- Research article
- Open Access
Cigarette smoke condensate increases C. albicans adhesion, growth, biofilm formation, and EAP1, HWP1 and SAP2 gene expression
© Semlali et al.; licensee BioMed Central Ltd. 2014
- Received: 3 December 2013
- Accepted: 7 March 2014
- Published: 12 March 2014
Smokers are more prone to oral infections than are non-smokers. Cigarette smoke reaches the host cells but also microorganisms present in the oral cavity. The contact between cigarette smoke and oral bacteria promotes such oral diseases as periodontitis. Cigarette smoke can also modulate C. albicans activities that promote oral candidiasis. The goal of this study was to investigate the effect of cigarette smoke condensate on C. albicans adhesion, growth, and biofilm formation as well as the activation of EAP1, HWP1 and secreted aspartic protease 2.
Cigarette smoke condensate (CSC) increased C. albicans adhesion and growth, as well as biofilm formation. These features may be supported by the activation of certain important genes. Using quantitative RT-PCR, we demonstrated that CSC-exposed C. albicans expressed high levels of EAP1, HWP1 and SAP2 mRNA and that this gene expression increased with increasing concentrations of CSC.
CSC induction of C. albicans adhesion, growth, and biofilm formation may explain the increased persistence of this pathogen in smokers. These findings may also be relevant to other biofilm-induced oral diseases.
One of the most commonly encountered opportunistic microorganisms in humans is Candida albicans, a ubiquitous fungus that is a part of the normal microbial flora found on mucosal surfaces such as those of the oral cavity, gastrointestinal tract, and vagina in human beings and domestic animals . This yeast is the most common cause of mucosal and invasive fungal infections observed in humans . Host protection against C. albicans infection is complex and includes different subsets of the immune defense system [3–5].
During the development of oropharyngeal candidiasis (OPC), Candida adheres to and invades the tissue. The adhesion of this yeast to host tissue is the initial phase of a potential infection that enables microorganisms to survive inside the host and eventually colonize host tissues during the onset of candidiasis [6, 7]. Following this irreversible attachment, fungal cells proliferate and optimally interact to ensure their sustainability in the imposed environment. After the proliferative phase comes the production and deposition of a thick extracellular matrix (mature biofilm) that procures chemical as well as physical protection for cells [8, 9].
C. albicans adhesion and growth leading to biofilm formation are mediated by various genes such as HWP1 and EAP1 that encode well-characterized class of cell wall proteins that house a glycosylphosphatidylinositol (GPI) anchorage motif in their C–terminal domains and a signal peptide at their N-termini. These C- and N-terminal domains mediate the adherence of C. albicans to various surfaces . HWP1, a hyphal-specific adhesion gene encodes the hyphal cell wall protein, and both are essential for biofilm formation . The involvement of HWP1 in C. albicans adhesion can be supported by the EAP1 gene which encodes a glucan-cross-linked cell wall protein (adhesin Eap1p) and mediates the adhesion of C. albicans to different surfaces, including epithelial cells and polystyrene . Similar to other genes, HWP1 and EAP1 are downstream effectors of EFG1, a transcription regulator . The efg1 mutant strain has been shown to exhibit defects in growth, biofilm formation, and virulence .
C. albicans virulence is also mediated by proteolytic enzymes such as secreted aspartyl proteinases (Saps) [16, 17]. The contribution of Saps to mucosal and systemic infections and their involvement in adherence, tissue damage, and evasion of host immune responses has been reported, showing the implication of the Sap2 gene in C. albicans growth in protein-containing media . SAP1 and SAP3 are expressed during phenotypic switching [19, 20], while SAP4, SAP5 and SAP6 are expressed upon hyphal formation . SAP9 and SAP10 are involved in the mechanism of adhesion to host cells . This proteolytic enzyme family is therefore involved in C. albicans virulence.
C. albicans infection can be promoted by several factors. Candidiasis has been associated with long-term antibiotics intake, AIDS, leukemia, malignancy, radiation therapy for head and neck cancer, or other risk factors that interfere with immunocompetence [22–24].
Environmental factors such as smoking may also promote Candida infections [25, 26]. Tobacco smoke exposure has been shown to promote microbial biofilm formation . Specifically, it has been shown that cigarette smoke interferes with S mutans and C. albicans adhesion, resulting in biofilm formation on dental restoration materials , which suggests that cigarette smokers are more susceptible to life-threatening oral infections including candidiasis. The aim of this study was to investigate the effect of cigarette smoke condensate on C. albicans adhesion, growth, and biofilm formation, and on the activation of several genes involved in the virulence of this yeast.
Cigarette smoke condensate promoted C albicansadhesion and growth
Cigarette smoke condensate promoted C albicansbiofilm formation
Cigarette smoke condensate modulated HWP1, EAP1, and SAP2expression
Smoking is known to induce a variety of changes in the oral cavity. Cigarette smoke affects both saliva  and oral microorganisms, including C. albicans, a leading cause of oral candidiasis . However, the specific effect of cigarette smoke on C. albicans remains to be elucidated. The first question we addressed in this study was: What is the effect of cigarette smoke on C. albicans adhesion? We demonstrated that CSC promoted C. albicans adhesion, which is in agreement with previously reported studies showing a high rate of oral candida carriage in tobacco smokers compared to non-smokers [30, 31]. Furthermore, bacteria exposed to CSC were shown to adhere more to epithelial cells compared to non-exposed specimens , which supports our data with C. albicans. Increased adhesion of C. albicans in the presence of CSC may occur due to changes in the interaction of C. albicans with its environment through the expression of high levels of adhesins, as previously suggested . Furthermore, it is important to realize that cigarette smoke comprises a high number of individual compounds , including acetaldehyde, benzene, 1,3-butadiene, and isoprene with an elevated mutagenic potential . Thus, it is possible that these compounds may have exerted specific effect on C. albicans adhesion, growth and probably biofilm formation. The effect of cigarette smoke promoting cell adhesion was previously reported by Baboni et al., (2009) showing linear dose response adhesion . The mechanism involved in such effect could involve kinase pathways. These pathways can be promoted by CSC compounds at certain concentration, but inhibited when these compounds are high explaining the decrease of C. albicans adhesion/biofilm formation at 40% and 50% of CSC. Further research is mandatory to shed light on the mechanisms leading to the up-regulation of C. albicans adhesion when exposed to cigarette smoke.
C. albicans adhesion is one of the key events leading to candidiasis [36, 37]. This adhesion is usually followed by overgrowth and invasion . Consequently, in promoting C. albicans adhesion, CSC may lead to an over-growth of this yeast. Our study confirms this hypothesis showing a growth increase of C. albicans in the presence of CSC. This concurs with previously published reports showing that smoking can be an important predisposing factor for oral candidiasis , which may be enhanced by cigarette smoke through an increased secretion of histolytic enzymes by C. albicans, thus contributing to its virulence . However, the exact pathogenic influence of smoking has yet to be investigated.
C. albicans adhesion and growth are particularly necessary for biofilm formation [39, 40]. Because CSC significantly increased C. albicans adhesion and growth in the present study, it is suggested that CSC may also promote C. albicans biofilm formation. Using appropriate conditions to form biofilms, our findings indicate that CSC was indeed capable of promoting biofilm formation. Of interest is that a significant increase of biofilm formation was obtained at both tested concentrations, and that this phenomenon was dependent on CSC concentration. These useful data are comparable to those of other studies showing increased microbial biofilm formation with cigarette smoke [41–43]. By showing the significant stimulatory effect on increasing C. albicans biofilm formation, cigarette smoke can thus be labeled as an infection-promoting agent.
Promoting C. albicans adhesion, growth, and biofilm formation may operate through the modulated expression of certain C. albicans genes [44, 45], as supported by our study demonstrating that CSC led to a high expression of the EAP1 gene. As a member of the GPI-CWP family in C. albicans, Eap1p was originally identified because of its ability to mediate adhesion to polystyrene when the EAP1 gene was expressed in a flocculin-deficient Saccharomyces cerevisiae strain. EAP1 expression in a C. albicans efg1/efg1 mutant was able to restore C. albicans adhesion to epithelial cells . Deleting EAP1 in C. albicans was shown to reduce cell adhesion to polystyrene and to epithelial cells in a gene dosage-dependent manner [12, 46]. Indeed, this suggests that exposure to CSC increases EAP1 expression, which may in turn contribute to increasing C. albicans adhesion, and ultimately, biofilm formation and pathogenesis.
We also demonstrated that CSC increased HWP1 mRNA expression. HWP1 is a downstream component of the cAMP-dependent PKA pathway and is positively regulated by EFG1. The transcript level of HWP1 increased with increasing CSC stimulation, which suggests that CSC did affect cAMP–EFG1 pathway activity, resulting in an increase of C. albicans adhesion and growth with biofilm formation. Further investigations are therefore warranted to gain greater insight into the interaction between cigarette smoke and C. albicans leading to infection.
Candida pathogenesis is associated with the production and secretion of histolytic enzymes . Secreted aspartyl proteases (Saps) and phospholipases were specifically reported as being directly related to C. albicans virulence . During infection, Saps are incriminated degrading host proteins involved in tissue barriers and immune defense [18, 50, 51]. Here, we report that CSC upregulated Sap2 mRNA expression. It is known that Sap gene upregulation contributes to increasing C. albicans transition, and later, its pathogenicity through an augmented secretion of proteinases . Our study thus establishes, for the first time, a clear link between cigarette smoke and C. albicans pathogenesis through the behavior of key genes such as EAP1, HWP1 and Sap2. These genes are known to be involved in controlling Candida adhesion, growth, and biofilm formation ; however, the precise interactions between these different genes and cigarette smoke during C. albicans pathogenesis have not yet been fully investigated. Data suggest that gene activation can be involved in C. albicans adhesion, growth and biofilm formation promoted by CSC. This may involve kinase pathways contributing to C. albicans adaptation to the CSC environment as previously suggested .
This study demonstrated that CSC upregulates C. albicans adhesion and growth that promote biofilm formation. Of interest is that these effects were supported by the modulation of C. albicans genes EAP1, HWP1, and Sap2. Overall results therefore suggest a possible link between cigarette smoke, C. albicans activation, and oral candidiasis.
Preparation of cigarette smoke condensate
C. albicans SC5314 was cultured for 24 h on Sabouraud dextrose agar plates (Becton Dickinson, Oakville, ON, Canada) at 30°C. For the C. albicans suspensions, one colony was used to inoculate 10 ml of Sabouraud liquid medium supplemented with 0.1% glucose, pH 5.6. The cultures were then grown to the stationary phase in a shaking water bath for 18 h at 30°C, after which time the yeast cells were collected, washed with phosphate-buffered saline (PBS), counted by means of a haemocytometer, and adjusted to 106/ml prior to use.
Effect of CSC on C albicans adhesion
A glass slide (0.5 cm in diameter) was placed into each well of a 12-well plate then covered with 1 ml of sterile artificial saliva solution at room temperature for 30 min under agitation to ensure that the slides were covered by liquid at all times. Before use, the artificial saliva (2.5 g of NaCl, 332.97 mg of CaCl2, 250 mg of MgCl2.6H2O, 189.48 mg of KCl, 3 g of anhydrous potassium acetate (C2H3O2K), 772.00 mg of K3PO4.3 H2O, and 0.1 ml of H3PO4 (85 wt. % in H2O, Sigma Aldrich)) was supplemented with 140 mg of Type II mucin in 1000 ml of the prepared saliva solution, pH 7. Following the saliva coating, the glass slides were gently rinsed with sterile saline, transferred to new wells of sterile 12-well plates, and subsequently dried for 3 h under a sterile culture hood. Each saliva-coated glass slide was then covered with 104 C. albicans cells in 50 μl of Sabouraud medium supplemented or not with CSC at various concentrations (10, 20, 30, 40 or 50%) and incubated for 60 nm at 30°C under stable conditions to prevent the medium from leaking from the slide onto the plastic. Following this incubation period, 1 ml of Sabouraud with or without CSC was added to each well and the cultures were further incubated for 1, 3, or 6 h. At the end of each incubation period, each slide was removed from its well and placed into new wells of a 12-well plate, subsequently washed twice with warm PBS, and subjected to crystal violet staining. One milliliter of 1% w/v crystal violet solution in demineralized water was added, and the slides were further incubated at room temperature for 30 min. After incubation, the non-bound dye was removed from the wells by thorough washing with demineralized water, followed by drying at 37°C. Bound crystal violet was dissolved by adding 1 ml of absolute ethanol and incubating on a rocking platform for 15 min at room temperature. The absorbance levels of the dissolved dye were measured at a wavelength of 590 nm by means of an optical density reader (X-Mark Microplate Spectrophotometer, Bio-Rad Laboratories, Mississauga, ON, Canada).
Effect of CSC on C albicans growth
The yeast was seeded into separate tubes (105 C. albicans per tube) in 4 ml of Sabouraud culture medium supplemented or not with CSC at 10, 20, 30, 40, or 50%. The cultures were maintained at 30°C for 24 h, after which time C. albicans growth was evaluated by means of the (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide) (MTT) assay (Sigma-Aldrich, St. Louis, MO) which measures viable cells as a function of mitochondrial activity. Briefly, an MTT stock solution (5 mg/ml) was prepared in PBS and added to each culture at a final concentration of 10% (v/v). The C. albicans cultures were then incubated with the MTT solution at 30°C for 4 h, after which time the plate was centrifuged for 10 min at 1200 rpm and the supernatant was removed. The remaining pellet in each condition was then washed with warm PBS, and 2 ml of 0.04 N HCl in isopropanol were added to each pellet, with a further incubation for 15 min. Absorbance (optical density, OD) was subsequently measured at 550 nm by means of an xMark microplate spectrophotometer (Bio-Rad, Mississauga, ON, Canada).
Effect of CSC on C albicansbiofilm formation
C. albicans biofilms were obtained by culturing the yeast on a porous collagen scaffold which facilitated C. albicans penetration through the pores and its adhesion to the scaffold through collagen affinity. This also promoted biofilm formation and handling with no cell loss, thus contributing to the maintenance of the biofilm structure. For this purpose, 5 mm × 5 mm samples of porous scaffold (Collatape, Zimmer Dental Inc., Carlsbad, CA, USA) were placed in a 24-well plate, rinsed twice with culture medium, seeded with C. albicans (106 cells), and finally incubated for 30 min at 30°C without shaking to allow for adherence. Fresh Sabouraud medium was added to each well in the presence or absence of various concentrations of CSC (10, 30, or 50%). The C. albicans-seeded scaffolds were then incubated for 2 or 3 days at 30°C. Following each culture period, C. albicans growth and biofilm formation was assessed by scanning electron microscopy and the crystal violet assay.
Scanning electron microscopy (SEM) analysis
C. albicans-rich scaffolds (biofilms) were fixed in ethylene glycol for 60 min followed by a rinse with sterile PBS. Dehydration was performed in a series of 5-min treatments with ethanol solutions of increasing concentration (50, 70, 90, and twice at 100%). The dehydrated biofilms were kept overnight in a vacuum oven at 25°C, after which time they were sputter-coated with gold, examined, and imaged under a JEOL 6360 LV SEM (Soquelec, Montréal, QC, Canada) operating at a 30 kV accelerating voltage.
Biofilm staining by crystal violet
Following incubation for 24 h at 30°C, biofilms were stained with 1% crystal violet (100 μl) for 15 min. They were then washed three times with PBS to remove unbound crystal violet dye and were dried overnight at room temperature. The biofilms were then covered with 1 ml of absolute ethanol and were incubated on a rocking platform for 20 min at room temperature to release the stain from the biofilms. Absorbance was recorded at 590 nm. Each biofilm assay was run in triplicate and the means ± standard deviations of four separate experiments were calculated and plotted.
Effect of CSC on C albicansgene activation/repression
C. albicans (105 cells) was cultured in the presence or absence of CSC at various concentrations (30 and 50%) at 30°C for 24 h under agitation. At the end of this incubation period, the cultures were centrifuged 10 min at 13,000 rpm, the supernatants were discarded, and each pellet was suspended in 0.6 ml of lysis buffer (1 M glycerol, 0.1 M EDTA). Glass beads (0.425-0.6 mm in diameter; 0.2 ml) were then added to each suspended pellet prior to sonication (4 × 1 min, followed by 2 min of incubation in ice) by means of a MiniBead-beater (Biospec Products, Bartlesville, OK, USA). Following cell lysis, the total RNA was extracted from each sample by means of the Illustra RNAspin Mini kit (GE Health Care UK Limited, Buckingham, UK). The concentration, purity, and quality of the extracted RNA were determined using the Experion system and the RNA StdSens analysis kit according to instructions provided by the manufacturer (Bio-Rad, Hercules, CA, USA). Appropriate RNAs were used to perform quantitative RT-PCR.
Quantitative real-time RT-PCR
Primer sequences used for the qRT-PCR
Primer sequence 5′ to 3′
Amp size (bp)
Each experiment was performed at least four times, with experimental values expressed as means ± SD. The statistical significance of the differences between the control (absence of CSC) and test (presence of CSC) values was determined by means of a one-way ANOVA. Posteriori comparisons were performed using Tukey’s method. Normality and variance assumptions were verified using the Shapiro-Wilk test and the Brown and Forsythe test, respectively. All of the assumptions were fulfilled. P values were declared significant at ≤ 0.05. The data were analyzed using the SAS version 8.2 statistical package (SAS Institute Inc., Cary, NC, USA).
This research was supported by NSERC discovery grant number-155234-07, as well as a grant from the Fonds Émile-Beaulieu (Laval University). The authors also thank Ms. Claire Kingston (Traduction CFK) for proofreading and editing this manuscript.
- Richardson M, Lass-Florl C: Changing epidemiology of systemic fungal infections. Clin Microbiol Infect. 2008, 14: 5-24.View ArticlePubMedGoogle Scholar
- Morschhauser J: Regulation of multidrug resistance in pathogenic fungi. Fungal Genet Biol. 2010, 47: 94-106. 10.1016/j.fgb.2009.08.002.View ArticlePubMedGoogle Scholar
- Rouabhia M, Ross G, Page N, Chakir J: Interleukin-18 and gamma interferon production by oral epithelial cells in response to exposure to Candida albicans or lipopolysaccharide stimulation. Infect Immun. 2002, 70: 7073-7080. 10.1128/IAI.70.12.7073-7080.2002.PubMed CentralView ArticlePubMedGoogle Scholar
- Rouabhia M, Schaller M, Corbucci C, Vecchiarelli A, Prill SK, Giasson L, Ernst JF: Virulence of the fungal pathogen Candida albicans requires the five isoforms of protein mannosyltransferases. Infect Immun. 2005, 73: 4571-4580. 10.1128/IAI.73.8.4571-4580.2005.PubMed CentralView ArticlePubMedGoogle Scholar
- Saunus JM, Kazoullis A, Farah CS: Cellular and molecular mechanisms of resistance to oral Candida albicans infections. Front Biosci. 2008, 13: 5345-5358.View ArticlePubMedGoogle Scholar
- Park H, Liu Y, Solis N: Transcriptional responses of Candida albicans to epithelial and endothelial cells. Eukaryot Cell. 2009, 8: 1498-1510. 10.1128/EC.00165-09.PubMed CentralView ArticlePubMedGoogle Scholar
- Zakikhany K, Naglik JR, Schmidt-Westhausen A, Holland G, Schaller M, Hube B: In vivo transcript profiling of Candida albicans identifies a gene essential for inter-epithelial dissemination. Cell Microbiol. 2007, 9: 2938-2954. 10.1111/j.1462-5822.2007.01009.x.View ArticlePubMedGoogle Scholar
- Costerton JWS, Stewart PS, Greenberg EP: Bacterial biofilms: a common cause of persistent infections. Science. 1999, 284: 1318-1322. 10.1126/science.284.5418.1318.View ArticlePubMedGoogle Scholar
- Grant SS, Hung DT: Persistent bacterial infections, antibiotic tolerance, and the oxidative stress response. Virulence. 2013, 4: 273-283. 10.4161/viru.23987.PubMed CentralView ArticlePubMedGoogle Scholar
- Sundstrom P: Adhesion in Candida spp. Cell Microbiol. 2002, 4: 461-469. 10.1046/j.1462-5822.2002.00206.x.View ArticlePubMedGoogle Scholar
- Nobile CJ, Nett JE, Andes DR, Mitchell AP: Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot Cell. 2006, 5: 1604-1610. 10.1128/EC.00194-06.PubMed CentralView ArticlePubMedGoogle Scholar
- Li F, Palecek SP: EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryot Cell. 2003, 2: 1266-1273. 10.1128/EC.2.6.1266-1273.2003.PubMed CentralView ArticlePubMedGoogle Scholar
- Sohn K, Urban C, Brunner H, Rupp S: EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol Microbiol. 2003, 47: 89-102.View ArticlePubMedGoogle Scholar
- Stoldt VR, Sonneborn A, Leuker CE, Ernst JF: Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J. 1997, 16: 1982-1991. 10.1093/emboj/16.8.1982.PubMed CentralView ArticlePubMedGoogle Scholar
- Lo HJ, Köhler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, Fink GR: Nonfilamentous C albicans mutants are avirulent. Cell. 1997, 90: 939-949. 10.1016/S0092-8674(00)80358-X.View ArticlePubMedGoogle Scholar
- Schaller M, Borelli C, Korting HC, Hube B: Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses. 2005, 48: 365-377. 10.1111/j.1439-0507.2005.01165.x.View ArticlePubMedGoogle Scholar
- Décanis N, Tazi N, Correia A, Vilanova M, Rouabhia M: Farnesol, a fungal quorum-sensing molecule triggers Candida albicans morphological changes by downregulating the expression of different secreted aspartyl proteinase genes. Open Microbiol J. 2011, 5: 119-126. 10.2174/1874285801105010119.PubMed CentralView ArticlePubMedGoogle Scholar
- Naglik JR, Challacombe SJ, Hube B: Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev. 2003, 67: 400-428. 10.1128/MMBR.67.3.400-428.2003.PubMed CentralView ArticlePubMedGoogle Scholar
- Hube B, Naglik J: Candida albicans proteinases: resolving the mystery of a gene family. Microbiology. 2001, 147: 1997-2005.View ArticlePubMedGoogle Scholar
- White TC, Agabian N: Candida albicans secreted aspartyl proteinases: isoenzyme pattern is determined by cell type, and levels are determined by environmental factors. J Bacteriol. 1995, 177: 5215-5221.PubMed CentralPubMedGoogle Scholar
- Albrecht A, Felk A, Pichova I, Naglik JR, Schaller M, de Groot P, Maccallum D, Odds FC, Schäfer W, Klis F, Monod M, Hube B: Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J Biol Chem. 2006, 281: 688-694. 10.1074/jbc.M509297200.View ArticlePubMedGoogle Scholar
- Nave R, Mueller H: From inhaler to lung: clinical implications of the formulations of ciclesonide and other inhaled corticosteroids. Int J Gen Med. 2013, 6: 99-107.PubMed CentralPubMedGoogle Scholar
- Pinel B, Cassou-Mounat T, Bensadoun RJ: Oropharyngeal candidiasis and radiotherapy. Cancer Radiother. 2012, 3: 222-229.View ArticleGoogle Scholar
- Fidel PL: Candida-host interactions in HIV disease: implications for oropharyngeal candidiasis. Adv Dent Res. 2011, 1: 45-49.View ArticleGoogle Scholar
- Baboni FB, Barp D, Izidoro AC, Samaranayake LP, Rosa EA: Enhancement of Candida albicans virulence after exposition to cigarette mainstream smoke. Mycopathologia. 2009, 168 (5): 227-235. 10.1007/s11046-009-9217-5.View ArticlePubMedGoogle Scholar
- Soysa NS, Ellepola AN: The impact of cigarette/tobacco smoking on oral candidosis: an overview. Oral Dis. 2005, 5: 268-273.View ArticleGoogle Scholar
- Goldstein-Daruech N, Cope EK, Zhao KQ, Vukovic K, Kofonow JM, Doghramji L, González B, Chiu AG, Kennedy DW, Palmer JN, Leid JG, Kreindler JL, Cohen NL: Tobacco smoke mediated induction of sinonasal microbial biofilms. PLoS One. 2011, 6: e15700-10.1371/journal.pone.0015700.PubMed CentralView ArticlePubMedGoogle Scholar
- Baboni FB, Guariza Filho O, Moreno AN, Rosa EA: Influence of cigarette smoke condensate on cariogenic and candidal biofilm formation on orthodontic materials. Am J Orthod Dentofacial Orthop. 2010, 4: 427-434.View ArticleGoogle Scholar
- Weiner D, Khankin EV, Levy Y, Aizenbud D, Reznick AZ: Effects of cigarette smoke on salivary protein tyrosine nitration. Eur J Med Res. 2010, 2: 211-216.Google Scholar
- Abu-Elteen KH, Abu-Alteen RM: The prevalence of Candida albicans populations in the mouths of complete denture wearers. New Microbiol. 1998, 21 (1): 41-48.PubMedGoogle Scholar
- Willis AM, Coulter WA, Fulton CR, Hayes JR, Bell PM, Lamey PJ: Oral candidal carriage and infection in insulin-treated diabetic patients. Diabet Med. 1999, 16 (8): 675-679. 10.1046/j.1464-5491.1999.00134.x.View ArticlePubMedGoogle Scholar
- Teughels W, Van Eldere J, van Steenberghe D, Cassiman JJ, Fives-Taylor P, Quirynen M: Influence of nicotine and cotinine on epithelial colonization by periodontopathogens. J Periodontol. 2005, 8: 1315-1322.View ArticleGoogle Scholar
- Feldman C, Anderson R: Cigarette smoking and mechanisms of susceptibility to infections of the respiratory tract and other organ systems. J Infect. 2013, 3: 169-184.View ArticleGoogle Scholar
- Gaworski CL, Dozier MM, Eldridge SR, Morrissey R, Rajendran N, Gerhart JM: Cigarette smoke vapor-phase effects on the rat upper respiratory tract. Inhalation Toxicol. 1998, 10: 857-873. 10.1080/089583798197420.View ArticleGoogle Scholar
- Adam T, Mitschke S, Streibel T, Baker RR, Zimmermann R: Quantitative puff-by-puff-resolved characterization of selected toxic compounds in cigarette mainstream smoke. Chem Res Toxicol. 2006, 19: 511-520. 10.1021/tx050220w.View ArticlePubMedGoogle Scholar
- Akerey B, Le-Lay C, Fliss I, Subirade M, Rouabhia M: In vitro efficacy of nisin Z against Candida albicans adhesion and transition following contact with normal human gingival cells. J Appl Microbiol. 2009, 107: 1298-1307. 10.1111/j.1365-2672.2009.04312.x.View ArticlePubMedGoogle Scholar
- Kempf M, Cottin J, Licznar P, Lefrançois C, Robert R, Apaire-Marchais V: Disruption of the GPI protein-encoding gene IFF4 of Candida albicans results in decreased adherence and virulence. Mycopathologia. 2009, 168: 73-77. 10.1007/s11046-009-9201-0.View ArticlePubMedGoogle Scholar
- Finkel JS, Xu W, Huang D, Hill EM, Desai JV, Woolford CA, Nett JE, Taff H, Norice CT, Andes DR, Lanni F, Mitchell AP: Portrait of Candida albicans adherence regulators. PLoS Pathog. 2012, 2: e1002525-View ArticleGoogle Scholar
- Inglis DO, Skrzypek MS, Arnaud MB, Binkley J, Shah P, Wymore F, Sherlock G: Improved gene ontology annotation for biofilm formation, filamentous growth, and phenotypic switching in Candida albicans. Eukaryot Cell. 2013, 12 (1): 101-108. 10.1128/EC.00238-12.PubMed CentralView ArticlePubMedGoogle Scholar
- Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J: Adherence and biofilm formation of non-Candida albicans Candida species. Trends Microbiol. 2011, 19 (5): 241-247. 10.1016/j.tim.2011.02.003.View ArticlePubMedGoogle Scholar
- Kulkarni R, Antala S, Wang A, Amaral FE, Rampersaud R, Larussa SJ, Planet PJ, Ratner AJ: Cigarette smoke increases staphylococcus aureus biofilm formation via oxidative stress. Infect Immun. 2012, 80 (11): 3804-3811. 10.1128/IAI.00689-12.PubMed CentralView ArticlePubMedGoogle Scholar
- Mutepe ND, Cockeran R, Steel HC, Theron AJ, Mitchell TJ, Feldman C, Anderson R: Effects of cigarette smoke condensate on pneumococcal biofilm formation and pneumolysin. Eur Respir J. 2013, 41 (2): 392-395. 10.1183/09031936.00213211.View ArticlePubMedGoogle Scholar
- Bagaitkar J, Daep CA, Patel CK, Renaud DE, Demuth DR, Scott DA: Tobacco smoke augments porphyromonas gingivalis-streptococcus gordonii biofilm formation. PLoS One. 2011, 6 (11): e27386-10.1371/journal.pone.0027386.PubMed CentralView ArticlePubMedGoogle Scholar
- Gutiérrez-Escribano P, Zeidler U, Suárez MB, Bachellier-Bassi S, Clemente-Blanco A, Bonhomme J, de Aldana CR V, d’Enfert C, Correa-Bordes J: The NDR/LATS kinase Cbk1 controls the activity of the transcriptional regulator Bcr1 duringbiofilm formation in Candida albicans. PLoS Pathog. 2012, 8 (5): e1002683-10.1371/journal.ppat.1002683.PubMed CentralView ArticlePubMedGoogle Scholar
- Rouabhia M, Semlali A, Chandra J, Mukherjee P, Chmielewski W, Ghannoum MA: Disruption of the ECM33 gene in Candida albicans prevents biofilm formation, engineered human oral mucosa tissue damage and gingival cell necrosis/apoptosis. Mediators Inflamm. 2012, 2012: 398207-PubMed CentralView ArticlePubMedGoogle Scholar
- Li F, Svarovsky MJ, Karlsson AJ, Wagner JP, Marchillo K, Oshel P, Andes D, Palecek SP: Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot Cell. 2007, 6: 931-939. 10.1128/EC.00049-07.PubMed CentralView ArticlePubMedGoogle Scholar
- Sharkey LL, McNemar MD, Saporito-Irwin SM, Sypherd PS, Fonzi WA: HWP1 functions in the morphological development of Candida albicans downstream of EFG1, TUP1, and RBF1. J Bacteriol. 1999, 181: 5273-5279.PubMed CentralPubMedGoogle Scholar
- Dostál J, Hamal P, Pavlícková L, Soucek M, Ruml T, Pichová I, Hrusková-Heidingsfeldová O: Simple method for screening Candida species isolates for the presence of secreted proteinases: a tool for the prediction of successful inhibitory treatment. J Clin Microbiol. 2003, 41 (2): 712-716. 10.1128/JCM.41.2.712-716.2003.PubMed CentralView ArticlePubMedGoogle Scholar
- Kantarcioglu AS, Yücel A: Phospholipase and protease activities in clinical Candida isolates with reference to the sources of strains. Mycoses. 2002, 45 (5–6): 160-165.View ArticlePubMedGoogle Scholar
- Kaminishi H, Miyaguchi H, Tamaki T, Suenaga N, Hisamatsu M, Mihashi I, Matsumoto H, Maeda H, Hagihara Y: Degradation of humoral host defense by Candida albicans proteinase. Infect Immun. 1995, 63: 984-988.PubMed CentralPubMedGoogle Scholar
- Rouabhia M, Semlali A, Audoy J, Chmielewski W: Antagonistic effect of Candida albicans and IFNγ on E-cadherin expression and production by human primary gingival epithelial cells. Cell Immunol. 2012, 280 (1): 61-67. 10.1016/j.cellimm.2012.11.008.View ArticlePubMedGoogle Scholar
- Naglik J, Albrecht A, Bader O, Hube B: Candida albicans proteinases and host/pathogen interactions. Cell Microbiol. 2004, 6 (10): 915-926. 10.1111/j.1462-5822.2004.00439.x.View ArticlePubMedGoogle Scholar
- Samaranayake YH, Cheung BP, Yau JY, Yeung SK, Samaranayake LP: Human serum promotes Candida albicans biofilm growth and virulence gene expression on silicone biomaterial. PLoS One. 2013, 8 (5): e62902-10.1371/journal.pone.0062902.PubMed CentralView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.