The DOI matches its Crossref record; 53 of the 53 references it cites were found in a registry or an index.
Candida albicans biofilms: building a heterogeneous, drug-tolerant environment
Abstract
Fungi are able to form biofilms on medical implants, causing serious infections. A better understanding of fungal biofilm formation is necessary to develop tools for detection or prevention and to identify new antifungal strategies. This review explores recent advances in the characterization at the molecular level of fungal biofilms, especially those formed by the yeast Candida albicans: the identification of complex transcriptional networks that control their formation; the pivotal role of the extracellular matrix in biofilm antifungal tolerance; and the knowledge gained on the physiology of biofilm cells and heterogeneity within these communities. These findings may help develop new, targeted therapeutic strategies.
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“In addition to the 6 master transcriptional regulators discussed above, another 44 transcriptional regulators have been identified; if any of these is deleted, some aspect of C. albicans biofilm formation is affected under at least one condition (Table 1; revised from 61 and 18).”
From Candida albicans Biofilms and Human Disease (2015) · cites this paper as [18]
In the citing paper
“Current antifungal drugs have only two specific targets (ergosterol biosynthesis and 1,3-β-D-glucan synthesis)”
From Candida albicans Biofilms and Human Disease (2015) · cites this paper as [18]
In the citing paper
“and it is widely believed that antifungal drugs with new mechanisms of action are needed (4, 18, 79).”
From Candida albicans Biofilms and Human Disease (2015) · cites this paper as [18]
Citations
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
Flemming, H.-C., & Wingender, J. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2415 · Cited by 10,137
Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms
Donlan, R. M., & Costerton, J. W. (2002) · Clinical Microbiology Reviews · doi:10.1128/cmr.15.2.167-193.2002 · Cited by 6,644
Biofilms as Complex Differentiated Communities
Stoodley, P., Sauer, K., Davies, D. G., & Costerton, J. W. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.160705 · Cited by 3,151
Physiological heterogeneity in biofilms
Stewart, P. S., & Franklin, M. J. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1838 · Cited by 2,483
Chandra, J., Kuhn, D. M., Mukherjee, P. K., Hoyer, L. L., McCormick, T., & Ghannoum, M. A. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.18.5385-5394.2001 · Cited by 1,578
Evolving concepts in biofilm infections
Hall‐Stoodley, L., & Stoodley, P. (2009) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01323.x · Cited by 1,138
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
Genetic control of Candida albicans biofilm development
Finkel, J. S., & Mitchell, A. P. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2475 · Cited by 641
Biofilm formation by Candida species on the surface of catheter materials in vitro
Hawser, S. P., & Douglas, L. J. (1994) · Infection and Immunity · doi:10.1128/iai.62.3.915-921.1994 · Cited by 599
Ramage, G., Rajendran, R., Sherry, L., & Williams, C. (2012) · International Journal of Microbiology · doi:10.1155/2012/528521 · Cited by 583
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
Candida albicans 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
Critical 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
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
Putative Role of β-1,3 Glucans in Candida albicans 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
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 402
Baillie, G. S. (2000) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/46.3.397 · Cited by 389
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
Self-citationBiofilm Matrix Regulation by Candida albicans Zap1
Nobile, C. J., Nett, J. E., Hernday, A. D., Homann, O. R., Deneault, J.-S., Nantel, A., Andes, D. R., Johnson, A. D., & Mitchell, A. P. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000133 · Cited by 337
Ramage, G., VandeWalle, K., López-Ribot, J. L., & Wickes, B. L. (2002) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(02)00853-4 · Cited by 334
Looking for Chinks in the Armor of Bacterial Biofilms
Monroe, D. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050307 · Cited by 302
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
Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans
Askew, C., Sellam, A., Epp, E., Hogues, H., Mullick, A., Nantel, A., & Whiteway, M. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000612 · Cited by 260
Genetic Basis of Candida Biofilm Resistance Due to Drug‐Sequestering Matrix Glucan
Nett, J. E., Sanchez, H., Cain, M. T., & Andes, D. R. (2010) · The Journal of Infectious Diseases · doi:10.1086/651200 · Cited by 250
Ramage, G., VandeWalle, K., Bachmann, S. P., Wickes, B. L., & Lopez-Ribot, J. L. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.46.11.3634-3636.2002 · Cited by 238
Portrait of Candida albicans Adherence Regulators
Finkel, J. S., Xu, W., Huang, D., Hill, E. M., Desai, J. V., Woolford, C. A., Nett, J. E., Taff, H., Norice, C. T., Andes, D. R., et al. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002525 · Cited by 228
Kumamoto, C. A. (2002) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(02)00371-5 · Cited by 217
Nett, J. E., Crawford, K., Marchillo, K., & Andes, D. R. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00227-10 · Cited by 207
Vediyappan, G., Rossignol, T., & d'Enfert, C. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01638-09 · Cited by 183
Self-citationThe Candida albicans CaACE2 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
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
Time Course Global Gene Expression Analysis of an In Vivo Candida 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
Genome-Wide Transcription Profiling of the Early Phase of Biofilm Formation by Candida albicans
Murillo, L. A., Newport, G., Lan, C., Habelitz, S., Dungan, J. M., & Agabian, N. M. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.9.1562-1573.2005 · Cited by 149
Bonhomme, J., Chauvel, M., Goyard, S., Roux, P., Rossignol, T., & d'Enfert, C. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07626.x · Cited by 144
Self-citationTemporal analysis of Candida albicans gene expression during biofilm development
Yeater, K. M., Chandra, J., Cheng, G., Mukherjee, P. K., Zhao, X., Rodriguez‐Zas, S. L., Kwast, K. E., Ghannoum, M. A., & Hoyer, L. L. (2007) · Microbiology · doi:10.1099/mic.0.2007/006163-0 · Cited by 140
Čáp, M., Štěpánek, L., Harant, K., Váchová, L., & Palková, Z. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.04.001 · Cited by 138
The characteristics of Aspergillus fumigatus 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
Gibbons, J. G., Beauvais, A., Beau, R., McGary, K. L., Latgé, J., & Rokas, A. (2011) · Eukaryotic Cell · doi:10.1128/ec.05102-11 · Cited by 115
Divergent Targets of Candida albicans Biofilm Regulator Bcr1 In Vitro and In Vivo
Fanning, S., Xu, W., Solis, N., Woolford, C. A., Filler, S. G., & Mitchell, A. P. (2012) · Eukaryotic Cell · doi:10.1128/ec.00103-12 · Cited by 106
Hnisz, D., Bardet, A. F., Nobile, C. J., Petryshyn, A., Glaser, W., Schöck, U., Stark, A., & Kuchler, K. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003118 · Cited by 100
Hypoxic Adaptation by Efg1 Regulates Biofilm Formation by Candida albicans
Stichternoth, C., & Ernst, J. F. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.00098-09 · Cited by 97
Correlation between Biofilm Formation and the Hypoxic Response in Candida parapsilosis
Rossignol, T., Ding, C., Guida, A., d’Enfert, C., Higgins, D. G., & Butler, G. (2009) · Eukaryotic Cell · doi:10.1128/ec.00350-08 · Cited by 93
Self-citationβ‐1,3 Glucan as a Test for Central Venous Catheter Biofilm Infection
Nett, J. E., Lincoln, L. M., Marchillo, K., & Andes, D. R. (2007) · The Journal of Infectious Diseases · doi:10.1086/517522 · Cited by 93
Ding, C., & Butler, G. (2007) · Eukaryotic Cell · doi:10.1128/ec.00136-07 · Cited by 83
Target specificity of the Candida albicans Efg1 regulator
Lassak, T., Schneider, E., Bussmann, M., Kurtz, D., Manak, J. R., Srikantha, T., Soll, D. R., & Ernst, J. F. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07837.x · Cited by 76
Zap1 Control of Cell-Cell Signaling in Candida albicans Biofilms
Ganguly, S., Bishop, A. C., Xu, W., Ghosh, S., Nickerson, K. W., Lanni, F., Patton, J. L., & Mitchell, A. P. (2011) · Eukaryotic Cell · doi:10.1128/ec.05196-11 · Cited by 66
The RAM network in pathogenic fungi
Saputo, S., Chabrier-Rosello, Y., Luca, F. C., Kumar, A., & Krysan, D. J. (2012) · Eukaryotic Cell · doi:10.1128/ec.00044-12 · Cited by 65
Bharucha, N., Chabrier‐Roselló, Y., Xu, T., Johnson, C., Sobczynski, S., Song, Q., Dobry, C. J., Eckwahl, M. J., Anderson, C. P., Benjamin, A. J., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002058 · Cited by 50
Petti, A. A., McIsaac, R. S., Ho-Shing, O., Bussemaker, H. J., & Botstein, D. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-03-0233 · Cited by 41
Traven, A., Jänicke, A., Harrison, P. F., Swaminathan, A., Seemann, T., & Beilharz, T. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046243 · Cited by 36
Gutiérrez-Escribano, P., Zeidler, U., Suárez, M. B., Bachellier‐Bassi, S., Clemente‐Blanco, A., Bonhomme, J., de Aldana, C. R. V., d’Enfert, C., & Correa‐Bordes, J. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002683 · Cited by 35
Self-citationCandida albicans survival and biofilm formation under starvation conditions
Ning, Y., Hu, X., Ling, J., Du, Y., Liu, J., Liu, H., & Peng, Z. (2012) · International Endodontic Journal · doi:10.1111/j.1365-2591.2012.02094.x · Cited by 24
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“The biofilm cells form a hypoxic environment and increase the expression of genes involved in glycolysis, fatty acid metabolism, and ergosterol synthesis [45].”
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Metadata
- Authors
- Bonhomme, J., & d’Enfert, C.
- Affiliations
- Centre Hospitalier Universitaire de Caen Normandie (FR)
- Institut Pasteur (FR)
- Corresponding author
- d’Enfert, Christophe
- Venue
- Current Opinion in Microbiology
- Publisher
- Elsevier BV
- Published
- 2013-08
- Volume
- 16
- Issue
- 4
- Pages
- 398-403
- ISSN
- 1369-5274 (ISSN-L)
- OpenAlex
- W2077255553
- Cited by
- 120
- References
- 53
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 7 · 2023: 7 · 2022: 1 · 2021: 8 · 2020: 4 · 2019: 11 · 2018: 11 · 2017: 9 · 2016: 12 · 2015: 16 · 2014: 16 · 2013: 6
- FWCI
- 2.21
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Current Opinion in Microbiology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-08-MIE-033-01, ANR-10-01)
- French Government's Investissement d’Avenir program, Laboratoire d’Excellence (ANR-10-LABX-62-IBEID)
- European Commission (PITN-GA-2008-214004)
- Fondation pour la Recherche Médicale (DEA20080713005)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Keywords
- Candida albicans, fungal biofilms, biofilm heterogeneity, antifungal drug tolerance, extracellular matrix, transcriptional regulatory networks, biofilm physiology, medical device infections
- MeSH terms
- Antifungal Agents, Candida albicans, Drug Tolerance, Biofilms
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