Characterization of a novel antibiofilm effect of nitric oxide-releasing aspirin (NCX-4040) on Candida albicans isolates from denture stomatitis patients
Candida albicans biofilms play a key role in denture stomatitis, one of the most common oral pathologies in elderly people. Because biofilms are highly resistant to antifungals, new pharmacological strategies are needed. Aspirin and nitric oxide-donor molecules have both shown antibiofilm effects on...
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| creator | Madariaga-Venegas, Francisco Fernández-Soto, Roberto Duarte, Luisa Fernanda Suarez, Nicole Delgadillo, Daniela Jara, José A Fernández-Ramires, Ricardo Urzúa, Blanca Molina-Berríos, Alfredo |
| description | Candida albicans biofilms play a key role in denture stomatitis, one of the most common oral pathologies in elderly people. Because biofilms are highly resistant to antifungals, new pharmacological strategies are needed. Aspirin and nitric oxide-donor molecules have both shown antibiofilm effects on C. albicans, making them promising candidates for treatment. In this study, we evaluated the antifungal/antibiofilm effect of a nitric-oxide releasing aspirin (NO-ASA) on C. albicans isolates from denture stomatitis patients in vitro. Disk diffusion assays showed that while NO-ASA had no antifungal effect, the drug potentiated fluconazole inhibition zone diameters, increasing the effect of fluconazole by 20-30% (p |
| doi_str_mv | 10.1371/journal.pone.0176755 |
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Because biofilms are highly resistant to antifungals, new pharmacological strategies are needed. Aspirin and nitric oxide-donor molecules have both shown antibiofilm effects on C. albicans, making them promising candidates for treatment. In this study, we evaluated the antifungal/antibiofilm effect of a nitric-oxide releasing aspirin (NO-ASA) on C. albicans isolates from denture stomatitis patients in vitro. Disk diffusion assays showed that while NO-ASA had no antifungal effect, the drug potentiated fluconazole inhibition zone diameters, increasing the effect of fluconazole by 20-30% (p<0.05). The effect of NO-ASA on the morphogenesis of C. albicans was evaluated using light microscopy after inducing hyphae formation. For all clinical strains assayed, 125 μM NO-ASA significantly decreased the number of filamentous cells present (p<0.01). Adhesion to abiotic surfaces, a critical event for biofilm formation, was evaluated in 96-well polystyrene plates using crystal violet assay; 125 μM NO-ASA significantly inhibited adhesion. Biofilms were observed with scanning electron microscopy (SEM) and quantified using XTT reduction assay. NO-ASA decreased biofilm formation (IC50 ranging from 300 μM to 700 μM), consistent with SEM findings of altered biofilm microarchitecture. PGE2 and carboxy-PTIO (an NO scavenger) both blocked the antibiofilm effects of NO-ASA, suggesting that the efficacy of NO-ASA may be associated with both inhibition of PGE2 synthesis and release of NO. NO-ASA is a promising novel antibiofilm agent for treating fluconazole-resistant strains of C. albicans.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0176755</identifier><identifier>PMID: 28493889</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adhesion ; Antifungal activity ; Antifungal agents ; Antifungal Agents - pharmacology ; Antifungal Agents - therapeutic use ; Antimicrobial agents ; Aspirin ; Aspirin - analogs & derivatives ; Aspirin - pharmacology ; Aspirin - therapeutic use ; Assaying ; Bacterial Adhesion - drug effects ; Biofilms ; Biofilms - drug effects ; Biology and Life Sciences ; Candida albicans ; Candida albicans - drug effects ; Candida albicans - isolation & purification ; Candida albicans - ultrastructure ; Care and treatment ; Dental materials ; Dentistry ; Dentures ; Dinoprostone - metabolism ; Disease ; Dosage and administration ; Drug resistance ; Drug Resistance, Fungal - drug effects ; Electron microscopy ; Fluconazole ; Fluconazole - pharmacology ; Fluconazole - therapeutic use ; Free Radical Scavengers - pharmacology ; Fungicides ; Geriatrics ; Humans ; Hyphae ; Infections ; Inflammation ; Inhibition ; Inhibitory Concentration 50 ; Light microscopy ; Medicine and Health Sciences ; Microbial Viability - drug effects ; Morphogenesis ; Na+/Ca2+ exchanger ; Nitric oxide ; Nitro Compounds - pharmacology ; Nitro Compounds - therapeutic use ; Nonsteroidal anti-inflammatory drugs ; Older people ; Optical microscopy ; Polystyrene ; Polystyrene resins ; Prostaglandin E2 ; Prostheses ; Research and Analysis Methods ; Scanning electron microscopy ; Stomatitis ; Stomatitis, Denture - drug therapy ; Stomatitis, Denture - microbiology ; Yeast</subject><ispartof>PloS one, 2017-05, Vol.12 (5), p.e0176755-e0176755</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Madariaga-Venegas et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2017 Madariaga-Venegas et al 2017 Madariaga-Venegas et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c523t-8378907829b5e58be98f90c77c2ec1d641b3fd39967e7ed93f1d58559ea49c383</citedby><cites>FETCH-LOGICAL-c523t-8378907829b5e58be98f90c77c2ec1d641b3fd39967e7ed93f1d58559ea49c383</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5426659/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5426659/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28493889$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Madariaga-Venegas, Francisco</creatorcontrib><creatorcontrib>Fernández-Soto, Roberto</creatorcontrib><creatorcontrib>Duarte, Luisa Fernanda</creatorcontrib><creatorcontrib>Suarez, Nicole</creatorcontrib><creatorcontrib>Delgadillo, Daniela</creatorcontrib><creatorcontrib>Jara, José A</creatorcontrib><creatorcontrib>Fernández-Ramires, Ricardo</creatorcontrib><creatorcontrib>Urzúa, Blanca</creatorcontrib><creatorcontrib>Molina-Berríos, Alfredo</creatorcontrib><title>Characterization of a novel antibiofilm effect of nitric oxide-releasing aspirin (NCX-4040) on Candida albicans isolates from denture stomatitis patients</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Candida albicans biofilms play a key role in denture stomatitis, one of the most common oral pathologies in elderly people. Because biofilms are highly resistant to antifungals, new pharmacological strategies are needed. Aspirin and nitric oxide-donor molecules have both shown antibiofilm effects on C. albicans, making them promising candidates for treatment. In this study, we evaluated the antifungal/antibiofilm effect of a nitric-oxide releasing aspirin (NO-ASA) on C. albicans isolates from denture stomatitis patients in vitro. Disk diffusion assays showed that while NO-ASA had no antifungal effect, the drug potentiated fluconazole inhibition zone diameters, increasing the effect of fluconazole by 20-30% (p<0.05). The effect of NO-ASA on the morphogenesis of C. albicans was evaluated using light microscopy after inducing hyphae formation. For all clinical strains assayed, 125 μM NO-ASA significantly decreased the number of filamentous cells present (p<0.01). Adhesion to abiotic surfaces, a critical event for biofilm formation, was evaluated in 96-well polystyrene plates using crystal violet assay; 125 μM NO-ASA significantly inhibited adhesion. Biofilms were observed with scanning electron microscopy (SEM) and quantified using XTT reduction assay. NO-ASA decreased biofilm formation (IC50 ranging from 300 μM to 700 μM), consistent with SEM findings of altered biofilm microarchitecture. PGE2 and carboxy-PTIO (an NO scavenger) both blocked the antibiofilm effects of NO-ASA, suggesting that the efficacy of NO-ASA may be associated with both inhibition of PGE2 synthesis and release of NO. NO-ASA is a promising novel antibiofilm agent for treating fluconazole-resistant strains of C. albicans.</description><subject>Adhesion</subject><subject>Antifungal activity</subject><subject>Antifungal agents</subject><subject>Antifungal Agents - pharmacology</subject><subject>Antifungal Agents - therapeutic use</subject><subject>Antimicrobial agents</subject><subject>Aspirin</subject><subject>Aspirin - analogs & derivatives</subject><subject>Aspirin - pharmacology</subject><subject>Aspirin - therapeutic use</subject><subject>Assaying</subject><subject>Bacterial Adhesion - drug effects</subject><subject>Biofilms</subject><subject>Biofilms - drug effects</subject><subject>Biology and Life Sciences</subject><subject>Candida albicans</subject><subject>Candida albicans - drug effects</subject><subject>Candida albicans - isolation & purification</subject><subject>Candida albicans - ultrastructure</subject><subject>Care and treatment</subject><subject>Dental materials</subject><subject>Dentistry</subject><subject>Dentures</subject><subject>Dinoprostone - metabolism</subject><subject>Disease</subject><subject>Dosage and administration</subject><subject>Drug resistance</subject><subject>Drug Resistance, Fungal - drug effects</subject><subject>Electron microscopy</subject><subject>Fluconazole</subject><subject>Fluconazole - pharmacology</subject><subject>Fluconazole - therapeutic use</subject><subject>Free Radical Scavengers - pharmacology</subject><subject>Fungicides</subject><subject>Geriatrics</subject><subject>Humans</subject><subject>Hyphae</subject><subject>Infections</subject><subject>Inflammation</subject><subject>Inhibition</subject><subject>Inhibitory Concentration 50</subject><subject>Light microscopy</subject><subject>Medicine and Health Sciences</subject><subject>Microbial Viability - drug effects</subject><subject>Morphogenesis</subject><subject>Na+/Ca2+ exchanger</subject><subject>Nitric oxide</subject><subject>Nitro Compounds - pharmacology</subject><subject>Nitro Compounds - therapeutic use</subject><subject>Nonsteroidal anti-inflammatory drugs</subject><subject>Older people</subject><subject>Optical microscopy</subject><subject>Polystyrene</subject><subject>Polystyrene resins</subject><subject>Prostaglandin E2</subject><subject>Prostheses</subject><subject>Research and Analysis Methods</subject><subject>Scanning electron microscopy</subject><subject>Stomatitis</subject><subject>Stomatitis, Denture - drug therapy</subject><subject>Stomatitis, Denture - microbiology</subject><subject>Yeast</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptUk1v1DAQjRCIlsI_QGCJSzlkseM4ti9I1YqPShVcQOJmOc546yqxF9tbAf-Ef4vTTasuqnywNfPmzbzxq6qXBK8I5eTdVdhFr8fVNnhYYcI7ztij6phI2tRdg-nje--j6llKVxgzKrruaXXUiFZSIeRx9Xd9qaM2GaL7o7MLHgWLNPLhGkakfXa9C9aNEwJrweQ5612OzqDwyw1QRxhBJ-c3SKeti86j0y_rH3WLW_wWFba19oMbNNJj74z2CbkURp0hIRvDhAbweRcBpRym0j67hLblLtH0vHpi9ZjgxXKfVN8_fvi2_lxffP10vj67qA1raK4F5UJiLhrZM2CiBymsxIZz04AhQ9eSntqBStlx4DBIasnABGMSdCsNFfSker3n3Y4hqWWrSREhBca8E7IgzveIIegrtY1u0vG3Ctqpm0CIG6VjdmYEJQXBnWWtkD1tOe50X36lwY0xvGskxoXr_dJt108wmKI06vGA9DDj3aXahGvF2qbr2DzM6UIQw88dpKwmlwyMo_YQdjdzS4JZS2bom_-gD6tbUBtdBDhvQ-lrZlJ11krCKMPNvKXVA6hyBpicKRYsJoHDgnZfYGJIKYK900iwmg18O4yaDawWA5eyV_f3c1d061j6D7RE7gE</recordid><startdate>20170511</startdate><enddate>20170511</enddate><creator>Madariaga-Venegas, Francisco</creator><creator>Fernández-Soto, Roberto</creator><creator>Duarte, Luisa Fernanda</creator><creator>Suarez, Nicole</creator><creator>Delgadillo, Daniela</creator><creator>Jara, José A</creator><creator>Fernández-Ramires, Ricardo</creator><creator>Urzúa, Blanca</creator><creator>Molina-Berríos, Alfredo</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20170511</creationdate><title>Characterization of a novel antibiofilm effect of nitric oxide-releasing aspirin (NCX-4040) on Candida albicans isolates from denture stomatitis patients</title><author>Madariaga-Venegas, Francisco ; Fernández-Soto, Roberto ; Duarte, Luisa Fernanda ; Suarez, Nicole ; Delgadillo, Daniela ; Jara, José A ; Fernández-Ramires, Ricardo ; Urzúa, Blanca ; Molina-Berríos, Alfredo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c523t-8378907829b5e58be98f90c77c2ec1d641b3fd39967e7ed93f1d58559ea49c383</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adhesion</topic><topic>Antifungal activity</topic><topic>Antifungal agents</topic><topic>Antifungal Agents - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Madariaga-Venegas, Francisco</au><au>Fernández-Soto, Roberto</au><au>Duarte, Luisa Fernanda</au><au>Suarez, Nicole</au><au>Delgadillo, Daniela</au><au>Jara, José A</au><au>Fernández-Ramires, Ricardo</au><au>Urzúa, Blanca</au><au>Molina-Berríos, Alfredo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Characterization of a novel antibiofilm effect of nitric oxide-releasing aspirin (NCX-4040) on Candida albicans isolates from denture stomatitis patients</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-05-11</date><risdate>2017</risdate><volume>12</volume><issue>5</issue><spage>e0176755</spage><epage>e0176755</epage><pages>e0176755-e0176755</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Candida albicans biofilms play a key role in denture stomatitis, one of the most common oral pathologies in elderly people. Because biofilms are highly resistant to antifungals, new pharmacological strategies are needed. Aspirin and nitric oxide-donor molecules have both shown antibiofilm effects on C. albicans, making them promising candidates for treatment. In this study, we evaluated the antifungal/antibiofilm effect of a nitric-oxide releasing aspirin (NO-ASA) on C. albicans isolates from denture stomatitis patients in vitro. Disk diffusion assays showed that while NO-ASA had no antifungal effect, the drug potentiated fluconazole inhibition zone diameters, increasing the effect of fluconazole by 20-30% (p<0.05). The effect of NO-ASA on the morphogenesis of C. albicans was evaluated using light microscopy after inducing hyphae formation. For all clinical strains assayed, 125 μM NO-ASA significantly decreased the number of filamentous cells present (p<0.01). Adhesion to abiotic surfaces, a critical event for biofilm formation, was evaluated in 96-well polystyrene plates using crystal violet assay; 125 μM NO-ASA significantly inhibited adhesion. Biofilms were observed with scanning electron microscopy (SEM) and quantified using XTT reduction assay. NO-ASA decreased biofilm formation (IC50 ranging from 300 μM to 700 μM), consistent with SEM findings of altered biofilm microarchitecture. PGE2 and carboxy-PTIO (an NO scavenger) both blocked the antibiofilm effects of NO-ASA, suggesting that the efficacy of NO-ASA may be associated with both inhibition of PGE2 synthesis and release of NO. NO-ASA is a promising novel antibiofilm agent for treating fluconazole-resistant strains of C. albicans.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28493889</pmid><doi>10.1371/journal.pone.0176755</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2017-05, Vol.12 (5), p.e0176755-e0176755 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1898007689 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Adhesion Antifungal activity Antifungal agents Antifungal Agents - pharmacology Antifungal Agents - therapeutic use Antimicrobial agents Aspirin Aspirin - analogs & derivatives Aspirin - pharmacology Aspirin - therapeutic use Assaying Bacterial Adhesion - drug effects Biofilms Biofilms - drug effects Biology and Life Sciences Candida albicans Candida albicans - drug effects Candida albicans - isolation & purification Candida albicans - ultrastructure Care and treatment Dental materials Dentistry Dentures Dinoprostone - metabolism Disease Dosage and administration Drug resistance Drug Resistance, Fungal - drug effects Electron microscopy Fluconazole Fluconazole - pharmacology Fluconazole - therapeutic use Free Radical Scavengers - pharmacology Fungicides Geriatrics Humans Hyphae Infections Inflammation Inhibition Inhibitory Concentration 50 Light microscopy Medicine and Health Sciences Microbial Viability - drug effects Morphogenesis Na+/Ca2+ exchanger Nitric oxide Nitro Compounds - pharmacology Nitro Compounds - therapeutic use Nonsteroidal anti-inflammatory drugs Older people Optical microscopy Polystyrene Polystyrene resins Prostaglandin E2 Prostheses Research and Analysis Methods Scanning electron microscopy Stomatitis Stomatitis, Denture - drug therapy Stomatitis, Denture - microbiology Yeast |
| title | Characterization of a novel antibiofilm effect of nitric oxide-releasing aspirin (NCX-4040) on Candida albicans isolates from denture stomatitis patients |
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