Biofilm Formation by the Fungal Pathogen Candida albicans : Development, Architecture, and Drug Resistance
Open accessAbstract
Biofilms are a protected niche for microorganisms, where they are safe from antibiotic treatment and can create a source of persistent infection. Using two clinically relevant Candida albicans biofilm models formed on bioprosthetic materials, we demonstrated that biofilm formation proceeds through three distinct developmental phases. These growth phases transform adherent blastospores to well-defined cellular communities encased in a polysaccharide matrix. Fluorescence and confocal scanning laser microscopy revealed that C. albicans biofilms have a highly heterogeneous architecture composed of cellular and noncellular elements. In both models, antifungal resistance of biofilm-grown cells increased in conjunction with biofilm formation. The expression of agglutinin-like ( ALS ) genes, which encode a family of proteins implicated in adhesion to host surfaces, was differentially regulated between planktonic and biofilm-grown cells. The ability of C. albicans to form biofilms contrasts sharply with that of Saccharomyces cerevisiae , which adhered to bioprosthetic surfaces but failed to form a mature biofilm. The studies described here form the basis for investigations into the molecular mechanisms of Candida biofilm biology and antifungal resistance and provide the means to design novel therapies for biofilm-based infections.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Ergosterol levels are significantly decreased in both intermediate (12-30h) and mature phases (31-72h) biofilms compared to early-phase (0-11h) biofilms, and this is connected to decreased expression of ERG25, ERG11, and ERG6.
“Sterol analyses show that ergosterol levels are signi fi cantly decreased in both intermediate (12-30h) and mature phases (31-72h), compared to those in earlyphase (0-11h) bio fi lms, and this is connected to the decreased expression of ergosterol biosynthetic genes ( ERG25 , ERG11 , and ERG6 ).”
From The synthesis, regulation, and functions of sterols in<i>Candida albicans</i>: Well-known but still lots to learn (2016) · cites this paper as [74]
The Results identify early (0–11 h) and intermediate (12–30 h) biofilm phases, but give the maturation phase as approximately 38–72 h, not 31–72 h. The Results report differential expression of ALS-family genes, not decreased ERG25, ERG11, or ERG6 expression; the passages do not report sterol analyses or a decline in ergosterol. (LLM, conf=0.82)
Experimental — accuracy not yet measuredC. albicans can colonize implanted medical devices via stable biofilms, leading to bloodstream infections and invasive systemic infections.
“Moreover, this yeast can easily colonize implanted medical devices thanks to its capacity to form stable biofilms, a contamination that could lead to bloodstream infections and even invasive systemic infections of organs or tissues [83].”
From Antimicrobial Properties of Antidepressants and Antipsychotics—Possibilities and Implications (2021) · cites this paper as [83]
The MICbiofilm of SM21 increases as the biofilm matures, a common phenomenon among antifungal agents.
“The MICbiofilm of SM21 increases as the biofilm matures, a common phenomenon among antifungal agents [53].”
From In Vitro and In Vivo Activity of a Novel Antifungal Small Molecule against Candida Infections (2014) · cites this paper as [53]
Specific biofilm formation genes are involved in different roles in biofilm resistance, including CTA1, ARO, MSK, HSP90, SKN1, KRE1, SIR, RIF, ZAP1, GCAL1, ADH5, and CSH1.
“Specific biofilm formation genes are being brought up regarding different roles in biofilm resistance: peroxisomal catalase (CTA1), the biosynthesis and degradation of tyrosine genes (ARO), the muscle creatine kinase (MSK), the heat shock protein 90 (HSP 90), the sphingolipid biosynthesis (SKN 1 and KRE1), SIR, RIF, and, finally, the extracellular matrix (ECM) regulators: zinc regulated genes (ZAP”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [159]
Resistance to chlorhexidine, fluconazole, amphotericin B, and nystatin increases as biofilms mature over time, corresponding to growth in metabolic activity over biofilm maturation.
“A study showed that the resistance to chlorhexidine, fluconazole, amphotericin B, and nystatin increased as biofilms mature over time, corresponding to a growth in metabolic activity over biofilm maturation.”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [159]
In experiments on biofilm maturation and metabolic activity, cell number was not controlled, making it unclear if the result is a true demonstration of metabolic activity.
“However, in these experiments, cell number was not controlled, thus making it unclear if this is a true demonstration of metabolic activity [159].”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [159]
C. albicans produces highly structured biofilms composed of multiple cell types encased in an extracellular matrix.
“C. albicans produces highly structured biofilms composed of multiple cell types (i.e., round, budding yeast-form cells; oval pseudohyphal cells; and elongated, cylindrical hyphal cells) encased in an extracellular matrix (23, 61, 158, 161).”
From <i>Candida albicans</i> Biofilms and Human Disease (2015) · cites this paper as [23]
C. albicans biofilm formation comprises four temporal stages: adherence to a surface, proliferation to form a basal layer, growth of pseudohyphae and hyphae with extracellular matrix production, and slow dispersal of yeast-form cells.
“C. albicans biofilm formation comprises four temporal stages (10, 23, 47, 75, 142, 194) (Figure 1): (a) adherence to a surface (spherical yeast cells), (b) proliferation to form a basal layer of anchoring cells, (c) growth of pseudohyphae (ellipsoid cells joined end to end) and hyphae (chains of cylindrical cells) concomitant with production of extracellular matrix material, and (d) slow dispersal”
From <i>Candida albicans</i> Biofilms and Human Disease (2015) · cites this paper as [23]
The biofilm master regulator Bcr1 and some of its downstream targets, including Als1, Als3, and Hwp1, are all required for adherence during biofilm formation.
“For example, the biofilm master regulator Bcr1 and some of its downstream targets, including the cell wall proteins Als1, Als3, and Hwp1, are all required for adherence during biofilm formation (23, 138, 141, 143, 145, 212).”
From <i>Candida albicans</i> Biofilms and Human Disease (2015) · cites this paper as [23]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Bacterial Biofilms: A Common Cause of Persistent Infections
Costerton, J. W., Stewart, P. S., & Greenberg, E. P. (1999) · Science · doi:10.1126/science.284.5418.1318 · Cited by 12,167 · see citing works
Biofilm formation as microbial development
O'Toole, G., Kaplan, H. B., & Kolter, R. (2000) · Annual Review of Microbiology · doi:10.1146/annurev.micro.54.1.49 · Cited by 3,571 · see citing works
The Involvement of Cell-to-Cell Signals in the Development of a Bacterial Biofilm
Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W., & Greenberg, E. P. (1998) · Science · doi:10.1126/science.280.5361.295 · Cited by 3,396 · see citing works
Microbial Biofilms: from Ecology to Molecular Genetics
Davey, M. E., & O’Toole, G. A. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.4.847-867.2000 · Cited by 3,072 · see citing works
Handbook of fluorescent probes and research chemicals
Haugland, R. P. (1996) · Medical Entomology and Zoology · Cited by 2,793 · see citing works
Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms
Singh, P. K., Schaefer, A. L., Parsek, M. R., Moninger, T. O., Welsh, M. J., & Greenberg, E. P. (2000) · Nature · doi:10.1038/35037627 · Cited by 1,519 · see citing works
Watnick, P. I., & Kolter, R. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.10.2675-2679.2000 · Cited by 1,434 · see citing works
Odds, F. C. (1979) · Medical Entomology and Zoology · Cited by 1,292 · see citing works
[6] Genetic approaches to study of biofilms
O’Toole, G. A., Pratt, L. A., Watnick, P. I., Newman, D. K., Weaver, V. B., & Kolter, R. (1999) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(99)10008-9 · Cited by 837 · see citing works
Hospital-Acquired Candidemia: The Attributable Mortality and Excess Length of Stay
Wey, S. B. (1988) · Archives of Internal Medicine · doi:10.1001/archinte.1988.00380120094019 · Cited by 831 · see citing works
Antifungal Resistance of Candidal Biofilms Formed on Denture Acrylic in vitro
Chandra, J., Mukherjee, P. K., Leidich, S. D., Faddoul, F., Hoyer, L. L., Douglas, L., & Ghannoum, M. A. (2001) · Journal of Dental Research · doi:10.1177/00220345010800031101 · Cited by 588 · see citing works
Self-citationBakers' Yeast, a Model for Fungal Biofilm Formation
Reynolds, T. B., & Fink, G. R. (2001) · Science · doi:10.1126/science.291.5505.878 · Cited by 585 · see citing works
The ALS gene family of Candida albicans.
Hoyer, L. L. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)01984-9 · Cited by 540 · see citing works
Self-citationHeterogeneity in biofilms: Table 1
WIMPENNY, J. W. T., Manz, W., & Szewzyk, U. (2000) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2000.tb00565.x · Cited by 530 · see citing works
Xu, K. D., Stewart, P. S., Xia, F., Huang, C., & McFeters, G. A. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.10.4035-4039.1998 · Cited by 501 · see citing works
Biofilm Susceptibility to Antimicrobials
Gilbert, P., Das, J., & Foley, I. (1997) · Advances in Dental Research · doi:10.1177/08959374970110010701 · Cited by 493 · see citing works
Collart, M. A., & Oliviero, S. (1993) · Current Protocols in Molecular Biology · doi:10.1002/0471142727.mb1312s23 · Cited by 451 · see citing works
Bacterial resistance to antibiotics: The role of biofilms
Hoyle, B. D., & Costerton, J. W. (1991) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-7139-6_2 · Cited by 451 · see citing works
Resistance of Candida albicans biofilms to antifungal agents in vitro
Hawser, S., & Douglas, L. (1995) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.39.9.2128 · Cited by 407 · see citing works
Nguyen, M. H. (1995) · Archives of Internal Medicine · doi:10.1001/archinte.1995.00430220087009 · Cited by 363 · see citing works
Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1.
Gale, C. A., Bendel, C. M., McClellan, M., Hauser, M., Becker, J. M., Berman, J., & Hostetter, M. K. (1998) · Science · doi:10.1126/science.279.5355.1355 · Cited by 356 · see citing works
Cystic fibrosis pathogenesis and the role of biofilms in persistent infection
Costerton, J. W. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01918-1 · Cited by 329 · see citing works
Biofilm resistance to antimicrobial agents
Xu, K. D., McFeters, G. A., & Stewart, P. S. (2000) · Microbiology · doi:10.1099/00221287-146-3-547 · Cited by 327 · see citing works
Role of dimorphism in the development of Candida albicans biofilms
BAILLIE, G. S., & DOUGLAS, L. J. (1999) · Journal of Medical Microbiology · doi:10.1099/00222615-48-7-671 · Cited by 304 · see citing works
Predictors of Adverse Outcome in Cancer Patients with Candidemia
Anaissie, E. J., Rex, J. H., Uzun, Ö., & Vartivarian, S. (1998) · The American Journal of Medicine · doi:10.1016/s0002-9343(98)00030-8 · Cited by 295 · see citing works
Adherence to stainless steel by foodborne microorganisms during growth in model food systems
Hood, S. K., & Zottola, E. A. (1997) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(97)00071-8 · Cited by 286 · see citing works
Use of Intrinsic Optical Signals to Monitor Physiological Changes in Brain Tissue Slices
Aitken, P. G., Fayuk, D. A., Somjen, G. G., & Turner, D. A. (1999) · Methods · doi:10.1006/meth.1999.0762 · Cited by 274 · see citing works
Architecture of Intact Natural Human Plaque Biofilms Studied by Confocal Laser Scanning Microscopy
Wood, S. R., Kirkham, J., Marsh, P. D., Shore, R. F., Nattress, B. R., & Robinson, C. (2000) · Journal of Dental Research · doi:10.1177/00220345000790010201 · Cited by 253 · see citing works
Millard, P. J., Roth, B. L., Thi, H. P., Yue, S. T., & Haugland, R. P. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.7.2897-2905.1997 · Cited by 240 · see citing works
Etiology, pathogenesis, therapy, and prophylaxis of oral yeast infections
Budtz‐Jørgensen, E. (1990) · Acta Odontologica Scandinavica · doi:10.3109/00016359009012735 · Cited by 227 · see citing works
Development of bacterial biofilms in dairy processing lines
Austin, J. W., & Bergeron, G. (1995) · Journal of Dairy Research · doi:10.1017/s0022029900031204 · Cited by 167 · see citing works
Yamada‐Okabe, T., Mio, T., Ono, N., Kashima, Y., Matsui, M., Arisawa, M., & Yamada‐Okabe, H. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.23.7243-7247.1999 · Cited by 166 · see citing works
[48] Candida biofilms and their susceptibility to antifungal agents
Baillie, G. S., & Douglas, L. (1999) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(99)10050-8 · Cited by 160 · see citing works
Hoyer, L. L., Scherer, S., Shatzman, A. R., & Livi, G. P. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.tb02219.x · Cited by 150 · see citing works
Self-citationInfluence of electric fields and pH on biofilm structure as related to the bioelectric effect
Stoodley, P., deBeer, D., & Lappin-Scott, H. M. (1997) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.41.9.1876 · Cited by 149 · see citing works
Hellio, C., Bremer, G. B., Pons, A. M., Gal, Y. L., & Bourgougnon, N. (2000) · Applied Microbiology and Biotechnology · doi:10.1007/s002530000413 · Cited by 137 · see citing works
Microelectrode measurements of local mass transport rates in heterogeneous biofilms
Rasmussen, K., & Lewandowski, Z. (1998) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19980805)59:3 · Cited by 130 · see citing works
Modern microscopy in biofilm research: confocal microscopy and other approaches
Palmer, R. J., Jr., & Sternberg, C. (1999) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(99)80046-9 · Cited by 128 · see citing works
Comparative Pathogenesis of Clinical and Nonclinical Isolates of Saccharomyces cerevisiae
Clemons, K. V., McCusker, J. H., Davis, R. W., & Stevens, D. A. (1994) · The Journal of Infectious Diseases · doi:10.1093/infdis/169.4.859 · Cited by 113 · see citing works
Hoyer, L. L., Payne, T. L., & Hecht, J. E. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.20.5334-5343.1998 · Cited by 103 · see citing works
Phototrophic Biofilms on Ancient Mayan Buildings in Yucatan, Mexico
Ortega-Morales, B. O., Guézennec, J., Hernandez-Duque, G., et al. (2000) · Current Microbiology · doi:10.1007/s002849910015 · Cited by 102 · see citing works
Biofilms, infectious agents, and dental unit waterlines: a review
Barbeau, J., Gauthier, C., & Payment, P. (1998) · Canadian Journal of Microbiology · doi:10.1139/cjm-44-11-1019 · Cited by 97 · see citing works
Biofilms, infectious agents, and dental unit waterlines: a review
Barbeau, J., Gauthier, C., & Payment, P. (1998) · Canadian Journal of Microbiology · doi:10.1139/w98-101 · Cited by 90 · see citing works
Yaar, L., Mevarech, M., & Koltint, Y. (1997) · Microbiology · doi:10.1099/00221287-143-9-3033 · Cited by 76 · see citing works
Histopathology, immunology, and serology of oral yeast infections: Diagnosis of oral candidosis
Budtz‐Jørgensen, E. (1990) · Acta Odontologica Scandinavica · doi:10.3109/00016359009012732 · Cited by 70 · see citing works
Bagge, N., Ciofu, O., Skovgaard, L. T., et al. (2000) · Apmis · doi:10.1034/j.1600-0463.2000.d01-102.x · Cited by 61 · see citing works
The prevalence of edentulism and diseases related to dentures—a literature review
MacEntee, M. I. (1985) · Journal of Oral Rehabilitation · doi:10.1111/j.1365-2842.1985.tb00636.x · Cited by 59 · see citing works
Carr, J. H., Anderson, R. L., & Favero, M. S. (1996) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1996.tb03214.x · Cited by 29 · see citing works
Interaction between calcofluor white and carbohydrates of α1-acid glycoprotein
Albani, J. R., & Plancke, Y. D. (1999) · Carbohydrate Research · doi:10.1016/s0008-6215(99)00128-7 · Cited by 23 · see citing works
Interaction between calcofluor white and carbohydrates of α1-acid glycoprotein
Albani, J. R., & Plancke, Y. D. (1998) · Carbohydrate Research · doi:10.1016/s0008-6215(98)00306-1 · Cited by 22 · see citing works
Both genes for EF‐1α in Candida albicans are translated
Sundstrom, P., Irwin, M. Y., Smith, D., & Sypherd, P. S. (1991) · Molecular Microbiology · doi:10.1111/j.1365-2958.1991.tb01918.x · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Flemming, H.-C., & Wingender, J. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2415 · Cited by 10,137 · see citing works
Sardi, J. C. O., Scorzoni, L., Bernardi, T., Fusco-Almeida, A. M., & Mendes Giannini, M. J. S. (2013) · Journal of Medical Microbiology · doi:10.1099/jmm.0.045054-0 · Cited by 1,184 · see citing works
Candida biofilms and their role in infection
Douglas, L. J. (2003) · Trends in Microbiology · doi:10.1016/s0966-842x(02)00002-1 · Cited by 1,150 · see citing works
<i>Candida albicans</i> Biofilms and Human Disease
Nobile, C. J., & Johnson, A. D. (2015) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091014-104330 · Cited by 1,057 · see citing works
<i>Candida</i> Infections of Medical Devices
Kojic, E. M., & Darouiche, R. O. (2004) · Clinical Microbiology Reviews · doi:10.1128/cmr.17.2.255-267.2004 · Cited by 1,055 · see citing works
Silva, S., Negri, M., Henriques, M., Oliveira, R., Williams, D. W., & Azeredo, J. (2012) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2011.00278.x · Cited by 969 · see citing works
Andes, D. R., Safdar, N., Baddley, J. W., Playford, G., Reboli, A. C., Rex, J. H., Sobel, J. D., Pappas, P. G., Kullberg, B. J., & for the Mycoses Study Group (2012) · Clinical Infectious Diseases · doi:10.1093/cid/cis021 · Cited by 793 · see citing works
Candida albicans biofilms: development, regulation, and molecular mechanisms
Gulati, M., & Nobile, C. J. (2016) · Microbes and Infection · doi:10.1016/j.micinf.2016.01.002 · Cited by 738 · see citing works
<i>Candida</i> Infections of the Genitourinary Tract
Achkar, J. M., & Fries, B. C. (2010) · Clinical Microbiology Reviews · doi:10.1128/cmr.00076-09 · Cited by 736 · see citing works
A Recently Evolved Transcriptional Network Controls Biofilm Development in Candida albicans
Nobile, C. J., Fox, E. P., Nett, J. E., Sorrells, T. R., Mitrovich, Q. M., Hernday, A. D., Tuch, B. B., Andes, D. R., & Johnson, A. D. (2012) · Cell · doi:10.1016/j.cell.2011.10.048 · Cited by 711 · see citing works
Candida Biofilms: Threats, Challenges, and Promising Strategies
Cavalheiro, M., & Teixeira, M. C. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00028 · Cited by 690 · see citing works
<i>Candida</i>Biofilms: an Update
Ramage, G., Saville, S. P., Thomas, D. P., & López-Ribot, J. L. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.4.633-638.2005 · Cited by 678 · see citing works
Ramage, G., Rajendran, R., Sherry, L., & Williams, C. (2012) · International Journal of Microbiology · doi:10.1155/2012/528521 · Cited by 583 · see citing works
<i>Candida</i> biofilms on implanted biomaterials: a clinically significant problem
Ramage, G., MartÃnez, J. P., & López-Ribot, J. L. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00117.x · Cited by 575 · see citing works
How to build a biofilm: a fungal perspective
Blankenship, J. R., & Mitchell, A. P. (2006) · Current Opinion in Microbiology · doi:10.1016/j.mib.2006.10.003 · Cited by 530 · see citing works
<i>Candida albicans</i> Biofilms Produce Antifungal-Tolerant Persister Cells
LaFleur, M. D., Kumamoto, C. A., & Lewis, K. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00684-06 · Cited by 521 · see citing works
Mukherjee, P. K., Chandra, J., Kuhn, D. M., & Ghannoum, M. A. (2003) · Infection and Immunity · doi:10.1128/iai.71.8.4333-4340.2003 · Cited by 511 · see citing works
Self-citationCritical Role of Bcr1-Dependent Adhesins in C. albicans Biofilm Formation In Vitro and In Vivo
Nobile, C. J., Andes, D. R., Nett, J. E., Smith, F. J., Yue, F., Phan, Q.-T., Edwards, J. E., Filler, S. G., & Mitchell, A. P. (2006) · PLoS Pathogens · doi:10.1371/journal.ppat.0020063 · Cited by 507 · see citing works
Our Current Understanding of Fungal Biofilms
Ramage, G., Mowat, E., Jones, B., Williams, C., & Lopez-Ribot, J. (2009) · Critical Reviews in Microbiology · doi:10.3109/10408410903241436 · Cited by 483 · see citing works
Regulation of Cell-Surface Genes and Biofilm Formation by the C. albicans Transcription Factor Bcr1p
Nobile, C. J., & Mitchell, A. P. (2005) · Current Biology · doi:10.1016/j.cub.2005.05.047 · Cited by 464 · see citing works
Dispersion as an Important Step in the Candida albicans Biofilm Developmental Cycle
Uppuluri, P., Chaturvedi, A. K., Srinivasan, A., Banerjee, M., Ramasubramaniam, A. K., Köhler, J. R., Kadosh, D., & Lopez-Ribot, J. L. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000828 · Cited by 432 · see citing works
Mechanisms of <i>Candida</i> Biofilm Drug Resistance
Taff, H. T., Mitchell, K. F., Edward, J. A., & Andes, D. R. (2013) · Future Microbiology · doi:10.2217/fmb.13.101 · Cited by 422 · see citing works
Putative Role of β-1,3 Glucans in <i>Candida albicans</i> Biofilm Resistance
Nett, J., Lincoln, L., Marchillo, K., Massey, R., Holoyda, K., Hoff, B., VanHandel, M., & Andes, D. (2007) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01056-06 · Cited by 407 · see citing works
Silva, S., Henriques, M., Martins, A., Oliveira, R., Williams, D., & Azeredo, J. (2009) · Medical Mycology · doi:10.3109/13693780802549594 · Cited by 390 · see citing works
Andes, D., Nett, J., Oschel, P., Albrecht, R., Marchillo, K., & Pitula, A. (2004) · Infection and Immunity · doi:10.1128/iai.72.10.6023-6031.2004 · Cited by 389 · see citing works
Hoyer, L. L., Green, C. B., Oh, S.-H., & Zhao, X. (2008) · Medical Mycology · doi:10.1080/13693780701435317 · Cited by 356 · see citing works
Self-citationCandida albicans Als3, a multifunctional adhesin and invasin
Liu, Y., & Filler, S. G. (2011) · Eukaryotic Cell · doi:10.1128/ec.00279-10 · Cited by 354 · see citing works
García-Sánchez, S., Aubert, S., Iraqui, I., Janbon, G., Ghigo, J.-M., & d'Enfert, C. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.2.536-545.2004 · Cited by 353 · see citing works
The evolution of drug resistance in clinical isolates of Candida albicans.
Ford, C. B., Funt, J. M., Abbey, D., Issi, L., Guiducci, C., Martinez, D. A., Delorey, T., Li, B. Y., White, T. C., Cuomo, C., et al. (2015) · eLife · doi:10.7554/elife.00662 · Cited by 348 · see citing works
Complementary Adhesin Function in C. albicans Biofilm Formation
Nobile, C. J., Schneider, H. A., Nett, J. E., Sheppard, D. C., Filler, S. G., Andes, D. R., & Mitchell, A. P. (2008) · Current Biology · doi:10.1016/j.cub.2008.06.034 · Cited by 351 · see citing works
Mukherjee, P. K., Chandra, J., Retuerto, M., Sikaroodi, M., Brown, R. E., Jurevic, R., Salata, R. A., Lederman, M. M., Gillevet, P. M., & Ghannoum, M. A. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1003996 · Cited by 337 · see citing works
Self-citationBiofilm lifestyle of <i>Candida:</i> a mini review
Seneviratne, C., Jin, L., & Samaranayake, L. (2008) · Oral Diseases · doi:10.1111/j.1601-0825.2007.01424.x · Cited by 317 · see citing works
Adherence and biofilm formation of non-Candida albicans Candida species
Silva, S., Negri, M., Henriques, M., Oliveira, R., Williams, D. W., & Azeredo, J. (2011) · Trends in Microbiology · doi:10.1016/j.tim.2011.02.003 · Cited by 304 · see citing works
Candida albicans forms biofilms on the vaginal mucosa
Harriott, M. M., Lilly, E. A., Rodriguez, T. E., Fidel, P. L., & Noverr, M. C. (2010) · Microbiology · doi:10.1099/mic.0.039354-0 · Cited by 301 · see citing works
Bamford, C. V., d'Mello, A., Nobbs, A. H., Dutton, L. C., Vickerman, M. M., & Jenkinson, H. F. (2009) · Infection and Immunity · doi:10.1128/iai.00438-09 · Cited by 291 · see citing works
A Candida Biofilm-Induced Pathway for Matrix Glucan Delivery: Implications for Drug Resistance
Taff, H. T., Nett, J. E., Zarnowski, R., Ross, K. M., Sanchez, H., Cain, M. T., Hamaker, J., Mitchell, A. P., & Andes, D. R. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002848 · Cited by 291 · see citing works
Fungal Biofilms and Drug Resistance
Jabra-Rizk, M. A., Falkler, W. A., & Meiller, T. F. (2004) · Emerging Infectious Diseases · doi:10.3201/eid1001.030119 · Cited by 292 · see citing works
Sanglard, D., Coste, A., & Ferrari, S. (2009) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2009.00578.x · Cited by 285 · see citing works
Recent insights into Candida albicans biofilm resistance mechanisms
Mathé, L., & Van Dijck, P. (2013) · Current Genetics · doi:10.1007/s00294-013-0400-3 · Cited by 271 · see citing works
Candida glabrata: A review of its features and resistance
Rodrigues, C. F., Silva, S., & Henriques, M. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-2009-3 · Cited by 268 · see citing works
An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus
Beauvais, A., Schmidt, C., Guadagnini, S., Roux, P., Perret, E., Henry, C., Paris, S., Mallet, A., Prévost, M.-C., & Latgé, J. P. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.00895.x · Cited by 262 · see citing works
Mowat, E., Butcher, J., Lang, S., Williams, C., & Ramage, G. (2007) · Journal of Medical Microbiology · doi:10.1099/jmm.0.47247-0 · Cited by 259 · see citing works
Fungal Biofilms, Drug Resistance, and Recurrent Infection
Desai, J. V., Mitchell, A. P., & Andes, D. R. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019729 · Cited by 252 · see citing works
Penetration of <i>Candida</i> Biofilms by Antifungal Agents
Al-Fattani, M. A., & Douglas, L. J. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.9.3291-3297.2004 · Cited by 235 · see citing works
Seidler, M. J., Salvenmoser, S., & Müller, F.-M. C. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00234-08 · Cited by 229 · see citing works
Candida albicans biofilm development, modeling a host–pathogen interaction
Nett, J., & Andes, D. (2006) · Current Opinion in Microbiology · doi:10.1016/j.mib.2006.06.007 · Cited by 210 · see citing works
Monteiro, D. R., Gorup, L. F., Silva, S., Negri, M., de Camargo, E. R., Oliveira, R., Barbosa, D. B., & Henriques, M. (2011) · Biofouling · doi:10.1080/08927014.2011.599101 · Cited by 205 · see citing works
Nett, J. E., Crawford, K., Marchillo, K., & Andes, D. R. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00227-10 · Cited by 207 · see citing works
Biofilm formation in clinical Candida isolates and its association with virulence
Hasan, F., Xess, I., Wang, X., Jain, N., & Fries, B. C. (2009) · Microbes and Infection · doi:10.1016/j.micinf.2009.04.018 · Cited by 206 · see citing works
Vediyappan, G., Rossignol, T., & d'Enfert, C. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01638-09 · Cited by 183 · see citing works
Antifungal therapy with an emphasis on biofilms
Pierce, C. G., Srinivasan, A., Uppuluri, P., Ramasubramanian, A. K., & López-Ribot, J. L. (2013) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2013.08.008 · Cited by 173 · see citing works
The <i>Candida albicans CaACE2</i> gene affects morphogenesis, adherence and virulence
Kelly, M. T., MacCallum, D. M., Clancy, S. D., Odds, F. C., Brown, A. J. P., & Butler, G. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04185.x · Cited by 175 · see citing works
Martins, M., Henriques, M., Lopez‐Ribot, J. L., & Oliveira, R. (2012) · Mycoses · doi:10.1111/j.1439-0507.2011.02047.x · Cited by 174 · see citing works
Fox, E. P., Bui, C. K., Nett, J. E., Hartooni, N., Mui, M. C., Andes, D. R., Nobile, C. J., & Johnson, A. D. (2015) · Molecular Microbiology · doi:10.1111/mmi.13002 · Cited by 173 · see citing works
Klis, F. M., Sosinska, G. J., de Groot, P. W. J., & Brul, S. (2009) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2009.00541.x · Cited by 165 · see citing works
Nett, J. E., Sanchez, H., Cain, M. T., Ross, K. M., & Andes, D. R. (2011) · Eukaryotic Cell · doi:10.1128/ec.05126-11 · Cited by 168 · see citing works
Role for Cell Density in Antifungal Drug Resistance in <i>Candida albicans</i> Biofilms
Perumal, P., Mekala, S., & Chaffin, W. L. (2007) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01237-06 · Cited by 165 · see citing works
Time Course Global Gene Expression Analysis of an In Vivo<i>Candida</i>Biofilm
Nett, J. E., Lepak, A. J., Marchillo, K., & Andes, D. R. (2009) · The Journal of Infectious Diseases · doi:10.1086/599838 · Cited by 162 · see citing works
Evolution of Drug Resistance in <i>Candida Albicans</i>
Cowen, L. E., Anderson, J. B., & Kohn, L. M. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.160907 · Cited by 151 · see citing works
Aspergillus biofilms: clinical and industrial significance
Ramage, G., Rajendran, R., Gutierrez-Correa, M., Jones, B., & Williams, C. (2011) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2011.02381.x · Cited by 136 · see citing works
Lv, Q.-Z., Yan, L., & Jiang, Y.-Y. (2016) · Virulence · doi:10.1080/21505594.2016.1188236 · Cited by 133 · see citing works
Conserved Role for Biofilm Matrix Polysaccharides in <i>Candida auris</i> Drug Resistance
Dominguez, E. G., Zarnowski, R., Choy, H. L., Zhao, M., Sanchez, H., Nett, J. E., & Andes, D. R. (2019) · mSphere · doi:10.1128/mspheredirect.00680-18 · Cited by 132 · see citing works
The characteristics of <i>Aspergillus fumigatus</i> mycetoma development: is this a biofilm?
Mowat, E., Williams, C., Jones, B., Mcchlery, S., & Ramage, G. (2009) · Medical Mycology · doi:10.1080/13693780802238834 · Cited by 131 · see citing works
Candida glabrata Biofilms: How Far Have We Come?
Rodrigues, C., Rodrigues, M., Silva, S., & Henriques, M. (2017) · Journal of Fungi · doi:10.3390/jof3010011 · Cited by 129 · see citing works
Yeast wall protein 1 of Candida albicans
Granger, B. L., Flenniken, M. L., Davis, D. A., Mitchell, A. P., & Cutler, J. E. (2005) · Microbiology · doi:10.1099/mic.0.27663-0 · Cited by 126 · see citing works
Biofilm formation by<b><i>Aspergillus fumigatus</i></b>
Kaur, S., & Singh, S. (2013) · Medical Mycology · doi:10.3109/13693786.2013.819592 · Cited by 128 · see citing works
Iraqui, I., Garcia‐Sanchez, S., Aubert, S., Dromer, F., Ghigo, J., D’Enfert, C., & Janbon, G. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04475.x · Cited by 126 · see citing works
Pierce, C. G., Chaturvedi, A. K., Lazzell, A. L., Powell, A. T., Saville, S. P., McHardy, S. F., & Lopez-Ribot, J. L. (2015) · npj Biofilms and Microbiomes · doi:10.1038/npjbiofilms.2015.12 · Cited by 124 · see citing works
Candida albicans biofilms: building a heterogeneous, drug-tolerant environment
Bonhomme, J., & d’Enfert, C. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.03.007 · Cited by 120 · see citing works
Fungicidal activity of miconazole against Candida spp. biofilms
Vandenbosch, D., Braeckmans, K., Nelis, H. J., & Coenye, T. (2010) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkq019 · Cited by 113 · see citing works
Fox, E. P., & Nobile, C. J. (2012) · Transcription · doi:10.4161/trns.22281 · Cited by 114 · see citing works
Adherence of <i>Candida albicans</i> to Silicone Induces Immediate Enhanced Tolerance to Fluconazole
Mateus, C., Crow, S. A., & Ahearn, D. G. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.9.3358-3366.2004 · Cited by 113 · see citing works
Nobbs, A. H., Vickerman, M. M., & Jenkinson, H. F. (2010) · Eukaryotic Cell · doi:10.1128/ec.00103-10 · Cited by 112 · see citing works
The Transcriptional Regulator Nrg1p Controls Candida albicans Biofilm Formation and Dispersion
Uppuluri, P., Pierce, C. G., Thomas, D. P., Bubeck, S. S., Saville, S. P., & Lopez-Ribot, J. L. (2010) · Eukaryotic Cell · doi:10.1128/ec.00111-10 · Cited by 110 · see citing works
In Vitro and In Vivo Activity of a Novel Antifungal Small Molecule against Candida Infections
Wong, S. S. W., Kao, R. Y. T., Yuen, K. Y., Wang, Y., Yang, D., Samaranayake, L. P., & Seneviratne, C. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085836 · Cited by 107 · see citing works
Role of matrix β-1,3 glucan in antifungal resistance of non-albicans Candida biofilms
Mitchell, K. F., Taff, H. T., Cuevas, M. A., Reinicke, E. L., Sanchez, H., & Andes, D. R. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02378-12 · Cited by 104 · see citing works
Seneviratne, C. J., Wang, Y., Jin, L., Abiko, Y., & Samaranayake, L. P. (2008) · PROTEOMICS · doi:10.1002/pmic.200701097 · Cited by 104 · see citing works
Khot, P. D., Suci, P. A., Miller, R. L., Nelson, R. D., & Tyler, B. J. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00997-06 · Cited by 104 · see citing works
Alves, C. T., Ferreira, I. C., Barros, L., Silva, S., Azeredo, J., & Henriques, M. (2014) · Future Microbiology · doi:10.2217/fmb.13.147 · Cited by 102 · see citing works
Biofilm Formation by <i>Pneumocystis</i> spp
Cushion, M. T., Collins, M. S., & Linke, M. J. (2009) · Eukaryotic Cell · doi:10.1128/ec.00202-08 · Cited by 96 · see citing works
Li, P., Seneviratne, C. J., Alpi, E., Vizcaino, J. A., & Jin, L. (2015) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00543-15 · Cited by 95 · see citing works
Conserved and Divergent Roles of Bcr1 and CFEM Proteins in Candida parapsilosis and Candida albicans
Ding, C., Vidanes, G. M., Maguire, S. L., Guida, A., Synnott, J. M., Andes, D. R., & Butler, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028151 · Cited by 93 · see citing works
Thangamani, S., Maland, M., Mohammad, H., Pascuzzi, P. E., Avramova, L., Koehler, C. M., Hazbun, T. R., & Seleem, M. N. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00004 · Cited by 90 · see citing works
A Histone Deacetylase Complex Mediates Biofilm Dispersal and Drug Resistance in Candida albicans
Nobile, C. J., Fox, E. P., Hartooni, N., Mitchell, K. F., Hnisz, D., Andes, D. R., Kuchler, K., & Johnson, A. D. (2014) · mBio · doi:10.1128/mbio.01201-14 · Cited by 87 · see citing works
“By CSLM, the wild-type reference strain and all four Set3 complex mutant strains formed mature biofilms with typical architecture and thickness (5, 13, 14, 16) after 24 h of development (Fig.”
Background<i>Candida</i> Species: New Insights into Biofilm Formation
Cuéllar-Cruz, M., López-Romero, E., Villagómez-Castro, J. C., & Ruiz-Baca, E. (2012) · Future Microbiology · doi:10.2217/fmb.12.48 · Cited by 80 · see citing works
Gu, W., Guo, D., Zhang, L., Xu, D., & Sun, S. (2016) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.03046-15 · Cited by 80 · see citing works
<i>O</i> -Mannosylation in Candida albicans Enables Development of Interkingdom Biofilm Communities
Dutton, L. C., Nobbs, A. H., Jepson, K., Jepson, M. A., Vickerman, M. M., Aqeel Alawfi, S., Munro, C. A., Lamont, R. J., & Jenkinson, H. F. (2014) · mBio · doi:10.1128/mbio.00911-14 · Cited by 75 · see citing works
Adhesion of<i>Histoplasma capsulatum</i>to pneumocytes and biofilm formation on an abiotic surface
Pitangui, N. S., Sardi, J. C. O., Silva, J. F., Benaducci, T., Moraes da Silva, R. A., Rodríguez-Arellanes, G., Taylor, M. L., Mendes-Giannini, M. J. S., & Fusco-Almeida, A. M. (2012) · Biofouling · doi:10.1080/08927014.2012.703659 · Cited by 69 · see citing works
Turbinmicin inhibits Candida biofilm growth by disrupting fungal vesicle-mediated trafficking
Zhao, M., Zhang, F., Zarnowski, R., Barns, K., Jones, R., Fossen, J., Sanchez, H., Rajski, S. R., Audhya, A., Bugni, T. S., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci145123 · Cited by 62 · see citing works
A common vesicle proteome drives fungal biofilm development
Zarnowski, R., Sanchez, H., Jaromin, A., Zarnowska, U. J., Nett, J. E., Mitchell, A. P., & Andes, D. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2211424119 · Cited by 63 · see citing works
The role of antifungals against Candida biofilm in catheter-related candidemia
Bouza, E., Guinea, J., & Guembe, M. (2014) · Antibiotics · doi:10.3390/antibiotics4010001 · Cited by 62 · see citing works
Johnson, C. J., Kernien, J. F., Hoyer, A. R., & Nett, J. E. (2017) · Scientific Reports · doi:10.1038/s41598-017-13588-6 · Cited by 58 · see citing works
Rat Indwelling Urinary Catheter Model of Candida albicans Biofilm Infection
Nett, J. E., Brooks, E. G., Cabezas-Olcoz, J., Sanchez, H., Zarnowski, R., Marchillo, K., & Andes, D. R. (2014) · Infection and Immunity · doi:10.1128/iai.02284-14 · Cited by 58 · see citing works
Paiva, L. C. F., Vidigal, P. G., Donatti, L., Svidzinski, T. I. E., & Consolaro, M. E. L. (2012) · Micron · doi:10.1016/j.micron.2011.09.013 · Cited by 55 · see citing works
Antimicrobial Properties of Antidepressants and Antipsychotics—Possibilities and Implications
Caldara, M., & Marmiroli, N. (2021) · Pharmaceuticals · doi:10.3390/ph14090915 · Cited by 54 · see citing works
Gong, S.-Q., Epasinghe, J., Rueggeberg, F. A., Niu, L.-N., Mettenberg, D., Yiu, C. K. Y., Blizzard, J. D., Wu, C. D., Mao, J., Drisko, C. L., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042355 · Cited by 53 · see citing works
Antifungal therapy of Candida biofilms: Past, present and future
Ajetunmobi, O. H., Badali, H., Romo, J. A., Ramage, G., & Lopez-Ribot, J. L. (2023) · Biofilm · doi:10.1016/j.bioflm.2023.100126 · Cited by 52 · see citing works
O'Connor, L., Lahiff, S., Casey, F., Glennon, M., Cormican, M., & Maher, M. (2005) · Molecular and Cellular Probes · doi:10.1016/j.mcp.2004.10.007 · Cited by 53 · see citing works
Efungumab and caspofungin: pre-clinical data supporting synergy.
Hodgetts, S., Nooney, L., Al-Akeel, R., Curry, A., Awad, S., Matthews, R., & Burnie, J. (2008) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkn075 · Cited by 51 · see citing works
Candida glabrata susceptibility to antifungals and phagocytosis is modulated by acetate
Mota, S., Alves, R., Carneiro, C., Silva, S., Brown, A. J., Istel, F., Kuchler, K., Sampaio, P., Casal, M., Henriques, M., et al. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00919 · Cited by 49 · see citing works
- Authors
- Chandra, J., Kuhn, D. M., Mukherjee, P. K., Hoyer, L. L., McCormick, T., & Ghannoum, M. A.
- Affiliations
- University Hospitals of Cleveland (US)
- University of Illinois Urbana-Champaign (US)
- Case Western Reserve University (US)
- ORCID
- Venue
- Journal of Bacteriology
- Publisher
- American Society for Microbiology
- Published
- 2001-09-15
- Volume
- 183
- Issue
- 18
- Pages
- 5385-5394
- ISSN
- 0021-9193 (ISSN-L)
- 1098-5530
- PMC
- PMC95423
- OpenAlex
- W2125848302
- Cited by
- 1,578
- References
- 51
- Citations by year
- 2026: 36 · 2025: 48 · 2024: 48 · 2023: 71 · 2022: 68 · 2021: 88 · 2020: 77 · 2019: 84 · 2018: 73 · 2017: 94 · 2016: 89 · 2015: 81 · 2014: 102 · 2013: 78 · 2012: 83
- FWCI
- 16.98
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Bacteriology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (R01AI035097, AI36219, AI35097-03, AIO7024, P30AI036219)
- National Institute of Dental and Craniofacial Research (R01-DE13992, R01DE013992)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- Candida albicans, biofilm formation, antifungal resistance, biofilm structure, planktonic versus biofilm growth, fungal adhesion, Saccharomyces cerevisiae comparison
- MeSH terms
- Antifungal Agents, Candida albicans, Candidiasis, Drug Resistance, Microbial, Fungal Proteins, Humans, Microbial Sensitivity Tests, Silicones, Gene Expression Regulation, Fungal, Biofilms, Microscopy, Confocal, Polymethyl Methacrylate
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review