glabrata requires Cyb2p-mediated lactate assimilation to adapt in mouse intestine. PLoS One 6(9):e24759PubMedCentralPubMed Ueno K, Matsumoto Y, Uno J et al (2011) Intestinal resident yeast Candida glabrata requires Cyb2p-mediated lactate assimilation to adapt in mouse intestine. PLoS One 6(9):e24759PubMedCentralPubMed
82.
go back to reference Sikora M, Dabkowska M, Swoboda-Kopec E et al (2011) Differences in proteolytic activity and gene profiles of fungal strains isolated from the total parenteral nutrition patients. Folia Microbiol (Praha) 56(2):143–148. doi:10.1007/s12223-011-0023-3 Sikora M, Dabkowska M, Swoboda-Kopec E et al (2011) Differences in proteolytic activity and gene profiles of fungal strains isolated from the total parenteral nutrition patients. Folia Microbiol (Praha) 56(2):143–148. doi:10.​1007/​s12223-011-0023-3
83.
go back to reference Negri M, Martins M, Henriques M et al (2010) Examination of potential virulence factors of Candida tropicalis clinical isolates from hospitalized patients. Mycophatologia 169:175–182. doi:10.1007/s11046-009-9246-0 Negri M, Martins M, Henriques M et al (2010) Examination of potential virulence factors of Candida tropicalis clinical isolates from hospitalized patients. Mycophatologia 169:175–182. doi:10.​1007/​s11046-009-9246-0
84.
go back to reference Luo G, Samaranayake LP (2002) Candida glabrata, an emerging fungal pathogen, exhibits superior relative cell surface hydrophobicity and adhesion to denture acrylic surfaces compared with Candida albicans. APMIS 110:601–610PubMed Luo G, Samaranayake LP (2002) Candida glabrata, an emerging fungal pathogen, exhibits superior relative cell surface hydrophobicity and adhesion to denture acrylic surfaces compared with Candida albicans. APMIS 110:601–610PubMed
85.
go back to reference Luo G, Samaranayake LP, Cheung BP, Tang G (2004) Reverse transcriptase polymerase chain reaction (RT-PCR) detection of HLP gene expression in Candida glabrata and its possible role in in vitro haemolysin production. APMIS 112:283–290PubMed Luo G, Samaranayake LP, Cheung BP, Tang G (2004) Reverse transcriptase polymerase chain reaction (RT-PCR) detection of HLP gene expression in Candida glabrata and its possible role in in vitro haemolysin production. APMIS 112:283–290PubMed
86.
go back to reference Berila N, Hyroššová P, Subík J (2011) Oxidative stress response and virulence factors in Candida glabrata clinical isolates. Folia Microbiol (Praha) 56(2):116–121. doi:10.1007/s12223-011-0016-2 Berila N, Hyroššová P, Subík J (2011) Oxidative stress response and virulence factors in Candida glabrata clinical isolates. Folia Microbiol (Praha) 56(2):116–121. doi:10.​1007/​s12223-011-0016-2
89.
go back to reference Niimi M, Firth NA, Cannon RD (2010) Antifungal drug resistance of oral fungi. Odontology 98(1):15–25PubMed Niimi M, Firth NA, Cannon RD (2010) Antifungal drug resistance of oral fungi. Odontology 98(1):15–25PubMed
90.
go back to reference Akins RA (2005) An update on antifungal targets and mechanisms of resistance in Candida albicans. Med Mycol 43(4):285–318PubMed Akins RA (2005) An update on antifungal targets and mechanisms of resistance in Candida albicans. Med Mycol 43(4):285–318PubMed
91.
go back to reference Van Bambeke F, Balzi E, Tulkens PM (2000) Antibiotic efflux pumps. Biochem Pharmacol 60(4):457–470PubMed Van Bambeke F, Balzi E, Tulkens PM (2000) Antibiotic efflux pumps. Biochem Pharmacol 60(4):457–470PubMed
92.
go back to reference Wilson D, Thewes S, Zakikhany K et al (2009) Identifying infection-associated genes of Candida albicans in the postgenomic era. FEMS Yeast Res 9:688–700PubMed Wilson D, Thewes S, Zakikhany K et al (2009) Identifying infection-associated genes of Candida albicans in the postgenomic era. FEMS Yeast Res 9:688–700PubMed
93.
go back to reference Brunke S, Seider K, Almeida RS et al (2010) Candida glabrata tryptophan-based pigment production via the Ehrlich pathway. Mol Microbiol 76:25–47PubMed Brunke S, Seider K, Almeida RS et al (2010) Candida glabrata tryptophan-based pigment production via the Ehrlich pathway. Mol Microbiol 76:25–47PubMed
94.
go back to reference Tscherner M, Schwarzmüller T, Kuchler K (2011) Pathogenesis and antifungal drug resistance of the human fungal pathogen Candida glabrata. Pharmaceuticals 4:169–186. doi:10.3390/ph4010169 Tscherner M, Schwarzmüller T, Kuchler K (2011) Pathogenesis and antifungal drug resistance of the human fungal pathogen Candida glabrata. Pharmaceuticals 4:169–186. doi:10.​3390/​ph4010169
95.
go back to reference Henry KW, Nickels JT, Edlind TD (2000) Upregulation of ERG genes in Candida species by azoles and other sterol biosynthesis inhibitors. Antimicrob Agents Chemother 44(10):2693–2700PubMedCentralPubMed Henry KW, Nickels JT, Edlind TD (2000) Upregulation of ERG genes in Candida species by azoles and other sterol biosynthesis inhibitors. Antimicrob Agents Chemother 44(10):2693–2700PubMedCentralPubMed
96.
go back to reference Stead DA, Walker J, Holcombe L et al (2009) Impact of the transcriptional regulator, Ace2, on the Candida glabrata secretome. Proteomics 10:212–223 Stead DA, Walker J, Holcombe L et al (2009) Impact of the transcriptional regulator, Ace2, on the Candida glabrata secretome. Proteomics 10:212–223
97.
go back to reference Calcagno AM, Bignell E, Warn P et al (2003) Candida glabrata STE12 is required for wild-type levels of virulence and nitrogen starvation induced filamentation. Mol Microbiol 50:1309–1318PubMed Calcagno AM, Bignell E, Warn P et al (2003) Candida glabrata STE12 is required for wild-type levels of virulence and nitrogen starvation induced filamentation. Mol Microbiol 50:1309–1318PubMed
98.
go back to reference Ferrari S, Sanguinetti M, De Bernardis F et al (2011) Loss of mitochondrial functions associated with azole resistance in Candida glabrata results in enhanced virulence in mice. Antimicrob Agents Chemother 55:1852–1860PubMedCentralPubMed Ferrari S, Sanguinetti M, De Bernardis F et al (2011) Loss of mitochondrial functions associated with azole resistance in Candida glabrata results in enhanced virulence in mice. Antimicrob Agents Chemother 55:1852–1860PubMedCentralPubMed
99.
go back to reference Kaur R, Castaño I, Cormack BP (2004) Functional genomic analysis of fluconazole susceptibility in the pathogenic yeast Candida glabrata: roles of calcium signaling and mitochondria. Antimicrob Agents Chemother 48:1600–1613PubMedCentralPubMed Kaur R, Castaño I, Cormack BP (2004) Functional genomic analysis of fluconazole susceptibility in the pathogenic yeast Candida glabrata: roles of calcium signaling and mitochondria. Antimicrob Agents Chemother 48:1600–1613PubMedCentralPubMed
100.
go back to reference Miyazaki T, Yamauchi S, Inamine T et al (2010) Roles of calcineurin and crz1 in antifungal susceptibility and virulence of Candida glabrata. Antimicrob Agents Chemother 54:1639–1643PubMedCentralPubMed Miyazaki T, Yamauchi S, Inamine T et al (2010) Roles of calcineurin and crz1 in antifungal susceptibility and virulence of Candida glabrata. Antimicrob Agents Chemother 54:1639–1643PubMedCentralPubMed
101.
go back to reference Bennett JE, Izumikawa K, Marr KA (2004) Mechanism of increased fluconazole resistance in Candida glabrata during prophylaxis. Antimicrob Agents Chemother 48:1773–1777PubMedCentralPubMed Bennett JE, Izumikawa K, Marr KA (2004) Mechanism of increased fluconazole resistance in Candida glabrata during prophylaxis. Antimicrob Agents Chemother 48:1773–1777PubMedCentralPubMed
103.
go back to reference Vermitsky JP, Edlind TD (2004) Azole resistance in Candida glabrata: coordinate upregulation of multidrug transporters and evidence for a Pdr1-Like transcription factor. Antimicrob Agents Chemother 48:3773–3781PubMedCentralPubMed Vermitsky JP, Edlind TD (2004) Azole resistance in Candida glabrata: coordinate upregulation of multidrug transporters and evidence for a Pdr1-Like transcription factor. Antimicrob Agents Chemother 48:3773–3781PubMedCentralPubMed
104.
go back to reference Vale-Silva L, Ischer F, LeibundGut-Landmann S, Sanglard D (2013) Gain-of-function mutations in PDR1, a regulator of antifungal drug resistance in Candida glabrata, control adherence to host cells. Infect Immun 81(5):1709–1720. doi:10.1128/IAI.00074-13 PubMedCentralPubMed Vale-Silva L, Ischer F, LeibundGut-Landmann S, Sanglard D (2013) Gain-of-function mutations in PDR1, a regulator of antifungal drug resistance in Candida glabrata, control adherence to host cells. Infect Immun 81(5):1709–1720. doi:10.​1128/​IAI.​00074-13 PubMedCentralPubMed
105.
go back to reference Paul S, Schmidt JA, Moye-Rowley WS (2011) Regulation of the CgPdr1 transcription factor from the pathogen Candida glabrata. Eukaryot Cell 10(2):187–197PubMedCentralPubMed Paul S, Schmidt JA, Moye-Rowley WS (2011) Regulation of the CgPdr1 transcription factor from the pathogen Candida glabrata. Eukaryot Cell 10(2):187–197PubMedCentralPubMed
107.
go back to reference Chen KH, Miyazaki T, Tsai HF, Bennett JE (2007) The bZip transcription factor Cgap1p is involved in multidrug resistance and required for activation of multidrug transporter gene CgFLR1 in Candida glabrata. Gene 386(1–2):63–72PubMed Chen KH, Miyazaki T, Tsai HF, Bennett JE (2007) The bZip transcription factor Cgap1p is involved in multidrug resistance and required for activation of multidrug transporter gene CgFLR1 in Candida glabrata. Gene 386(1–2):63–72PubMed
108.
go back to reference Farahyar S, Zaini F, Kordbacheh P et al (2013) Overexpression of aldo-keto-reductase in azole-resistant clinical isolates of Candida glabrata determined by cDNA-AFLP. Daru 21:1PubMedCentralPubMed Farahyar S, Zaini F, Kordbacheh P et al (2013) Overexpression of aldo-keto-reductase in azole-resistant clinical isolates of Candida glabrata determined by cDNA-AFLP. Daru 21:1PubMedCentralPubMed
109.
go back to reference Thompson GR 3rd, Wiederhold NP, Vallor AC, Villareal NC, Lewis JS 2nd, Patterson TF (2008) Development of caspofungin resistance following prolonged therapy for invasive candidiasis secondary to Candida glabrata infection. Antimicrob Agents Chemother 52:3783–3785PubMedCentralPubMed Thompson GR 3rd, Wiederhold NP, Vallor AC, Villareal NC, Lewis JS 2nd, Patterson TF (2008) Development of caspofungin resistance following prolonged therapy for invasive candidiasis secondary to Candida glabrata infection. Antimicrob Agents Chemother 52:3783–3785PubMedCentralPubMed
110.
go back to reference Pfaller MA, Castanheira M, Lockhart SR, Ahlquist AM, Messer SA, Jones RN (2012) Frequency of decreased susceptibility and resistance to echinocandins among fluconazole-resistant bloodstream isolates of Candida glabrata. J Clin Microbiol 50:1199–1203PubMedCentralPubMed Pfaller MA, Castanheira M, Lockhart SR, Ahlquist AM, Messer SA, Jones RN (2012) Frequency of decreased susceptibility and resistance to echinocandins among fluconazole-resistant bloodstream isolates of Candida glabrata. J Clin Microbiol 50:1199–1203PubMedCentralPubMed
111.
go back to reference Arendrup MC, Perlin DS, Jensen RH, Howard SJ, Goodwin J, Hope W (2012) Differential in vivo activities of anidulafungin, caspofungin, and micafungin against Candida glabrata isolates with and without FKS resistance mutations. Antimicrob Agents Chemother 56:2435–2442PubMedCentralPubMed Arendrup MC, Perlin DS, Jensen RH, Howard SJ, Goodwin J, Hope W (2012) Differential in vivo activities of anidulafungin, caspofungin, and micafungin against Candida glabrata isolates with and without FKS resistance mutations. Antimicrob Agents Chemother 56:2435–2442PubMedCentralPubMed
112.
go back to reference Shields RK, Nguyen MH, Press EG et al (2012) The presence of an FKS mutation rather than MIC is an independent risk factor for failure of echinocandin therapy among patients with invasive candidiasis due to Candida glabrata. Antimicrob Agents Chemother 56:4862–4869PubMedCentralPubMed Shields RK, Nguyen MH, Press EG et al (2012) The presence of an FKS mutation rather than MIC is an independent risk factor for failure of echinocandin therapy among patients with invasive candidiasis due to Candida glabrata. Antimicrob Agents Chemother 56:4862–4869PubMedCentralPubMed
113.
go back to reference Alexander BD, Johnson MD, Pfeiffer CD et al (2013) Increasing echinocandin resistance in Candida glabrata: clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clin Infect Dis 56(12):1724–1732PubMed Alexander BD, Johnson MD, Pfeiffer CD et al (2013) Increasing echinocandin resistance in Candida glabrata: clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clin Infect Dis 56(12):1724–1732PubMed
114.
go back to reference Vandeputte P, Tronchin G, Larcher G et al (2008) A nonsense mutation in the ERG6 gene leads to reduced susceptibility to polyenes in a clinical isolate of Candida glabrata. Antimicrob Agents Chemother 52:3701–3709PubMedCentralPubMed Vandeputte P, Tronchin G, Larcher G et al (2008) A nonsense mutation in the ERG6 gene leads to reduced susceptibility to polyenes in a clinical isolate of Candida glabrata. Antimicrob Agents Chemother 52:3701–3709PubMedCentralPubMed
115.
go back to reference Vandeputte P, Tronchin G, Bergès T, Hennequin C, Chabasse D, Bouchara JP (2007) Reduced susceptibility to polyenes associated with a missense mutation in the erg6 gene in a clinical isolate of Candida glabrata with pseudohyphal growth. Antimicrob Agents Chemother 51:982–990PubMedCentralPubMed Vandeputte P, Tronchin G, Bergès T, Hennequin C, Chabasse D, Bouchara JP (2007) Reduced susceptibility to polyenes associated with a missense mutation in the erg6 gene in a clinical isolate of Candida glabrata with pseudohyphal growth. Antimicrob Agents Chemother 51:982–990PubMedCentralPubMed
116.
go back to reference Helmerhorst EJ, Venuleo C, Sanglard D, Oppenheim FG (2006) Roles of cellular respiration, CgCDR1, and CgCDR2 in Candida glabrata resistance to histatin 5. Antimicrob Agents Chemother 50:1100–1103PubMedCentralPubMed Helmerhorst EJ, Venuleo C, Sanglard D, Oppenheim FG (2006) Roles of cellular respiration, CgCDR1, and CgCDR2 in Candida glabrata resistance to histatin 5. Antimicrob Agents Chemother 50:1100–1103PubMedCentralPubMed
117.
go back to reference Edgerton M, Koshlukova SE (2000) Salivary histatin 5 and its similarities to the other antimicrobial proteins in human saliva. Adv Dent Res 14:16–21PubMed Edgerton M, Koshlukova SE (2000) Salivary histatin 5 and its similarities to the other antimicrobial proteins in human saliva. Adv Dent Res 14:16–21PubMed
118.
go back to reference Helmerhorst EJ, Oppenheim FG (2004) The antifungal mechanisms of antimicrobial proteins. In: Hancock REW, Devine D (eds) Mammalian antimicrobial proteins, 1st edn. Cambridge University Press, Cambridge, pp 245–277 Helmerhorst EJ, Oppenheim FG (2004) The antifungal mechanisms of antimicrobial proteins. In: Hancock REW, Devine D (eds) Mammalian antimicrobial proteins, 1st edn. Cambridge University Press, Cambridge, pp 245–277
119.
go back to reference Oppenheim FG (1989) Salivary histidine-rich proteins. In: Tenovuo JO (ed) Human saliva: clinical chemistry and microbiology. CRC Press, Boca Raton, pp 151–160 Oppenheim FG (1989) Salivary histidine-rich proteins. In: Tenovuo JO (ed) Human saliva: clinical chemistry and microbiology. CRC Press, Boca Raton, pp 151–160
120.
go back to reference Oppenheim FG, Xu T, McMillian FM et al (1988) Histatins, a novel family of histidine-rich proteins in human parotid secretion. Isolation, characterization, primary structure, and fungistatic effects on Candida albicans. J Biol Chem 263:7472–7477PubMed Oppenheim FG, Xu T, McMillian FM et al (1988) Histatins, a novel family of histidine-rich proteins in human parotid secretion. Isolation, characterization, primary structure, and fungistatic effects on Candida albicans. J Biol Chem 263:7472–7477PubMed
121.
go back to reference Tsai H, Bobek LA (1998) Human salivary histatins: promising anti-fungal therapeutic agents. Crit Rev Oral Biol Med 9:480–497PubMed Tsai H, Bobek LA (1998) Human salivary histatins: promising anti-fungal therapeutic agents. Crit Rev Oral Biol Med 9:480–497PubMed
122.
go back to reference Van Urk H, Voll WSL, Scheffers WA, van Dijken JP (1990) Transient-state analysis of metabolic fluxes in Crabtree-positive and Crabtree-negative yeasts. Appl Environ Microbiol 56:281–287PubMedCentralPubMed Van Urk H, Voll WSL, Scheffers WA, van Dijken JP (1990) Transient-state analysis of metabolic fluxes in Crabtree-positive and Crabtree-negative yeasts. Appl Environ Microbiol 56:281–287PubMedCentralPubMed
123.
go back to reference Niimi M, Kamiyama A, Tokunaga M (1988) Respiration of medically important Candida species and Saccharomyces cerevisiae in relation to glucose effect. J Med Vet Mycol 26:195–198PubMed Niimi M, Kamiyama A, Tokunaga M (1988) Respiration of medically important Candida species and Saccharomyces cerevisiae in relation to glucose effect. J Med Vet Mycol 26:195–198PubMed
124.
go back to reference Shahi P, Moye-Rowley WS (2009) Coordinate control of lipid composition and drug transport activities is required for normal multidrug resistance in fungi. Biochim Biophys Acta 1794:852–859PubMedCentralPubMed Shahi P, Moye-Rowley WS (2009) Coordinate control of lipid composition and drug transport activities is required for normal multidrug resistance in fungi. Biochim Biophys Acta 1794:852–859PubMedCentralPubMed
125.
go back to reference Muller H, Thierry A, Coppée JY et al (2009) Genomic polymorphism in the population of Candida glabrata: Gene copy-number variation and chromosomal translocations. Fungal Genet Biol 46:264–276PubMed Muller H, Thierry A, Coppée JY et al (2009) Genomic polymorphism in the population of Candida glabrata: Gene copy-number variation and chromosomal translocations. Fungal Genet Biol 46:264–276PubMed
126.
go back to reference Thierry A, Bouchier C, Dujon B, Richard GF (2008) Megasatellites: a peculiar class of giant minisatellites in genes involved in cell adhesion and pathogenicity in Candida glabrata. Nucleic Acids Res 36(18):5970–5982PubMedCentralPubMed Thierry A, Bouchier C, Dujon B, Richard GF (2008) Megasatellites: a peculiar class of giant minisatellites in genes involved in cell adhesion and pathogenicity in Candida glabrata. Nucleic Acids Res 36(18):5970–5982PubMedCentralPubMed
127.
go back to reference Barchiesi F, Falconi Di Francesco L, Arzeni D, Caselli F, Gallo D, Scalise G (1999) Electrophoretic karyotyping and triazole susceptibility of Candida glabrata clinical isolates. Eur J Clin Microbiol Infect Dis 18:184–187PubMed Barchiesi F, Falconi Di Francesco L, Arzeni D, Caselli F, Gallo D, Scalise G (1999) Electrophoretic karyotyping and triazole susceptibility of Candida glabrata clinical isolates. Eur J Clin Microbiol Infect Dis 18:184–187PubMed
128.
129.
go back to reference Klempp-Selb B, Rimek D, Kappe R (2000) Karyotyping of Candida albicans and Candida glabrata from patients with Candida sepsis. Mycoses 43:159–163PubMed Klempp-Selb B, Rimek D, Kappe R (2000) Karyotyping of Candida albicans and Candida glabrata from patients with Candida sepsis. Mycoses 43:159–163PubMed
130.
go back to reference Lin CY, Chen YC, Lo HJ, Chen KW, Li SY (2007) Assessment of Candida glabrata strain relatedness by pulsed-field gel electrophoresis and multilocus sequence typing. J Clin Microbiol 45:2452–2459PubMedCentralPubMed Lin CY, Chen YC, Lo HJ, Chen KW, Li SY (2007) Assessment of Candida glabrata strain relatedness by pulsed-field gel electrophoresis and multilocus sequence typing. J Clin Microbiol 45:2452–2459PubMedCentralPubMed
131.
go back to reference Shin JH, Chae MJ, Song JW et al (2007) Changes in karyotype and azole susceptibility of sequential bloodstream isolates from patients with Candida glabrata candidemia. J Clin Microbiol 45:2385–2391PubMedCentralPubMed Shin JH, Chae MJ, Song JW et al (2007) Changes in karyotype and azole susceptibility of sequential bloodstream isolates from patients with Candida glabrata candidemia. J Clin Microbiol 45:2385–2391PubMedCentralPubMed
132.
go back to reference Magee BB, Sanchez MD, Saunders D, Harris D, Berriman M, Magee PT (2008) Extensive chromosome rearrangements distinguish the karyotype of the hypovirulent species Candida dubliniensis from the virulent Candida albicans. Fungal Genet Biol 45:338–350PubMedCentralPubMed Magee BB, Sanchez MD, Saunders D, Harris D, Berriman M, Magee PT (2008) Extensive chromosome rearrangements distinguish the karyotype of the hypovirulent species Candida dubliniensis from the virulent Candida albicans. Fungal Genet Biol 45:338–350PubMedCentralPubMed
133.
go back to reference Samaranayake LP (1990) Host factors and oral candidosis. In: Samaranayake LP, MacFarlane TW (eds) Oral candidosis. Wright-Butterworth, London, pp 66–103 Samaranayake LP (1990) Host factors and oral candidosis. In: Samaranayake LP, MacFarlane TW (eds) Oral candidosis. Wright-Butterworth, London, pp 66–103
134.
go back to reference Hawser SP, Baillie GS, Douglas LJ (1998) Production of extracellular matrix by Candida albicans biofilms. J Med Microbiol 47(3):253–256PubMed Hawser SP, Baillie GS, Douglas LJ (1998) Production of extracellular matrix by Candida albicans biofilms. J Med Microbiol 47(3):253–256PubMed
135.
go back to reference Chandra J, Mukherjee PK, Leidich SD et al (2001) Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J Dent Res 80(3):903–908PubMed Chandra J, Mukherjee PK, Leidich SD et al (2001) Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J Dent Res 80(3):903–908PubMed
136.
go back to reference Al-Fattani MA, Douglas LJ (2004) Penetration of Candida biofilms by antifungal agents. Antimicrob Agents Chemother 48(9):3291–3297PubMedCentralPubMed Al-Fattani MA, Douglas LJ (2004) Penetration of Candida biofilms by antifungal agents. Antimicrob Agents Chemother 48(9):3291–3297PubMedCentralPubMed
137.
go back to reference Blankenship JR, Mitchell AP (2006) How to build a biofilm: a fungal perspective. Curr Opin Microbiol 9(6):588–594PubMed Blankenship JR, Mitchell AP (2006) How to build a biofilm: a fungal perspective. Curr Opin Microbiol 9(6):588–594PubMed
138.
go back to reference Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183(18):5385–5394PubMedCentralPubMed Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183(18):5385–5394PubMedCentralPubMed
139.
go back to reference Ramage G, Vande Walle K, Wickes BL, López-Ribot JL (2001) Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 45(9):2475–2479PubMedCentralPubMed Ramage G, Vande Walle K, Wickes BL, López-Ribot JL (2001) Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 45(9):2475–2479PubMedCentralPubMed
140.
go back to reference Hawser S (1996) Adhesion of different Candida spp. to plastic: XTT formazan determinations. J Med Vet Mycol 34(6):407–410PubMed Hawser S (1996) Adhesion of different Candida spp. to plastic: XTT formazan determinations. J Med Vet Mycol 34(6):407–410PubMed
141.
go back to reference Mah TFC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39PubMed Mah TFC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39PubMed
142.
go back to reference Uppuluri P, Chaturvedi AK, Srinivasan A et al (2010) Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6(3):e1000828PubMedCentralPubMed Uppuluri P, Chaturvedi AK, Srinivasan A et al (2010) Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6(3):e1000828PubMedCentralPubMed
143.
go back to reference Perumal P, Mekala S, Chaffin WL (2007) Role for cell density in antifungal drug resistance in Candida albicans biofilms. Antimicrob Agents Chemother 51(7):2454–2463PubMedCentralPubMed Perumal P, Mekala S, Chaffin WL (2007) Role for cell density in antifungal drug resistance in Candida albicans biofilms. Antimicrob Agents Chemother 51(7):2454–2463PubMedCentralPubMed
145.
go back to reference Bandara HM, Lam OL, Watt RM, Jin LJ, Samaranayake LP (2010) Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species. J Med Microbiol 59(Pt 10):1225–1234. doi:10.1099/jmm.0.021832-0 PubMed Bandara HM, Lam OL, Watt RM, Jin LJ, Samaranayake LP (2010) Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species. J Med Microbiol 59(Pt 10):1225–1234. doi:10.​1099/​jmm.​0.​021832-0 PubMed
146.
go back to reference Halliwell SC, Smith MCA, Muston P, Holland SL, Avery SV (2012) Heterogeneous expression of the virulence-related adhesin Epa1 between individual cells and strains of the pathogen Candida glabrata. Eukaryot Cell 11(2):141–150PubMedCentralPubMed Halliwell SC, Smith MCA, Muston P, Holland SL, Avery SV (2012) Heterogeneous expression of the virulence-related adhesin Epa1 between individual cells and strains of the pathogen Candida glabrata. Eukaryot Cell 11(2):141–150PubMedCentralPubMed
148.
go back to reference Cannon RD, Lamping E, Holmes AR et al (2007) Candida albicans drug resistance—another way to cope with stress. Microbiology 153(Pt 10):3211–3217PubMed Cannon RD, Lamping E, Holmes AR et al (2007) Candida albicans drug resistance—another way to cope with stress. Microbiology 153(Pt 10):3211–3217PubMed
149.
go back to reference Seneviratne CJ, Wang Y, Jin L, Abiko Y, Samaranayake LP (2010) Proteomics of drug resistance in Candida glabrata biofilms. Proteomics 10:1444–1454PubMed Seneviratne CJ, Wang Y, Jin L, Abiko Y, Samaranayake LP (2010) Proteomics of drug resistance in Candida glabrata biofilms. Proteomics 10:1444–1454PubMed
150.
go back to reference LaFleur MD, Kumamoto CA, Lewis K (2006) Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother 50(11):3839–3846PubMedCentralPubMed LaFleur MD, Kumamoto CA, Lewis K (2006) Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother 50(11):3839–3846PubMedCentralPubMed
151.
go back to reference Lewis K (2008) Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol 322:107–131PubMed Lewis K (2008) Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol 322:107–131PubMed
152.
153.
go back to reference Lafleur MD, Qi Q, Lewis K (2010) Patients with long-term oral carriage harbor high-persister mutants of Candida albicans”. Antimicrob Agents Chemother 54(1):39–44PubMedCentralPubMed Lafleur MD, Qi Q, Lewis K (2010) Patients with long-term oral carriage harbor high-persister mutants of Candida albicans”. Antimicrob Agents Chemother 54(1):39–44PubMedCentralPubMed
Metadata
Title
Candida glabrata: a review of its features and resistance
Authors
C. F. Rodrigues
S. Silva
M. Henriques
Publication date
01-05-2014
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 5/2014
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-013-2009-3

Other articles of this Issue 5/2014

European Journal of Clinical Microbiology & Infectious Diseases 5/2014 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.