Difference in virulence between fluconazole-susceptible and fluconazole-resistant Candida albicans in a mouse model

Mycoses

Volumn 54, Issue 5, 2011, Pages

  Schulz, Bettina ^a   Weber, Kai ^a   Schmidt, Axel ^b   Borg von Zepelin, Margarete ^c   Ruhnke, Markus ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b BAYER AG   (Germany)

^c Hufeland Klinikum   (Germany)

Author keywords

Adherence; Biofilm; Candida; Fluconazole; Resistance; Virulence

Indexed keywords

FLUCONAZOLE; MULTIDRUG RESISTANCE PROTEIN 1; PROTEINASE; VIRULENCE FACTOR;

ANIMAL MODEL; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; BIOFILM; CANDIDA ALBICANS; CELL LINE; CSH1 GENE; ENZYME RELEASE; EPITHELIUM CELL; FUNGAL GENE; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS ISOLATION; GENE EXPRESSION; GROWTH RATE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; MINIMUM INHIBITORY CONCENTRATION; MORTALITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OROPHARYNX CANDIDIASIS; PRIORITY JOURNAL; RECURRENT INFECTION; STRAIN DIFFERENCE; SURVIVAL RATE; UPREGULATION;

ANIMALS; ANTIFUNGAL AGENTS; CANDIDA ALBICANS; CANDIDIASIS; CELL ADHESION; CELL LINE; DISEASE MODELS, ANIMAL; DNA, FUNGAL; DRUG RESISTANCE, FUNGAL; EPITHELIAL CELLS; FLUCONAZOLE; GENOTYPE; HIV INFECTIONS; HUMANS; MALE; MICE; MYCOLOGICAL TYPING TECHNIQUES; RODENT DISEASES; SURVIVAL ANALYSIS; VIRULENCE;

CANDIDA; CANDIDA ALBICANS; MUS;

EID: 80052821706     PISSN: 09337407     EISSN: 14390507     Source Type: Journal    
DOI: 10.1111/j.1439-0507.2010.01970.x     Document Type: Article

References (42)

1. Espinel-Ingroff A. Mechanisms of resistance to antifungal agents: yeasts and filamentous fungi. Rev Iberoam Micol 2008; 25: 101-6.
2. Rex JH, Rinaldi MG, Pfaller MA. Resistance of Candida species to fluconazole. Antimicrob Agents Chemother 1995; 39: 1-8.
3. Ruhnke M, Eigler A, Tennagen I, Geiseler B, Engelmann E, Trautmann M. Emergence of fluconazole-resistant strains of Candida albicans in patients with recurrent oropharyngeal candidosis and human immunodeficiency virus infection. J Clin Microbiol 1994; 32: 2092-8.
4. Sanglard D, Kuchler K, Ischer F, Pagani JL, Monod M, Bille J. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob Agents Chemother 1995; 39: 2378-86.
5. Franz R, Kelly SL, Lamb DC, Kelly DE, Ruhnke M, Morschhäuser J. Multiple molecular mechanisms contribute to a stepwise development of fluconazole resistance in clinical Candida albicans strains. Antimicrob Agents Chemother 1998; 42: 3065-72.
6. White TC. Increased mRNA levels of ERG16, CDR, and MDR1 correlate with increases in azole resistance in Candida albicans isolates from a patient infected with human immunodeficiency virus. Antimicrob Agents Chemother 1997; 41: 1482-7.
7. White TC, Holleman S, Dy F, Mirels LF, Stevens DA. Resistance mechanisms in clinical isolates of Candida albicans. Antimicrob Agents Chemother 2002; 46: 1704-13.
8. Kusch H, Biswas K, Schwanfelder S et al. A proteomic approach to understanding the development of multidrug-resistant Candida albicans strains. Mol Genet Genomics 2004; 271: 554-65.
9. National Committee for Clinical Laboratory Standards. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. Approved standard NCCLS document M27-A. Wayne, PA: National Committee for Clinical Laboratory Standards, 1997.
10. Sullivan D, Bennett D, Henman M et al. Oligonucleotide fingerprinting of isolates of Candida species other than C. albicans and of atypical Candida species from human immunodeficiency virus-positive and AIDS patients. J Clin Microbiol 1993; 31: 2124-33.
11. Jin Y, Yip HK, Samaranayake YH, Yau JY, Samaranayake LP. Biofilm-forming ability of Candida albicans is unlikely to contribute to high levels of oral yeast carriage in cases of human immunodeficiency virus infection. J Clin Microbiol 2003; 41: 2961-7.
12. Kofla G, Ruhnke M. Development of a new real-time TaqMan PCR assay for quantitative analyses of Candida albicans resistance genes expression. J Microbiol Methods 2007; 68: 178-83.
13. Fling ME, Kopf J, Tamarkin A, Gorman JA, Smith HA, Koltin Y. Analysis of a Candida albicans gene that encodes a novel mechanism for resistance to benomyl and methotrexate. Mol Gen Genet 1991; 227: 318-29.
14. Sanglard D, Ischer F, Monod M, Bille J. Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiology 1997; 143: 405-16.
15. Singleton DR, Masuoka J, Hazen KC. Cloning and analysis of a Candida albicans gene that affects cell surface hydrophobicity. J Bacteriol 2001; 183: 3582-8.
16. Crandall M, Edwards JE Jr. Segregation of proteinase-negative mutants from heterozygous Candida albicans. J Gen Microbiol 1987; 133: 2817-24.
17. Pinto E, Ribeiro IC, Ferreira NJ, Fortes CE, Fonseca PA, Figueiral MH. Correlation between enzyme production, germ tube formation and susceptibility to fluconazole in Candida species isolated from patients with denture-related stomatitis and control individuals. J Oral Pathol Med 2008; 37: 587-92.
18. Borg-von ZM, Wagner T. Fluorescence assay for the detection of adherent Candida yeasts to target cells in microtest plates. Mycoses 1995; 38: 339-47.
19. Schmidt A, Geschke U. Comparative virulence of Candida albicans strains in CFW1 mice and Sprague-Dawley rats. Mycoses 1996; 39: 157-60.
20. Morschhäuser J, Barker KS, Liu TT, BlaB-Warmuth J, Homayouni R, Rogers PD. The transcription factor Mrr1p controls expression of the MDR1 efflux pump and mediates multidrug resistance in Candida albicans. PLoS Pathog 2007; 3: e164.
21. Lischewski A, Ruhnke M, Tennagen I, Schonian G, Morschhäuser J, Hacker J. Molecular epidemiology of Candida isolates from AIDS patients showing different fluconazole resistance profiles. J Clin Microbiol 1995; 33: 769-71.
22. Rex JH, Pfaller MA, Walsh TJ et al. Antifungal susceptibility testing: practical aspects and current challenges. Clin Microbiol Rev 2001; 14: 643-58, table.
23. Cowen LE, Kohn LM, Anderson JB. Divergence in fitness and evolution of drug resistance in experimental populations of Candida albicans. J Bacteriol 2001; 183: 2971-8.
24. Graybill JR, Montalbo E, Kirkpatrick WR, Luther MF, Revankar SG, Patterson TF. Fluconazole versus Candida albicans: a complex relationship. Antimicrob Agents Chemother 1998; 42: 2938-42.
25. Andersson DI, Hughes D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 2010; 8: 260-71.
26. Wirsching S, Michel S, Morschhäuser J. Targeted gene disruption in Candida albicans wild-type strains: the role of the MDR1 gene in fluconazole resistance of clinical Candida albicans isolates. Mol Microbiol 2000; 36: 856-65.
27. Angiolella L, Stringaro AR, De BF et al. Increase of virulence and its phenotypic traits in drug-resistant strains of Candida albicans. Antimicrob Agents Chemother 2008; 52: 927-36.
28. Fekete-Forgacs K, Gyure L, Lenkey B. Changes of virulence factors accompanying the phenomenon of induced fluconazole resistance in Candida albicans. Mycoses 2000; 43: 273-9.
29. Wu T, Wright K, Hurst SF, Morrison CJ. Enhanced extracellular production of aspartyl proteinase, a virulence factor, by Candida albicans isolates following growth in subinhibitory concentrations of fluconazole. Antimicrob Agents Chemother 2000; 44: 1200-8.
30. Schaller M, Borelli C, Korting HC, Hube B. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses 2005; 48: 365-77.
31. Schaller M, Bein M, Korting HC et al. The secreted aspartyl proteinases Sap1 and Sap2 cause tissue damage in an in vitro model of vaginal candidiasis based on reconstituted human vaginal epithelium. Infect Immun 2003; 71: 3227-34.
32. Schaller M, Korting HC, Schafer W, Bastert J, Chen W, Hube B. Secreted aspartic proteinase (Sap) activity contributes to tissue damage in a model of human oral candidosis. Mol Microbiol 1999; 34: 169-80.
33. Monod M, Borg-von ZM. Secreted aspartic proteases as virulence factors of Candida species. Biol Chem 2002; 383: 1087-93.
34. Sweet SP, Cookson S, Challacombe SJ. Candida albicans isolates from HIV-infected and AIDS patients exhibit enhanced adherence to epithelial cells. J Med Microbiol 1995; 43: 452-7.
35. Cutler JE. Putative virulence factors of Candida albicans. Annu Rev Microbiol 1991; 45: 187-218.
36. Müller FM, Morschhäuser J, Köhler G, Oelschlaeger TA, Ziebuhr W, Hacker J. Adherence and invasion-two pathogenicity factors in bacterial and fungal pathogens. Mycoses 1999; 42(Suppl. 1): 39-42.
37. Rotrosen D, Calderone RA, Edwards JE Jr. Adherence of Candida species to host tissues and plastic surfaces. Rev Infect Dis 1986; 8: 73-85.
38. Hazen KC. Participation of yeast cell surface hydrophobicity in adherence of Candida albicans to human epithelial cells. Infect Immun 1989; 57: 1894-900.
39. Singleton DR, Fidel PL Jr, Wozniak KL, Hazen KC. Contribution of cell surface hydrophobicity protein 1 (Csh1p) to virulence of hydrophobic Candida albicans serotype A cells. FEMS Microbiol Lett 2005; 244: 373-7.
40. Karababa M, Coste AT, Rognon B, Bille J, Sanglard D. Comparison of gene expression profiles of Candida albicans azole-resistant clinical isolates and laboratory strains exposed to drugs inducing multidrug transporters. Antimicrob Agents Chemother 2004; 48: 3064-79.
41. Rogers PD, Barker KS. Genome-wide expression profile analysis reveals coordinately regulated genes associated with stepwise acquisition of azole resistance in Candida albicans clinical isolates. Antimicrob Agents Chemother 2003; 47: 1220-7.
42. Nobile CJ, Nett JE, Hernday AD et al. Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 2009; 7: e1000133.