The DOI matches its Crossref record; 35 of the 35 references it cites were found in a registry or an index.
Candida albicans forms biofilms on the vaginal mucosa
Open accessAbstract
Current understanding of resistance and susceptibility to vulvovaginal candidiasis challenges existing paradigms of host defence against fungal infection. While abiotic biofilm formation has a clearly established role during systemic Candida infections, it is not known whether C. albicans forms biofilms on the vaginal mucosa and the possible role of biofilms in disease. In vivo and ex vivo murine vaginitis models were employed to examine biofilm formation by scanning electron and confocal microscopy. C. albicans strains included 3153A (lab strain), DAY185 (parental control strain), and mutants defective in morphogenesis and/or biofilm formation in vitro (efg1/efg1 and bcr1/bcr1). Both 3153A and DAY815 formed biofilms on the vaginal mucosa in vivo and ex vivo as indicated by high fungal burden and microscopic analysis demonstrating typical biofilm architecture and presence of extracellular matrix (ECM) co-localized with the presence of fungi. In contrast, efg1/efg1 and bcr1/bcr1 mutant strains exhibited weak or no biofilm formation/ECM production in both models compared to wild-type strains and complemented mutants despite comparable colonization levels. These data show for the first time that C. albicans forms biofilms in vivo on vaginal epithelium, and that in vivo biotic biofilm formation requires regulators of biofilm formation (BCR1) and morphogenesis (EFG1).
Overview
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
Verification
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?
In the citing paper
“Vaginal mucosal mouse models, both in vivo (live mice inoculated with C. albicans on the vaginal mucosa) and ex vivo (vaginas excised from euthanized mice and then inoculated with C. albicans in tissue culture plates), show similar biofilm architectures, with clear yeast, hyphae, and extracellular matrix evident throughout the biofilms formed on top of the mucosal layers (72).”
From Candida albicans Biofilms and Human Disease (2015) · cites this paper as [72]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Nonfilamentous C. albicans Mutants Are Avirulent
Lo, H.-J., Köhler, J. R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A., & Fink, G. R. (1997) · Cell · doi:10.1016/s0092-8674(00)80358-x · Cited by 1,809
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
Candida 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 · cited 2×
“Significant attention has been given to Candida biofilm formation of indwelling catheters, which can lead to life-threatening systemic infections (Crump & Collignon, 2000; Dominic et al., 2007; Kojic & Darouiche, 2004).”
Owen, D. H., & Katz, D. F. (1999) · Contraception · doi:10.1016/s0010-7824(99)00010-4 · Cited by 721 · cited 1×
“Second, in vivo vaginal tissue 3640 Microbiology 156 contains many secretions, composed of electrolytes, organic acids and proteins, which maintain properties such as pH and osmolarity (Owen & Katz, 1999).”
Vulvovaginal candidiasis: Epidemiologic, diagnostic, and therapeutic considerations
Sobel, J. D., Faro, S., Force, R. W., Foxman, B., Ledger, W. J., Nyirjesy, P., Reed, B. D., & Summers, P. R. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)80001-x · Cited by 694 · cited 2×
“Although several Candida species have been implicated in VVC and RVVC, Candida albicans is the predominant aetiological agent, causing 85– 95 % of these infections (Sobel et al., 1998).”
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 · cited 1×
“Our results are also consistent with the kinetics of in vitro biofilms grown on silicone discs, which show steady increases in dry weight measurements until 36–48 h and then remain stationary (Chandra et al., 2001; Hawser & Douglas, 1994).”
Stoldt, V. R., Sonneborn, A., Leuker, C. E., & Ernst, J. F. (1997) · The EMBO Journal · doi:10.1093/emboj/16.8.1982 · Cited by 595 · cited 1×
“EFG1 encodes a transcriptional factor that is required for morphogenesis under most hypha-inducing conditions in vitro (Lo et al., 1997; Stoldt et al., 1997).”
BackgroundCandida 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 · cited 1×
“Candida biofilms have been studied primarily on abiotic surfaces (reviewed by Blankenship & Mitchell, 2006; Ramage et al., 2006).”
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 · cited 2×
“At 72 h, yeast forms (CM) were evident at the apical surface of the biofilm in conjunction with the residential hyphae, which coincided with the predicted dispersal phase of biofilm growth (Blankenship & Mitchell, 2006).”
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 · cited 6×
“…biofilm formation, i.e. ECM production and hyphal growth. http://mic.sgmjournals.org 3641 BCR1 encodes a transcriptional regulator that is required for production of vigorous biofilms on abiotic surfaces in vitro and in vivo in a catheter model (Nobile et al., 2006a; Nobile & Mitchell, 2005).”
Influential
Research works printed but not linked: 1
- 1999, SBIR/STTR study and control of microbial biofilms
Cited by
Sorted by citations
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
“Most infections result from pathogenic biofilms; therefore, the biomedical significance of biofilms is substantial (Ganguly & Mitchell, 2011; Harriott et al., 2010).”
BackgroundCandida albicans 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
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
“albicans in 166 tissue culture plates) also show similar biofilm architectures with yeast cells, hyphae, 167 and extracellular matrix evident throughout the biofilms, formed on top of mucosal 168 layers [18].”
BackgroundResistance of Candida to azoles and echinocandins worldwide
Pristov, K. E., & Ghannoum, M. A. (2019) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2019.03.028 · Cited by 706
“Biofilms allow the cells to adhere to and proliferate onmedically implanted devices as well as host tissue, causing infections [10,18,19].”
BackgroundGenetic control of Candida albicans biofilm development
Finkel, J. S., & Mitchell, A. P. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2475 · Cited by 641
“albicans produces dense three-dimensional biofilms that are embedded in extracellular matrix materia”
Development and regulation of single- and multi-species Candida albicans biofilms
Lohse, M. B., Gulati, M., Johnson, A. D., & Nobile, C. J. (2018) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.107 · Cited by 643
Ramage, G., Rajendran, R., Sherry, L., & Williams, C. (2012) · International Journal of Microbiology · doi:10.1155/2012/528521 · Cited by 583
“In addition, there are now also a significant number of biofilm models available for in vivo investigations, and many of these have been utilised to elucidate biofilm resistance mechanisms [83], including an implanted chamber under the skin [71], catheter models [84, 85], vaginal model [86], and denture model [87].”
BackgroundFrom in vitro to in vivo Models of Bacterial Biofilm-Related Infections
Lebeaux, D., Chauhan, A., Rendueles, O., & Beloin, C. (2013) · Pathogens · doi:10.3390/pathogens2020288 · Cited by 574
Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors
Gonçalves, B., Ferreira, C., Alves, C. T., Henriques, M., Azeredo, J., & Silva, S. (2016) · Critical Reviews in Microbiology · doi:10.3109/1040841x.2015.1091805 · Cited by 669
“Concerning the vaginal environment, Candida species can form biofilms on vaginal epithelium (Harriott et al., 2010) and have high capacity to produce biofilms on IUDs promoting VVC (Chassot et al., 2008; Lal et al., 2008).”
BackgroundInfluentialPathogenesis ofCandida albicansbiofilm
Tsui, C., Kong, E. F., & Jabra‐Rizk, M. A. (2016) · Pathogens and Disease · doi:10.1093/femspd/ftw018 · Cited by 522
“…properties of C. albicans have been proposed to play major roles in causing recurring VVC; notably, strains of C. albicans defective in hyphae formation display significantly reduced vaginitis symptomatology indicating a requirement for hyphae in the pathogenesis of disease (Harriott et al. 2010).”
BackgroundFanning, S., & Mitchell, A. P. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002585 · Cited by 465
In vitro and in vivo model systems to study microbial biofilm formation
Coenye, T., & Nelis, H. J. C. F. (2010) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2010.08.018 · Cited by 465
Vulvovaginal Candidiasis: A Current Understanding and Burning Questions
Willems, H. M. E., Ahmed, S. S., Liu, J., Xu, Z., & Peters, B. M. (2020) · Journal of Fungi · doi:10.3390/jof6010027 · Cited by 357
“albicans to the mucosal epithelium and are important for mature biofilm formation in the vagina as deletion of the master adhesin regulator BCR1 impaired biofilm formation in vivo [60].”
BackgroundImportance of Candida–bacterial polymicrobial biofilms in disease
Harriott, M. M., & Noverr, M. C. (2011) · Trends in Microbiology · doi:10.1016/j.tim.2011.07.004 · Cited by 325
“To this end, in vivo and ex vivo murine vaginitis models were recently used to examine mucosal biofilm formation by scanning electron and confocal microscopy [17].”
BackgroundSelf-citationCandida Species Biofilms’ Antifungal Resistance
Silva, S. M., Rodrigues, C. F., Araújo, D., Rodrigues, M. E., & Henriques, M. (2017) · Journal of Fungi · doi:10.3390/jof3010008 · Cited by 317
Kong, E. F., Tsui, C., Kucharíková, S., Andes, D. R., Dijck, P. V., & Jabra‐Rizk, M. A. (2016) · mBio · doi:10.1128/mbio.01365-16 · Cited by 305
“albicans and staphylococcus mixed biofilms has been reported, the mechanism and specific factors behind these observations remain undefined (40, 41).”
BackgroundNanotechnology-based drug delivery systems for control of microbial biofilms: a review
Ramos, M. A. D. S., da Silva, P. B., Spósito, L., de Toledo, L. G., Bonifácio, B., Rodero, C. F., dos Santos, K. C., Chorilli, M., & Bauab, T. M. (2018) · International Journal of Nanomedicine · doi:10.2147/ijn.s146195 · Cited by 286
“However, the number of CFU after 24 and 48 h of exposure of the biofilm to AgNPs was significantly different only in C. albicans strain 324LA/94.”
Kalia, N., Singh, J., & Kaur, M. (2020) · Annals of Clinical Microbiology and Antimicrobials · doi:10.1186/s12941-020-0347-4 · Cited by 308
Candida albicans biofilms and polymicrobial interactions
Ponde, N. O., Lortal, L., Ramage, G., Naglik, J. R., & Richardson, J. P. (2021) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2020.1843400 · Cited by 281
“…and on the mucosal surfaces of the oral cavity, conflicting observations have been made regarding the formation of biofilms on the vaginal mucosa (Harriott et al. 2010; Paiva et al. 2012; Sherry et al. 2017; Noverr and Fidel 2019; Swidsinski et al. 2019; Xu et al. 2019), suggesting that…”
BackgroundFungal 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
“Consistent with this idea, Noverr and colleagues have shown that Bcr1 is required for matrix accumulation in a vaginal colonization model (Harriott et al. 2010).”
Fungal Biofilms and Polymicrobial Diseases
Costa-Orlandi, C. B., Sardi, J. D. C. O., Pitangui, N. D. S., de Oliveira, H. C., Scorzoni, L., Galeane, M. C., Medina‐Alarcón, K. P., Melo, W., Marcelino, M., Braz, J. D., et al. (2017) · Journal of Fungi · doi:10.3390/jof3020022 · Cited by 247
“This yeast can grow as biofilm on biotic surfaces during oral, oropharyngeal, and vulvovaginal infection [149,155].”
BackgroundMucosal biofilms of Candida albicans
Ganguly, S., & Mitchell, A. P. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2011.06.001 · Cited by 200
Vulvovaginal C andida albicans infections: pathogenesis, immunity and vaccine prospects
Cassone, A. (2014) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.12994 · Cited by 206
The vaginal mycobiome: A contemporary perspective on fungi in women's health and diseases
Bradford, L. L., & Ravel, J. (2016) · Virulence · doi:10.1080/21505594.2016.1237332 · Cited by 192
Candida albicans Pathogenesis: Fitting within the Host-Microbe Damage Response Framework
Jabra‐Rizk, M. A., Kong, E. F., Tsui, C., Nguyen, M. H., Clancy, C. J., Fidel, P. L., & Noverr, M. C. (2016) · Infection and Immunity · doi:10.1128/iai.00469-16 · Cited by 191
“These include oral epithelial cells via annexin-A1 and CD8 T cells, although the mechanisms are not well understood (37, 53, 54).”
BackgroundSelf-citationHyphal Growth in Human Fungal Pathogens and Its Role in Virulence
Brand, A. (2011) · International Journal of Microbiology · doi:10.1155/2012/517529 · Cited by 184
“albicans are the primary cause of mucosal infection in susceptible humans, where the plaques formed by overproliferation of adhered cells to vaginal or oral epithelia are easily visible [38, 43].”
Peters, B. M., Palmer, G. E., Nash, A. K., Lilly, E. A., Fidel, P. L., & Noverr, M. C. (2013) · Infection and Immunity · doi:10.1128/iai.01417-13 · Cited by 169
“Despite knowing that these transcription factors are presumably activated during vaginal infection (by evidence of biofilm formation on the vaginal epithelium), there exists a significant gap in knowledge as to the effects of fungal morphogenesis on the immunopathogenesis of vaginitis (14).”
BackgroundSelf-citationCandida Biofilms: Development, Architecture, and Resistance
Chandra, J., & Mukherjee, P. K. (2015) · Microbiology Spectrum · doi:10.1128/microbiolspec.mb-0020-2015 · Cited by 177
“albicans can also form biofilms on the vaginal mucosa, with typical biofilm composition of yeast and hyphal cells embedded in an extracellular matrix; this vaginal biofilm model was replicated in immunocompetent estradiol-treated mice (50).”
BackgroundMuzny, C. A., & Schwebke, J. R. (2015) · Clinical Infectious Diseases · doi:10.1093/cid/civ353 · Cited by 165
Candida Vaginitis: When Opportunism Knocks, the Host Responds
Peters, B. M., Yano, J., Noverr, M. C., & Fidel, P. L. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1003965 · Cited by 153
“albicans forms biofilms on the vaginal mucosa of mice but biofilm formation is not required for colonization [29].”
BackgroundSelf-citationThe Interface between Fungal Biofilms and Innate Immunity
Kernien, J. F., Snarr, B. D., Sheppard, D. C., & Nett, J. E. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01968 · Cited by 158
“Both vaginal and oral mucosal surfaces promote biofilm formation as well (16, 61).”
BackgroundTerraf, M. C. L., Tomás, M. S. J., Nader-Macı́as, M. E., & Silva, C. N. (2012) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2012.05429.x · Cited by 138
“Escherichia coli and Candida albicans have been reported in vivo biofilms in women with urinary or vaginal infections (Harriott et al. 2010; McMillan et al. 2011).”
BackgroundTackling Fungal Resistance by Biofilm Inhibitors
Wu, S., Wang, Y., Liu, N., Dong, G., & Sheng, C. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.6b01203 · Cited by 134
Biofilms and vulvovaginal candidiasis
Rodríguez‐Cerdeira, C., Carnero-Gregorio, M., Molares-Vila, A., López-Bárcenas, A., Fabbrocini, G., Bardhi, B., Sinani, A., Sánchez-Blanco, E., Arenas, R., & Hernández‐Castro, R. (2018) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2018.11.011 · Cited by 159
Gao, M. H., Hui, W., & Zhu, L. (2016) · Cellular Physiology and Biochemistry · doi:10.1159/000453134 · Cited by 135
Neutrophil extracellular traps in fungal infection
Urban, C. F., & Nett, J. E. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.03.020 · Cited by 130
“Biofilms commonly propagate on surfaces of medical devices, such as vascular catheters, urinary catheters, and ventricular fluid shunts (76–79), as well as mucosal surfaces (80, 81).”
BackgroundThe role of fungi in fungal keratitis
Mills, B., Radhakrishnan, N., Karthikeyan, R. S. G., Rameshkumar, G., Lalitha, P., & Prajna, N. V. (2020) · Experimental Eye Research · doi:10.1016/j.exer.2020.108372 · Cited by 120
Pathogenesis and Clinical Relevance of Candida Biofilms in Vulvovaginal Candidiasis
Rodríguez‐Cerdeira, C., Martínez-Herrera, E. O., Carnero-Gregorio, M., López-Bárcenas, A., Fabbrocini, G., Fida, M., El-Samahy, M., & González-Cespón, J. L. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.544480 · Cited by 132
Fazly, A., Jain, C. M., Dehner, A. C., Issi, L., Lilly, E. A., Ali, A., Cao, H., Fidel, P. L., Rao, R. P., & Kaufman, P. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305982110 · Cited by 119
“This system is ideal for evaluating our compounds, because VVC infections depend on fungal morphogenesis and biofilm formation (35).”
BackgroundSelf-citationDivergent 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
“Findings from these studies have underscored the utility of this perspective, in that there are several common genetic requirements for the formation of abiotic surface biofilms and mucosal infections (10, 11, 15, 19).”
BackgroundDwivedi, P., Thompson, A., Xie, Z., Kashleva, H., Ganguly, S., Mitchell, A. P., & Dongari-Bagtzoglou, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016218 · Cited by 110
“with results in the mouse vaginal mucosa model [16], we found that the bcr1/bcr1 strain was deficient in forming a clinically visible mucosal biofilm on the tongues of immunocompromised mice in vivo (Fig.”
BackgroundResultAntifungal Susceptibility and Biofilm Production of Candida spp. Isolated from Clinical Samples
Marak, M. B., & Dhanashree, B. (2018) · International Journal of Microbiology · doi:10.1155/2018/7495218 · Cited by 107
“Biofilms are the group of microorganisms that are embedded in an extracellular matrix (ECM), forming a complex three-dimensional architecture on biotic and abiotic surfaces [6].”
BackgroundNovel Mechanism behind the Immunopathogenesis of Vulvovaginal Candidiasis: “Neutrophil Anergy”
Yano, J., Peters, B. M., Noverr, M. C., & Fidel, P. L. (2017) · Infection and Immunity · doi:10.1128/iai.00684-17 · Cited by 107
“Other hypha-associated virulence factors studied in vaginitis include the agglutinin-like sequence (ALS) genes that regulate mucosal tissue attachment (48–50) and biofilm formation on vaginal mucosa (51), which seemingly play minor roles in the immunopathogenic response.”
BackgroundSelf-citationAlves, 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
Czechowicz, P., Nowicka, J., & Gościniak, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23115895 · Cited by 122
“Classically, the process of forming this structure is divided into four phases: early (adhesion), intermediate (multiplication, filamentation, and ECM production), maturation, and spreading (dispersion) [8,44,69,71,75].”
BackgroundInfluentialCandida and its dual lifestyle as a commensal and a pathogen
Cauchie, M., Desmet, S., & Lagrou, K. (2017) · Research in Microbiology · doi:10.1016/j.resmic.2017.02.005 · Cited by 101
Fungal Quorum-Sensing Molecules: A Review of Their Antifungal Effect against Candida Biofilms
Kovács, R., & Majoros, L. (2020) · Journal of Fungi · doi:10.3390/jof6030099 · Cited by 99
CandidaBiofilms and the Host: Models and New Concepts for Eradication
Tournu, H., & Dijck, P. V. (2011) · International Journal of Microbiology · doi:10.1155/2012/845352 · Cited by 94
“albicans can also form biofilms on the vaginal mucosa, illustrated by two in vivo and ex vivo models in immunocompetent estradiol-treated mice [69].”
BackgroundHemizygosity Enables a Mutational Transition Governing Fungal Virulence and Commensalism
Liang, S.-H., Anderson, M. Z., Hirakawa, M. P., Wang, J. M., Frazer, C., Alaalm, L., Thomson, G. J., Ene, I. V., & Bennett, R. J. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2019.01.005 · Cited by 88
“As evidenced here, the efg1 null state also provides a fitness advantage in several infection types, yet previous work has established that EFG1 function is critical for infection of other host niches (Harriott et al., 2010; Stoldt et al., 1997; Yano et al., 2016).”
BackgroundSwidsinski, A., Guschin, A. E., Tang, Q.-L., Dörffel, Y., Verstraelen, H., Tertychnyy, A. S., Khayrullina, G., Luo, X., Sobel, J. D., & Jiang, X. (2018) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2018.10.023 · Cited by 88
“The only publication claiming Candida albicans forms biofilms on the vaginal mucosa exclusively includes pictures of smears from vagina without vaginal epithelium.(13) Confirmation of the presence of Candida mucosal biofilm in vivo is thus lacking.”
BackgroundThe Extracellular Matrix of Fungal Biofilms
Mitchell, K. F., Żarnowski, R., & Andes, D. R. (2016) · Advances in experimental medicine and biology · doi:10.1007/5584_2016_6 · Cited by 93
Ardizzoni, A., Wheeler, R. T., & Pericolini, E. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.692491 · Cited by 89
Clinical Implications of Oral Candidiasis: Host Tissue Damage and Disseminated Bacterial Disease
Kong, E. F., Kucharíková, S., Dijck, P. V., Peters, B. M., Shirtliff, M. E., & Jabra‐Rizk, M. A. (2014) · Infection and Immunity · doi:10.1128/iai.02843-14 · Cited by 84
“It is important to note, however, that although individuals with immune suppression are the most vulnerable, other mundane factors are also considered risk factors for candidiasis; these factors include steroid and antibiotic usage, hormonal imbalances, nutritional deficiency, age, diabetes, metabolic disorders, and d…”
BackgroundSherry, L., Kean, R., McKloud, E., O’Donnell, L. E., Metcalfe, R., Jones, B., & Ramage, G. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01065-17 · Cited by 84
“beginning to consider them to be important determinants of disease (13, 14), further”
BackgroundYano, J., Noverr, M. C., & Fidel, P. L. (2017) · mBio · doi:10.1128/mbio.00211-17 · Cited by 84
“albicans has been shown to form biofilms on the vaginal mucosa in mice (47), PMNs may exert reduced killing activity, as has been shown in vitro and with other in vivo candidiasis models (48–50).”
BackgroundSelf-citationBioactive Peptides Against Fungal Biofilms
Oshiro, K. G. N., Rodrigues, G. R., Monges, B. E. D., Cardoso, M. H. E. S., & Franco, O. L. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02169 · Cited by 85
“(Capilla et al., 2007; Hohl, 2014; Dijck et al., 2018).”
InfluentialGaziano, R., Sabbatini, S., & Monari, C. (2023) · Microorganisms · doi:10.3390/microorganisms11051211 · Cited by 84
Janeczko, M., Masłyk, M., Kubiński, K., & Golczyk, H. (2017) · Yeast · doi:10.1002/yea.3230 · Cited by 80
“Most cases of these infections are caused by C. albicans (Harriott et al., 2010).”
BackgroundO -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
“The outer cell wall layer is comprised principally of mannoproteins which are embedded in a polysaccharide skeleton provided by -(1,3)- and -(1,6)-linked glucan chains and covalently linked chitin (18).”
BackgroundWu, X., Zhang, S., Li, H., Shen, L., Dong, C., Sun, Y., Chen, H., Xu, B., Zhuang, W., Deighton, M. A., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01117 · Cited by 80
Ismaila, A. A., Ahmad, K., Siddique, Y., Wahab, M. A. A., Kutawa, A. B., Adamu, A., Zobir, S. A. M., Abdu, A., & Abdullah, S. N. A. (2022) · Horticultural Plant Journal · doi:10.1016/j.hpj.2022.02.004 · Cited by 88
Overview of vertebrate animal models of fungal infection
Hohl, T. M. (2014) · Journal of Immunological Methods · doi:10.1016/j.jim.2014.03.022 · Cited by 74
“The recent recognition that C. albicans can form structured biofilms within the murine vaginal mucosa will undoubtedly inform studies on the genetic requirements for biofilm formation and its role in pathogenesis on biotic surfaces versus abiotic medical devices (Harriott et al., 2010).”
BackgroundMcKloud, E., Delaney, C., Sherry, L., Kean, R., Williams, S., Metcalfe, R., Thomas, R., Rautemaa‐Richardson, R., Gerasimidis, K., Nile, C. J., et al. (2021) · mSystems · doi:10.1128/msystems.00622-21 · Cited by 79
“C. albicans has been shown to form bio fi lms on vaginal mucosa both ex vivo and in vivo by identi-fi cation of signi fi cant fungal load, bio fi lm architecture, and extracellular matrix using confocal and electron microscopy (12).”
MethodMusa, S. F., Yeat, T. S., Kamal, L. Z. M., Tabana, Y., Ahmed, M. A., Ouweini, A. E., Lim, V., Keong, L. C., & Sandai, D. A. (2017) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.8573 · Cited by 74
Boral, H., Metin, B., Döğen, A., Seyedmousavi, S., & İlkit, M. (2017) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2017.10.008 · Cited by 71
“, 2009), intestinal (Ganguly and Mitchell, 2011), and vaginal (Harriott et al., 2010) environments.”
BackgroundHow Biofilm Growth Affects Candida-Host Interactions
Eix, E. F., & Nett, J. E. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01437 · Cited by 72
Combination Therapy to Treat Fungal Biofilm-Based Infections
Tits, J., Cammue, B. P. A., & Thevissen, K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228873 · Cited by 71
“Increasing evidence points to the involvement of drug tolerant biofilms in mucosal fungal infections, such as vulvovaginal candidiasis [10,22,33,34].”
BackgroundA Review on Antifungal Efficiency of Plant Extracts Entrenched Polysaccharide-Based Nanohydrogels
Kaur, N., Bains, A., Kaushik, R., Dhull, S. B., Fogarasi, M., & Chawla, P. (2021) · Nutrients · doi:10.3390/nu13062055 · Cited by 81
Scarsini, M., Tomasinsig, L., Arzese, A., D’Este, F., Oro, D., & Skerlavaj, B. (2015) · Peptides · doi:10.1016/j.peptides.2015.07.023 · Cited by 70
Adhesion of bacteria to surfaces and biofilm formation on medical devices
Floyd, K. A., Eberly, A. R., & Hadjifrangiskou, M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-08-100382-4.00003-4 · Cited by 71
Identification of novel mechanisms involved in generating localized vulvodynia pain
Falsetta, M. L., Foster, D. C., Woeller, C. F., Pollock, S. J., Bonham, A. D., Haidaris, C. G., Stodgell, C. J., & Phipps, R. P. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.02.002 · Cited by 69
“Using an NFkB reporter, we show that activation is considerably more robust when fibroblasts are challenged with common vaginal pathogen C albicans, vs S cerevisiae, a Brewer’s yeast largely regarded as nonpathogenic.(25-28,78,79) In keeping with this observation, our previous work has shown that the response to diffe…”
BackgroundOrsi, C. F., Borghi, E., Colombari, B., Neglia, R. G., Quaglino, D., Ardizzoni, A., Morace, G., & Blasi, E. (2014) · Microbial Pathogenesis · doi:10.1016/j.micpath.2014.03.003 · Cited by 69
Host Contributions to Construction of Three Device-Associated Candida albicans Biofilms
Nett, J. E., Żarnowski, R., Cabezas‐Olcoz, J., Brooks, E. G., Bernhardt, J., Marchillo, K., Mosher, D. F., & Andes, D. R. (2015) · Infection and Immunity · doi:10.1128/iai.00931-15 · Cited by 68
Simitsopoulou, M., Pešková, P., Tasina, E., Katragkou, A., Kyrpitzi, D., Velegraki, A., Walsh, T. J., & Roilides, E. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02541-12 · Cited by 66
“In addition, oropharyngeal and vaginal in vivo models have demonstrated that mucosal Candida infections are due to the development of biofilms, a process controlled by morphogenetic and biofilm regulators (4, 5).”
BackgroundAction mechanisms of probiotics on Candida spp. and candidiasis prevention: an update
Ribeiro, F. D. C., Rossoni, R. D., de Barros, P. P., dos Santos, J. D., Fugisaki, L. R. D. O., Leão, M. V. P., & Junqueira, J. (2019) · Journal of Applied Microbiology · doi:10.1111/jam.14511 · Cited by 65
“Recent evidence indicates that the pathogenic potential of Candida also depends on its ability to produce biofilms on abiotic and living surfaces (Harriott et al. 2010; Ramage et al. 2012).”
BackgroundWang, X., You, J., King, J. B., Powell, D. R., & Cichewicz, R. H. (2012) · Journal of Natural Products · doi:10.1021/np2009994 · Cited by 66
Sardi, J. D. C. O., Silva, D. R., Aníbal, P. C., Baldin, J. J. C. M. D. C., Ramalho, S. R., Rosalen, P. L., Macedo, M. L. R., & Höfling, J. F. (2021) · Current Fungal Infection Reports · doi:10.1007/s12281-021-00415-9 · Cited by 62
Fungal Biofilms: In Vivo Models for Discovery of Anti-Biofilm Drugs
Nett, J. E., & Andes, D. R. (2015) · Microbiology Spectrum · doi:10.1128/microbiolspec.mb-0008-2014 · Cited by 68
“In addition to these animal models of device-associated infections, models of mucosal Candida biofilms will surely be helpful for the study of these common infections (25, 26).”
BackgroundExperimental Models of Vaginal Candidiasis and Their Relevance to Human Candidiasis
Cassone, A., & Sobel, J. D. (2016) · Infection and Immunity · doi:10.1128/iai.01544-15 · Cited by 63
“In both rodents, pseudoestrus induces stage-dependent, profound changes in the vaginal epithelium, with a keratinized surface to which fungal cells strongly adhere and upon which they multiply by hyphal growth and by eventually forming a biofilm (19, 24).”
BackgroundLaFleur, M. D., Lucumi, E., Napper, A. D., Diamond, S. L., & Lewis, K. (2011) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkq530 · Cited by 59
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
“The adherent community of Candida cells suggested the presence of a mucosal biofilm, as has been described for both oral and vaginal candidiasis (25, 60).”
BackgroundYou, J., Du, L., King, J. B., Hall, B. E., & Cichewicz, R. H. (2013) · ACS Chemical Biology · doi:10.1021/cb400009f · Cited by 60
Connolly, L. A., Riccombeni, A., Grózer, Z., Holland, L., Lynch, D. B., Andes, D. R., Gácser, A., & Butler, G. (2013) · Molecular Microbiology · doi:10.1111/mmi.12345 · Cited by 59
“Cells with an efg1 deletion form very loose biofilms on plastic consisting mostly of yeast cells (Ramage et al., 2002), and form defective biofilms on vaginal mucosa (Harriott et al., 2010).”
BackgroundTroskie, A. M., Rautenbach, M., Delattin, N., Vosloo, J. A., Dathe, M., Cammue, B. P. A., & Thevissen, K. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02381-14 · Cited by 57
The Clinical Importance of Fungal Biofilms
Ramage, G., & Williams, C. (2013) · Advances in applied microbiology · doi:10.1016/b978-0-12-407673-0.00002-3 · Cited by 58
Srikantha, T., Daniels, K. J., Pujol, C., Kim, E., & Soll, D. R. (2013) · Eukaryotic Cell · doi:10.1128/ec.00071-13 · Cited by 54
“been demonstrated by Noverr and coworkers (39).”
MethodGaining Insights from Candida Biofilm Heterogeneity: One Size Does Not Fit All
Kean, R., Delaney, C., Rajendran, R., Sherry, L., Metcalfe, R., Thomas, R., McLean, W., Williams, C., & Ramage, G. (2018) · Journal of Fungi · doi:10.3390/jof4010012 · Cited by 56
Comparative Analysis of the Capacity of the Candida Species To Elicit Vaginal Immunopathology
Willems, H. M. E., Lowes, D. J., Barker, K. S., Palmer, G. E., & Peters, B. M. (2018) · Infection and Immunity · doi:10.1128/iai.00527-18 · Cited by 56
Identification of the cell targets important for propolis-induced cell death in Candida albicans
de Castro, P. A., Bom, V. L. P., Brown, N. A., Almeida, R. S., Ramalho, L. N. Z., Savoldi, M., Goldman, M. H. S., Berretta, A. A., & Goldman, G. H. (2013) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2013.07.001 · Cited by 55
Role ofCandida albicanssecreted aspartyl protease Sap9 in interkingdom biofilm formation
Dutton, L. C., Jenkinson, H. F., Lamont, R. J., & Nobbs, A. H. (2016) · Pathogens and Disease · doi:10.1093/femspd/ftw005 · Cited by 54
“Candida albicans biofilm formation on a range of surfaces in vitro and in vivo (Paulitsch et al. 2009; Busscher et al. 2010; Harriott et al. 2010) occurs in several phases, beginning with the deposition of yeast-form cells onto a substratum and subsequent formation of hyphae (Nobile et al. 2012).”
BackgroundThe SPS amino acid sensor mediates nutrient acquisition and immune evasion inCandida albicans
Miramón, P., & Lorenz, M. C. (2016) · Cellular Microbiology · doi:10.1111/cmi.12600 · Cited by 56
Tulasidas, S., Rao, P., Bhat, S., & Manipura, R. (2018) · Infection and Drug Resistance · doi:10.2147/idr.s179462 · Cited by 51
Araújo, M. G. D. F., Pacífico, M., Vilegas, W., dos Santos, L. C., Icely, P. A., Miró, M. S., Scarpa, M. V., Bauab, T. M., & Sotomayor, C. E. (2013) · Medical Mycology · doi:10.3109/13693786.2013.795294 · Cited by 49
The Host’s Reply to Candida Biofilm
Nett, J. E. (2016) · Pathogens · doi:10.3390/pathogens5010033 · Cited by 46
“Recent investigations have identified mucosal biofilm formation in a murine model of vaginal candidiasis [14,39,40].”
BackgroundEllah, N. H. A., Abdel-Aleem, J. A., Abdo, M. N., Abou‐Ghadir, O. F., Zahran, K. M., & Hetta, . F. (2019) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2019.118472 · Cited by 47
Our current clinical understanding of Candida biofilms: where are we two decades on?
Ramage, G., Borghi, E., Rodrigues, C. F., Kean, R., Williams, C., & Lopez-Ribot, J. L. (2023) · Apmis · doi:10.1111/apm.13310 · Cited by 47
“However, there is unequivocal evidence that C. albicans biofilm formation on vaginal mucosa in a murine model of VVC, which has been visualized using scanning electron and confocal microscopy (63).”
Bonifácio, B. V., Vila, T. V. M., Masiero, I. F., da Silva, P. B., da Silva, I. C., Lopes, É. D. O., Ramos, M. A. D. S., de Souza, L. P., Vilegas, W., Pavan, F. R., et al. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02642 · Cited by 48
Iseppi, R., Tardugno, R., Brighenti, V., Benvenuti, S., Sabia, C., Pellati, F., & Messi, P. (2020) · Antibiotics · doi:10.3390/antibiotics9090592 · Cited by 46
Sudjana, A. N., Carson, C. F., Carson, K. C., Riley, T. V., & Hammer, K. A. (2012) · Medical Mycology · doi:10.3109/13693786.2012.683540 · Cited by 43
The Vaginal Microbiota, Bacterial Biofilms and Polymeric Drug-Releasing Vaginal Rings
Carson, L., Merkatz, R. B., Martinelli, E., Boyd, P., Variano, B., Sallent, T., & Malcolm, K. R. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13050751 · Cited by 41
“to form biofilms that attach irreversibly to both biotic and abiotic surfaces; this trait is highly dependent on yeast to hyphal morphogenesis [73,75].”
Background
Metadata
- Authors
- Harriott, M. M., Lilly, E. A., Rodriguez, T. E., Fidel, P. L., & Noverr, M. C.
- Affiliations
- Wayne State University (US)
- Louisiana State University Health Sciences Center New Orleans (US)
- Venue
- Microbiology
- Publisher
- Microbiology Society
- Published
- 2010-12-01
- Volume
- 156
- Issue
- 12
- Pages
- 3635-3644
- ISSN
- 1350-0872 (ISSN-L)
- 1465-2080
- PMC
- PMC3068702
- OpenAlex
- W2063801124
- Cited by
- 301
- References
- 35
- Citations by year
- 2026: 10 · 2025: 14 · 2024: 13 · 2023: 20 · 2022: 19 · 2021: 26 · 2020: 27 · 2019: 24 · 2018: 16 · 2017: 25 · 2016: 21 · 2015: 26 · 2014: 25 · 2013: 16 · 2012: 9
- FWCI
- 7.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Microbiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Louisiana Board of Regents
- Carnegie Mellon University
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (R01 AI72406-01, R01AI072406, R01AI32556, R01AI032556)
- 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, biofilm formation, vaginal mucosa, vaginal candidiasis, vaginal epithelium, extracellular matrix, BCR1, EFG1, morphogenesis, fungal virulence
- MeSH terms
- Animals, Candida albicans, Candidiasis, Female, Humans, Mice, Inbred C57BL, Mucous Membrane, Vagina, Biofilms, Dioxygenases, Mice
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
