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Chapter 19 : From Biology to Drug Development: New Approaches to Combat the Threat of Fungal Biofilms

Authors: Christopher G. Pierce1, Anand Srinivasan2, Anand K. Ramasubramanian3, José L. López-Ribot4
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Affiliations: 1: Departments of Biology, South Texas Center for Emerging Infectious Diseases, The University of Texas at San Antonio, San Antonio, TX 78249; 2: Biomedical Engineering, South Texas Center for Emerging Infectious Diseases, The University of Texas at San Antonio, San Antonio, TX 78249; 3: Biomedical Engineering, South Texas Center for Emerging Infectious Diseases, The University of Texas at San Antonio, San Antonio, TX 78249; 4: Departments of Biology, South Texas Center for Emerging Infectious Diseases, The University of Texas at San Antonio, San Antonio, TX 78249
Content Type: Monograph
Publication Year: 2015

Category: Environmental Microbiology

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Abstract:

Advances in modern medicine are prolonging the lives of severely ill individuals; however, at the same time they are creating an expanding population of compromised patients at increased risk of suffering from invasive fungal infections ( ). These include surgical, transplant, cancer, intensive care unit, and HIV-infected patients, as well as neonates. The use of broad-spectrum antibiotics, parenteral nutrition, medical implant devices, and immune suppression, as well as disruption of mucosal barriers due to surgery, chemotherapy, and radiotherapy represent the most important predisposing factors for these infections. Unfortunately, the mortality rates associated with these fungal infections remain unacceptably high, which clearly points to the many limitations of current antifungal therapy, including the limited armamentarium of antifungal agents, their inherent toxicity, and the emergence of resistance ( ). Fungi are eukaryotic organisms, and there is a paucity of selective targets which can be exploited for antifungal drug development, while at the same time this is also the main reason for the elevated toxicity of some of the current agents ( ). Only three classes of antifungal agents—azoles, polyenes, and echinocandins—constitute the mainstay of antifungal therapy for patients with life-threatening invasive fungal infections. Moreover, the antifungal drug pipeline is mostly dry and, with the exception of isavuconazole, no new agents are expected to reach the market any time soon ( ).

Citation: Pierce C, Srinivasan A, Ramasubramanian A, López-Ribot J. 2015. From Biology to Drug Development: New Approaches to Combat the Threat of Fungal Biofilms, p 373-388. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0007-2014
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From Biology to Drug Development: New Approaches to Combat the Threat of Fungal Biofilms
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Citation: Pierce C, Srinivasan A, Ramasubramanian A, López-Ribot J. 2015. From Biology to Drug Development: New Approaches to Combat the Threat of Fungal Biofilms, p 373-388. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0007-2014
/content/10.1128/9781555817466.chap19.fig19-1
Figure 1
Images depicting the BChip as a new technology platform for microbial culture at the nanoscale level. The technique allows for a variety of high-throughput applications, including ultra-high-throughput drug screening.
10.1128/9781555817466/fig19-1_thmb.gif
10.1128/9781555817466/fig19-1.gif
Image of Figure 1
Figure 1

Images depicting the BChip as a new technology platform for microbial culture at the nanoscale level. The technique allows for a variety of high-throughput applications, including ultra-high-throughput drug screening.

Citation: Pierce C, Srinivasan A, Ramasubramanian A, López-Ribot J. 2015. From Biology to Drug Development: New Approaches to Combat the Threat of Fungal Biofilms, p 373-388. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0007-2014
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References

/content/book/10.1128/9781555817466.chap19
1. Brown GD,, Denning DW,, Gow NA,, Levitz SM,, Netea MG,, White TC . 2012. Hidden killers: human fungal infections. Sci Transl Med 4 : 165rv113. [CrossRef]
2. Ostrosky-Zeichner L,, Casadevall A,, Galgiani JN,, Odds FC,, Rex JH . 2010. An insight into the antifungal pipeline: selected new molecules and beyond. Nat Rev Drug Discov 9 : 719– 727.[PubMed] [CrossRef]
3. Pierce CG,, Lopez-Ribot JL . 2013. Candidiasis drug discovery and development: new approaches targeting virulence for discovering and identifying new drugs. Expert Opin Drug Discov 8 : 1117– 1126.[PubMed] [CrossRef]
4. Pierce CG,, Srinivasan A,, Uppuluri P,, Ramasubramanian AK,, Lopez-Ribot JL . 2013. Antifungal therapy with an emphasis on biofilms. Curr Opin Pharmacol 13 : 726– 730.[PubMed] [CrossRef]
5. Odds FC,, Brown AJ,, Gow NA . 2003. Antifungal agents: mechanisms of action. Trends Microbiol 11 : 272– 279.[PubMed] [CrossRef]
6. Fanning S,, Mitchell AP . 2012. Fungal biofilms. PLoS Pathog 8 : e1002585. doi:10.1371/journal.ppat.1002585. [PubMed] [CrossRef]
7. Ramage G,, Mowat E,, Jones B,, Williams C,, Lopez-Ribot J . 2009. Our current understanding of fungal biofilms. Crit Rev Microbiol 35 : 340– 355.[PubMed] [CrossRef]
8. Ramage G,, Saville SP,, Thomas DP,, Lopez-Ribot JL . 2005. Candida biofilms: an update. Eukaryot Cell 4 : 633– 638.[PubMed] [CrossRef]
9. Kojic EM,, Darouiche RO . 2004. Candida infections of medical devices. Clin Microbiol Rev 17 : 255– 267.[CrossRef]
10. Ramage G,, Martinez JP,, Lopez-Ribot JL . 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 6 : 979– 986.[PubMed] [CrossRef]
11. Crump JA,, Collignon PJ . 2000. Intravascular catheter-associated infections. Eur J Clin Microbiol Infect Dis 19 : 1– 8.[PubMed] [CrossRef]
12. Pierce CG,, Uppuluri P,, Tristan AR,, Wormley FL Jr,, Mowat E,, Ramage G,, Lopez-Ribot JL . 2008. A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc 3 : 1494– 1500.[PubMed] [CrossRef]
13. Ramage G,, VandeWalle K,, Wickes BL,, Lopez-Ribot JL . 2001. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 45 : 2475– 2479.[PubMed] [CrossRef]
14. Blankenship JR,, Mitchell AP . 2006. How to build a biofilm: a fungal perspective. Curr Opin Microbiol 9 : 588– 594.[PubMed] [CrossRef]
15. Nett J,, Andes D . 2006. Candida albicans biofilm development, modeling a host-pathogen interaction. Curr Opin Microbiol 9 : 340– 345.[PubMed] [CrossRef]
16. Chandra J,, Kuhn DM,, Mukherjee PK,, Hoyer LL,, McCormick T,, Ghannoum MA . 2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183 : 5385– 5394.[PubMed] [CrossRef]
17. Ramage G,, VandeWalle K,, Wickes BL,, Lopez-Ribot JL . 2001. Characteristics of biofilm formation by Candida albicans . Rev Iberoam Micol 18 : 163– 170.[PubMed]
18. Bachmann SP,, Patterson TF,, Lopez-Ribot JL . 2002. In vitro activity of caspofungin (MK-0991) against Candida albicans clinical isolates displaying different mechanisms of azole resistance. J Clin Microbiol 40 : 2228– 2230.[PubMed] [CrossRef]
19. Uppuluri P,, Chaturvedi AK,, Srinivasan A,, Banerjee M,, Ramasubramaniam AK,, Kohler JR,, Kadosh D,, Lopez-Ribot JL . 2010. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6 : e1000828. [PubMed] [CrossRef]
20. Andes D,, Nett J,, Oschel P,, Albrecht R,, Marchillo K,, Pitula A . 2004. Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun 72 : 6023– 6031.[PubMed] [CrossRef]
21. Kucharikova S,, Tournu H,, Holtappels M,, Van Dijck P,, Lagrou K . 2010. In vivo efficacy of anidulafungin against mature Candida albicans biofilms in a novel rat model of catheter-associated candidiasis. Antimicrob Agents Chemother 54 : 4474– 4475.[PubMed] [CrossRef]
22. Kucharikova S,, Tournu H,, Lagrou K,, Van Dijck P,, Bujdakova H . 2011. Detailed comparison of Candida albicans and Candida glabrata biofilms under different conditions and their susceptibility to caspofungin and anidulafungin. J Med Microbiol 60 : 1261– 1269.[PubMed] [CrossRef]
23. Lazzell AL,, Chaturvedi AK,, Pierce CG,, Prasad D,, Uppuluri P,, Lopez-Ribot JL . 2009. Treatment and prevention of Candida albicans biofilms with caspofungin in a novel central venous catheter murine model of candidiasis. J Antimicrob Chemother 64 : 567– 570.[PubMed] [CrossRef]
24. Schinabeck MK,, Long LA,, Hossain MA,, Chandra J,, Mukherjee PK,, Mohamed S,, Ghannoum MA . 2004. Rabbit model of Candida albicans biofilm infection: liposomal amphotericin B antifungal lock therapy. Antimicrob Agents Chemother 48 : 1727– 1732.[PubMed] [CrossRef]
25. Shuford JA,, Rouse MS,, Piper KE,, Steckelberg JM,, Patel R . 2006. Evaluation of caspofungin and amphotericin B deoxycholate against Candida albicans biofilms in an experimental intravascular catheter infection model. J Infect Dis 194 : 710– 713.[PubMed] [CrossRef]
26. Nobile CJ,, Fox EP,, Nett JE,, Sorrells TR,, Mitrovich QM,, Hernday AD,, Tuch BB,, Andes DR,, Johnson AD . 2012. A recently evolved transcriptional network controls biofilm development in Candida albicans . Cell 148 : 126– 138.[PubMed] [CrossRef]
27. Nobile CJ,, Mitchell AP . 2006. Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol 8 : 1382– 1391.[PubMed] [CrossRef]
28. Lopez-Ribot JL . 2005. Candida albicans biofilms: more than filamentation. Curr Biol 15 : R453– R455.[PubMed] [CrossRef]
29. Hogan DA . 2006. Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5 : 613– 619.[PubMed] [CrossRef]
30. Ramage G,, Saville SP,, Wickes BL,, Lopez-Ribot JL . 2002. Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68 : 5459– 5463.[PubMed] [CrossRef]
31. Ramage G,, VandeWalle K,, Bachmann SP,, Wickes BL,, Lopez-Ribot JL . 2002. In vitro pharmacodynamic properties of three antifungal agents against preformed Candida albicans biofilms determined by time-kill studies. Antimicrob Agents Chemother 46 : 3634– 3636.[PubMed] [CrossRef]
32. Bachmann SP,, VandeWalle K,, Ramage G,, Patterson TF,, Wickes BL,, Graybill JR,, Lopez-Ribot JL . 2002. In vitro activity of caspofungin against Candida albicans biofilms. Antimicrob Agents Chemother 46 : 3591– 3596.[PubMed] [CrossRef]
33. Kuhn DM,, George T,, Chandra J,, Mukherjee PK,, Ghannoum MA . 2002. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother 46 : 1773– 1780.[PubMed] [CrossRef]
34. Ramage G,, Rajendran R,, Sherry L,, Williams C . 2012. Fungal biofilm resistance. Int J Microbiol 2012 : 528521. [PubMed] [CrossRef]
35. Mathe L,, Van Dijck P . 2013. Recent insights into Candida albicans biofilm resistance mechanisms. Curr Genet 59 : 251– 264.[PubMed] [CrossRef]
36. Taff HT,, Mitchell KF,, Edward JA,, Andes DR . 2013. Mechanisms of Candida biofilm drug resistance. Future Microbiol 8 : 1325– 1337.[PubMed] [CrossRef]
37. Perumal P,, Mekala S,, Chaffin WL . 2007. Role for cell density in antifungal drug resistance in Candida albicans biofilms. Antimicrob Agents Chemother 51 : 2454– 2463.[PubMed] [CrossRef]
38. LaFleur MD,, Kumamoto CA,, Lewis K . 2006. Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob Agents Chemother 50 : 3839– 3846.[PubMed] [CrossRef]
39. Ramage G,, Bachmann S,, Patterson TF,, Wickes BL,, Lopez-Ribot JL . 2002. Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J Antimicrob Chemother 49 : 973– 980.[PubMed] [CrossRef]
40. Mukherjee PK,, Chandra J,, Kuhn DM,, Ghannoum MA . 2003. Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect Immun 71 : 4333– 4340.[PubMed] [CrossRef]
41. Robbins N,, Uppuluri P,, Nett J,, Rajendran R,, Ramage G,, Lopez-Ribot JL,, Andes D,, Cowen LE . 2011. Hsp90 governs dispersion and drug resistance of fungal biofilms. PLoS Pathog 7 : e1002257. [PubMed] [CrossRef]
42. Martins M,, Uppuluri P,, Thomas DP,, Cleary IA,, Henriques M,, Lopez-Ribot JL,, Oliveira R . 2010. Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms. Mycopathologia 169 : 323– 331.[PubMed] [CrossRef]
43. Nett JE,, Sanchez H,, Cain MT,, Andes DR . 2010. Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J Infect Dis 202 : 171– 175.[PubMed] [CrossRef]
44. Frade JP,, Arthington-Skaggs BA . 2011. Effect of serum and surface characteristics on Candida albicans biofilm formation. Mycoses 54 : e154– e162.[PubMed] [CrossRef]
45. Chandra J,, Patel JD,, Li J,, Zhou G,, Mukherjee PK,, McCormick TS,, Anderson JM,, Ghannoum MA . 2005. Modification of surface properties of biomaterials influences the ability of Candida albicans to form biofilms. Appl Environ Microbiol 71 : 8795– 8801.[PubMed] [CrossRef]
46. Valentin A,, Canton E,, Peman J,, Martinez JP . 2012. Voriconazole inhibits biofilm formation in different species of the genus Candida . J Antimicrob Chemother 67 : 2418– 2423.[PubMed] [CrossRef]
47. Redding S,, Bhatt B,, Rawls HR,, Siegel G,, Scott K,, Lopez-Ribot J . 2009. Inhibition of Candida albicans biofilm formation on denture material. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 107 : 669– 672.[PubMed] [CrossRef]
48. Pusateri CR,, Monaco EA,, Edgerton M . 2009. Sensitivity of Candida albicans biofilm cells grown on denture acrylic to antifungal proteins and chlorhexidine. Arch Oral Biol 54 : 588– 594.[PubMed] [CrossRef]
49. Monteiro DR,, Silva S,, Negri M,, Gorup LF,, de Camargo ER,, Oliveira R,, Barbosa DB,, Henriques M . 2013. Antifungal activity of silver nanoparticles in combination with nystatin and chlorhexidine digluconate against Candida albicans and Candida glabrata biofilms. Mycoses 56 : 672– 680.[PubMed] [CrossRef]
50. Silva S,, Pires P,, Monteiro DR,, Negri M,, Gorup LF,, Camargo ER,, Barbosa DB,, Oliveira R,, Williams DW,, Henriques M,, Azeredo J . 2013. The effect of silver nanoparticles and nystatin on mixed biofilms of Candida glabrata and Candida albicans on acrylic. Med Mycol 51 : 178– 184.[PubMed] [CrossRef]
51. Coad BR,, Kidd SE,, Ellis DH,, Griesser HJ . 2014. Biomaterials surfaces capable of resisting fungal attachment and biofilm formation. Biotechnol Adv 32 : 296– 307.[PubMed] [CrossRef]
52. Raad I . 1998. Intravascular-catheter-related infections. Lancet 351 : 893– 898.[PubMed] [CrossRef]
53. Pappas PG,, Kauffman CA,, Andes D,, Benjamin DK Jr,, Calandra TF,, Edwards JE Jr,, Filler SG,, Fisher JF,, Kullberg BJ,, Ostrosky-Zeichner L,, Reboli AC,, Rex JH,, Walsh TJ,, Sobel JD . 2009. Clinical practice guidelines for the management of candidiasis: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis 48 : 503– 535.[PubMed] [CrossRef]
54. Walraven CJ,, Lee SA . 2013. Antifungal lock therapy. Antimicrob Agents Chemother 57 : 1– 8.[PubMed] [CrossRef]
55. Cateau E,, Rodier MH,, Imbert C . 2008. In vitro efficacies of caspofungin or micafungin catheter lock solutions on Candida albicans biofilm growth. J Antimicrob Chemother 62 : 153– 155.[PubMed] [CrossRef]
56. Sherertz RJ,, Boger MS,, Collins CA,, Mason L,, Raad II . 2006. Comparative in vitro efficacies of various catheter lock solutions. Antimicrob Agents Chemother 50 : 1865– 1868.[PubMed] [CrossRef]
57. Sousa C,, Henriques M,, Oliveira R . 2011. Mini-review: antimicrobial central venous catheters: recent advances and strategies. Biofouling 27 : 609– 620.[PubMed] [CrossRef]
58. Mukherjee PK,, Mohamed S,, Chandra J,, Kuhn D,, Liu S,, Antar OS,, Munyon R,, Mitchell AP,, Andes D,, Chance MR,, Rouabhia M,, Ghannoum MA . 2006. Alcohol dehydrogenase restricts the ability of the pathogen Candida albicans to form a biofilm on catheter surfaces through an ethanol-based mechanism. Infect Immun 74 : 3804– 3816.[PubMed] [CrossRef]
59. LaFleur MD,, Lucumi E,, Napper AD,, Diamond SL,, Lewis K . 2011. Novel high-throughput screen against Candida albicans identifies antifungal potentiators and agents effective against biofilms. J Antimicrob Chemother 66 : 820– 826.[PubMed] [CrossRef]
60. LaFleur MD,, Sun L,, Lister I,, Keating J,, Nantel A,, Long L,, Ghannoum M,, North J,, Lee RE,, Coleman K,, Dahl T,, Lewis K . 2013. Potentiation of azole antifungals by 2-adamantanamine. Antimicrob Agents Chemother 57 : 3585– 3592.[PubMed] [CrossRef]
61. Midkiff J,, Borochoff-Porte N,, White D,, Johnson DI . 2011. Small molecule inhibitors of the Candida albicans budded-to-hyphal transition act through multiple signaling pathways. PLoS One 6 : e25395. doi:10.1371/journal.pone.0025395. [PubMed] [CrossRef]
62. Grald A,, Yargosz P,, Case S,, Shea K,, Johnson DI . 2012. Small-molecule inhibitors of biofilm formation in laboratory and clinical isolates of Candida albicans . J Med Microbiol 61 : 109– 114.[PubMed] [CrossRef]
63. Fazly A,, Jain C,, Dehner AC,, Issi L,, Lilly EA,, Ali A,, Cao H,, Fidel PL Jr,, Rao RP,, Kaufman PD . 2013. Chemical screening identifies filastatin, a small molecule inhibitor of Candida albicans adhesion, morphogenesis, and pathogenesis. Proc Natl Acad Sci USA 110 : 13594– 13599.[PubMed] [CrossRef]
64. Wong SS,, Kao RY,, Yuen KY,, Wang Y,, Yang D,, Samaranayake LP,, Seneviratne CJ . 2014. In vitro and in vivo activity of a novel antifungal small molecule against Candida infections. PLoS One 9 : e85836. doi:10.1371/journal.pone.0085836. [PubMed] [CrossRef]
65. Pierce CG,, Saville SP,, Lopez-Ribot JL . 2014. High content phenotypic screenings to identify inhibitors of Candida albicans biofilm formation and filamentation. Pathog Dis 70 : 423– 431.[PubMed] [CrossRef]
66. Srinivasan A,, Leung KP,, Lopez-Ribot JL,, Ramasubramanian AK . 2013. High-throughput nano-biofilm microarray for antifungal drug discovery. mBio 4 : e00331-13. doi:10.1128/mBio.00331-13. [PubMed] [CrossRef]
67. Srinivasan A,, Uppuluri P,, Lopez-Ribot J,, Ramasubramanian AK . 2011. Development of a high-throughput Candida albicans biofilm chip. PLoS One 6 : e19036. doi:10.1371/journal.pone.0019036. [PubMed] [CrossRef]
68. Tobinick EL . 2009. The value of drug repositioning in the current pharmaceutical market. Drug News Perspect 22 : 119– 125.[PubMed] [CrossRef]
69. Alem MA,, Douglas LJ . 2004. Effects of aspirin and other nonsteroidal anti-inflammatory drugs on biofilms and planktonic cells of Candida albicans . Antimicrob Agents Chemother 48 : 41– 47.[CrossRef]
70. Stepanovic S,, Vukovic D,, Jesic M,, Ranin L . 2004. Influence of acetylsalicylic acid (aspirin) on biofilm production by Candida species. J Chemother 16 : 134– 138.[PubMed] [CrossRef]
71. Chavez-Dozal AA,, Jahng M,, Rane HS,, Asare K,, Kulkarny VV,, Bernardo SM,, Lee SA . 2014. In vitro analysis of flufenamic acid activity against Candida albicans biofilms. Int J Antimicrob Agents 43 : 86– 91.[PubMed] [CrossRef]
72. Siles SA,, Srinivasan A,, Pierce CG,, Lopez-Ribot JL,, Ramasubramanian AK . 2013. High-throughput screening of a collection of known pharmacologically active small compounds for the identification of Candida albicans biofilm inhibitors. Antimicrob Agents Chemother 57 : 3681– 3687.[PubMed] [CrossRef]
73. Sardi JC,, Scorzoni L,, Bernardi T,, Fusco-Almeida AM,, Mendes Giannini MJ . 2013. Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol 62 : 10– 24.[PubMed] [CrossRef]
74. Delattin N,, De Brucker K,, Craik DJ,, Cheneval O,, Frohlich M,, Veber M,, Girandon L,, Davis TR,, Weeks AE,, Kumamoto CA,, Cos P,, Coenye T,, De Coninck B,, Cammue BP,, Thevissen K . 2014. The plant-derived decapeptide OSIP108 interferes with Candida albicans biofilm formation without affecting cell viability. Antimicrob Agents Chemother 58 : 2647– 2656.[PubMed] [CrossRef]
75. You J,, Du L,, King JB,, Hall BE,, Cichewicz RH . 2013. Small-molecule suppressors of Candida albicans biofilm formation synergistically enhance the antifungal activity of amphotericin B against clinical Candida isolates. ACS Chem Biol 8 : 840– 848.[PubMed] [CrossRef]
76. Martinez LR,, Mihu MR,, Han G,, Frases S,, Cordero RJ,, Casadevall A,, Friedman AJ,, Friedman JM,, Nosanchuk JD . 2010. The use of chitosan to damage Cryptococcus neoformans biofilms. Biomaterials 31 : 669– 679.[PubMed] [CrossRef]
77. Martinez LR,, Mihu MR,, Tar M,, Cordero RJ,, Han G,, Friedman AJ,, Friedman JM,, Nosanchuk JD . 2010. Demonstration of antibiofilm and antifungal efficacy of chitosan against candidal biofilms, using an in vivo central venous catheter model. J Infect Dis 201 : 1436– 1440.[PubMed] [CrossRef]
78. Alem MA,, Oteef MD,, Flowers TH,, Douglas LJ . 2006. Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryot Cell 5 : 1770– 1779.[PubMed] [CrossRef]
79. Chen H,, Fujita M,, Feng Q,, Clardy J,, Fink GR . 2004. Tyrosol is a quorum-sensing molecule in Candida albicans . Proc Natl Acad Sci USA 101 : 5048– 5052.[PubMed] [CrossRef]
80. Hornby JM,, Jensen EC,, Lisec AD,, Tasto JJ,, Jahnke B,, Shoemaker R,, Dussault P,, Nickerson KW . 2001. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67 : 2982– 2992.[PubMed] [CrossRef]
81. Navarathna DH,, Hornby JM,, Krishnan N,, Parkhurst A,, Duhamel GE,, Nickerson KW . 2007. Effect of farnesol on a mouse model of systemic candidiasis, determined by use of a DPP3 knockout mutant of Candida albicans . Infect Immun 75 : 1609– 1618.[PubMed] [CrossRef]
82. Sharma M,, Prasad R . 2011. The quorum-sensing molecule farnesol is a modulator of drug efflux mediated by ABC multidrug transporters and synergizes with drugs in Candida albicans . Antimicrob Agents Chemother 55 : 4834– 4843.[PubMed] [CrossRef]
83. Martins M,, Henriques M,, Azeredo J,, Rocha SM,, Coimbra MA,, Oliveira R . 2007. Morphogenesis control in Candida albicans and Candida dubliniensis through signaling molecules produced by planktonic and biofilm cells. Eukaryot Cell 6 : 2429– 2436.[PubMed] [CrossRef]
84. Martins M,, Lazzell AL,, Lopez-Ribot JL,, Henriques M,, Oliveira R . 2012. Effect of exogenous administration of Candida albicans autoregulatory alcohols in a murine model of hematogenously disseminated candidiasis. J Basic Microbiol 52 : 487– 491.[PubMed] [CrossRef]
85. Hogan DA,, Vik A,, Kolter R . 2004. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54 : 1212– 1223.[PubMed] [CrossRef]
86. Gibson J,, Sood A,, Hogan DA . 2009. Pseudomonas aeruginosa- Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl Environ Microbiol 75 : 504– 513.[PubMed] [CrossRef]
87. Morales DK,, Jacobs NJ,, Rajamani S,, Krishnamurthy M,, Cubillos-Ruiz JR,, Hogan DA . 2010. Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms. Mol Microbiol 78 : 1379– 1392.[PubMed] [CrossRef]
88. Joyner PM,, Liu J,, Zhang Z,, Merritt J,, Qi F,, Cichewicz RH . 2010. Mutanobactin A from the human oral pathogen Streptococcus mutans is a cross-kingdom regulator of the yeast-mycelium transition. Org Biomol Chem 8 : 5486– 5489.[PubMed] [CrossRef]
89. Wang X,, Du L,, You J,, King JB,, Cichewicz RH . 2012. Fungal biofilm inhibitors from a human oral microbiome-derived bacterium. Org Biomol Chem 10 : 2044– 2050.[PubMed] [CrossRef]
90. Bugli F,, Posteraro B,, Papi M,, Torelli R,, Maiorana A,, Paroni Sterbini F,, Posteraro P,, Sanguinetti M,, De Spirito M . 2013. In vitro interaction between alginate lyase and amphotericin B against Aspergillus fumigatus biofilm determined by different methods. Antimicrob Agents Chemother 57 : 1275– 1282.[PubMed] [CrossRef]
91. Nobile CJ,, Nett JE,, Hernday AD,, Homann OR,, Deneault JS,, Nantel A,, Andes DR,, Johnson AD,, Mitchell AP . 2009. Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 7 : e1000133. doi:10.1371/journal.pbio.1000133. [PubMed] [CrossRef]
92. Taff HT,, Nett JE,, Zarnowski R,, Ross KM,, Sanchez H,, Cain MT,, Hamaker J,, Mitchell AP,, Andes DR . 2012. A Candida biofilm-induced pathway for matrix glucan delivery: implications for drug resistance. PLoS Pathog 8 : e1002848. doi:10.1371/journal.ppat.1002848. [PubMed] [CrossRef]
93. Lopez-Ribot JL,, Casanova M,, Murgui A,, Martinez JP . 2004. Antibody response to Candida albicans cell wall antigens. FEMS Immunol Med Microbiol 41 : 187– 196.[PubMed] [CrossRef]
94. Fujibayashi T,, Nakamura M,, Tominaga A,, Satoh N,, Kawarai T,, Narisawa N,, Shinozuka O,, Watanabe H,, Yamazaki T,, Senpuku H . 2009. Effects of IgY against Candida albicans and Candida spp. adherence and biofilm formation. Jpn J Infect Dis 62 : 337– 342.[PubMed]
95. Bujdakova H,, Paulovicova E,, Paulovicova L,, Simova Z . 2010. Participation of the Candida albicans surface antigen in adhesion, the first phase of biofilm development. FEMS Immunol Med Microbiol 59 : 485– 492.[PubMed] [CrossRef]
96. Martinez LR,, Casadevall A . 2007. Cryptococcus neoformans biofilm formation depends on surface support and carbon source and reduces fungal cell susceptibility to heat, cold, and UV light. Appl Environ Microbiol 73 : 4592– 4601.[PubMed] [CrossRef]
97. Martinez LR,, Christaki E,, Casadevall A . 2006. Specific antibody to Cryptococcus neoformans glucurunoxylomannan antagonizes antifungal drug action against cryptococcal biofilms in vitro . J Infect Dis 194 : 261– 266.[PubMed] [CrossRef]
98. Bachmann SP,, Ramage G,, VandeWalle K,, Patterson TF,, Wickes BL,, Lopez-Ribot JL . 2003. Antifungal combinations against Candida albicans biofilms in vitro . Antimicrob Agents Chemother 47 : 3657– 3659.[PubMed] [CrossRef]
99. Sarkar S,, Uppuluri P,, Pierce CG,, Lopez-Ribot JL . 2014. In vitro study of sequential fluconazole and caspofungin treatment against Candida albicans biofilms. Antimicrob Agents Chemother 58 : 1183– 1186.[PubMed] [CrossRef]
100. Uppuluri P,, Nett J,, Heitman J,, Andes D . 2008. Synergistic effect of calcineurin inhibitors and fluconazole against Candida albicans biofilms. Antimicrob Agents Chemother 52 : 1127– 1132.[PubMed] [CrossRef]
101. Costa AC,, Pereira CA,, Freire F,, Junqueira JC,, Jorge AO . 2013. Methods for obtaining reliable and reproducible results in studies of Candida biofilms formed in vitro . Mycoses 56 : 614– 622.[PubMed] [CrossRef]
102. Junqueira JC,, Jorge AO,, Barbosa JO,, Rossoni RD,, Vilela SF,, Costa AC,, Primo FL,, Goncalves JM,, Tedesco AC,, Suleiman JM . 2012. Photodynamic inactivation of biofilms formed by Candida spp., Trichosporon mucoides, and Kodamaea ohmeri by cationic nanoemulsion of zinc 2,9,16,23-tetrakis(phenylthio)-29H, 31H–phthalocyanine (ZnPc). Lasers Med Sci 27 : 1205– 1212.[PubMed] [CrossRef]
103. Pereira CA,, Romeiro RL,, Costa AC,, Machado AK,, Junqueira JC,, Jorge AO . 2011. Susceptibility of Candida albicans, Staphylococcus aureus, and Streptococcus mutans biofilms to photodynamic inactivation: an in vitro study. Lasers Med Sci 26 : 341– 348.[PubMed] [CrossRef]
104. Dovigo LN,, Pavarina AC,, Carmello JC,, Machado AL,, Brunetti IL,, Bagnato VS . 2011. Susceptibility of clinical isolates of Candida to photodynamic effects of curcumin. Lasers Surg Med 43 : 927– 934.[PubMed] [CrossRef]
105. Dovigo LN,, Pavarina AC,, Ribeiro AP,, Brunetti IL,, Costa CA,, Jacomassi DP,, Bagnato VS,, Kurachi C . 2011. Investigation of the photodynamic effects of curcumin against Candida albicans . Photochem Photobiol 87 : 895– 903.[PubMed] [CrossRef]
106. Khan S,, Alam F,, Azam A,, Khan AU . 2012. Gold nanoparticles enhance methylene blue-induced photodynamic therapy: a novel therapeutic approach to inhibit Candida albicans biofilm. Int J Nanomed 7 : 3245– 3257.[PubMed] [CrossRef]

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