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Chapter 6 : Biofilms: Development, Architecture, and Resistance

Authors: Jyotsna Chandra1, Pranab K. Mukherjee2
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Affiliations: 1: Center for Medical Mycology and Mycology Reference Laboratory, Department of Dermatology, University Hospitals of Cleveland and Case Western Reserve University, Cleveland, OH 44106; 2: Center for Medical Mycology and Mycology Reference Laboratory, Department of Dermatology, University Hospitals of Cleveland and Case Western Reserve University, Cleveland, OH 44106
Content Type: Monograph
Publication Year: 2015

Category: Environmental Microbiology

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Biofilms: Development, Architecture, and Resistance, Page 1 of 2

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Abstract:

The use of indwelling devices in current therapeutic practice is associated with hospital-acquired bloodstream and deep tissue infections ( ). Transplantation medical procedures, immunosuppression, and prolonged intensive care unit stays have also increased the prevalence of nosocomial infections. Device-associated infections are commonly associated with the ability of bacteria and fungi to form biofilms, which are defined as communities of sessile organisms irreversibly associated with a surface, encased within a polysaccharide-rich extracellular matrix, and exhibiting enhanced resistance to antimicrobial drugs ( ). Forming a biofilm provides the microbes protection from host immunity, environmental stresses due to contaminants, and nutritional depletion or imbalances, while being dangerous to human health due to biofilms’ inherent robustness and elevated resistance.

Citation: Chandra J, Mukherjee P. 2015. Biofilms: Development, Architecture, and Resistance, p 115-134. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0020-2015
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References

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1. Nicastri E,, Petrosiillo N,, Viale P,, Ippolito G . 2001. Catheter-related bloodstream infections in HIV-infected patients. Ann NY Acad Sci 946 : 274– 290.[PubMed] [CrossRef]
2. Costerton JW,, Cheng KJ,, Geesey GG,, Ladd TI,, Nickel JC,, Dasgupta M,, Marrie TJ . 1987. Bacterial biofilms in nature and disease. Annu Rev Microbiol 41 : 435– 464.[PubMed] [CrossRef]
3. Costerton JW,, Lewandowski Z,, Caldwell DE,, Korber DR,, Lappin-Scott HM . 1995. Microbial biofilms. Annu Rev Microbiol 49 : 711– 745.[PubMed] [CrossRef]
4. Costerton JW,, Stewart PS,, Greenberg EP . 1999. Bacterial biofilms: a common cause of persistent infections. Science 284 : 1318– 1322.[PubMed] [CrossRef]
5. Donlan RM . 2002. Biofilms: microbial life on surfaces. Emerg Infect Dis 8 : 881– 890.[PubMed] [CrossRef]
6. Edmond MB,, Wallace SE,, McClish DK,, Pfaller MA,, Jones RN,, Wenzel RP . 1999. Nosocomial bloodstream infections in United States hospitals: a three-year analysis. Clin Infect Dis 29 : 239– 244.[PubMed] [CrossRef]
7. Andes DR,, Safdar N,, Baddley JW,, Playford G,, Reboli AC,, Rex JH,, Sobel JD,, Pappas PG,, Kullberg BJ . 2012. Impact of treatment strategy on outcomes in patients with candidemia and other forms of invasive candidiasis: a patient-level quantitative review of randomized trials. Clin Infect Dis 54 : 1110– 1122.[PubMed] [CrossRef]
8. Costa SF,, Marinho I,, Araujo EA,, Manrique AE,, Medeiros EA,, Levin AS . 2000. Nosocomial fungaemia: a 2-year prospective study. J Hosp Infect 45 : 69– 72.[PubMed] [CrossRef]
9. Moran C,, Grussemeyer CA,, Spalding JR,, Benjamin DK Jr,, Reed SD . 2009. Candida albicans and non- albicans bloodstream infections in adult and pediatric patients: comparison of mortality and costs. Pediatr Infect Dis J 28 : 433– 435.[PubMed] [CrossRef]
10. Viudes A,, Peman J,, Canton E,, Ubeda P,, Lopez-Ribot JL,, Gobernado M . 2002. Candidemia at a tertiary-care hospital: epidemiology, treatment, clinical outcome and risk factors for death. Eur J Clin Microbiol Infect Dis 21 : 767– 774.[PubMed] [CrossRef]
11. Marrie TJ,, Costerton JW . 1984. Scanning and transmission electron microscopy of in situ bacterial colonization of intravenous and intraarterial catheters. J Clin Microbiol 19 : 687– 693.[PubMed]
12. Tchekmedyian NS,, Newman K,, Moody MR,, Costerton JW,, Aisner J,, Schimpff SC,, Reed WP . 1986. Special studies of the Hickman catheter of a patient with recurrent bacteremia and candidemia. Am J Med Sci 291 : 419– 424.[PubMed] [CrossRef]
13. Reid G,, Denstedt JD,, Kang YS,, Lam D,, Nause C . 1992. Microbial adhesion and biofilm formation on ureteral stents in vitro and in vivo . J Urol 148 : 1592– 1594.[PubMed]
14. Elder MJ,, Matheson M,, Stapleton F,, Dart JK . 1996. Biofilm formation in infectious crystalline keratopathy due to Candida albicans . Cornea 15 : 301– 304.[PubMed] [CrossRef]
15. Chandra J,, Mukherjee PK,, Ghannoum MA . 2010. Fungal biofilms in the clinical lab setting. Curr Rep Fungal Inf 4 : 137– 144.[CrossRef]
16. Nett J,, Andes DR . 2006. Candida albicans biofilm development, modeling a host-pathogen interaction. Curr Opin Microbiol 9 : 340– 345.[PubMed] [CrossRef]
17. Douglas LJ . 2003. Candida biofilms and their role in infection. Trends Microbiol 11 : 30– 36.[CrossRef]
18. Baillie GS,, Douglas LJ . 1999. Candida biofilms and their susceptibility to antifungal agents. Methods Enzymol 310 : 644– 656.[CrossRef]
19. Mukherjee PK,, Chand DV,, Chandra J,, Anderson JM,, Ghannoum MA . 2009. Shear stress modulates the thickness and architecture of Candida albicans biofilms in a phase-dependent manner. Mycoses 52 : 440– 446.[PubMed] [CrossRef]
20. 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]
21. Chandra J,, Mukherjee PK,, Leidich SD,, Faddoul FF,, Hoyer LL,, Douglas LJ,, Ghannoum MA . 2001. Antifungal resistance of candidal biofilms formed on denture acrylic in vitro . J Dent Res 80 : 903– 908.[PubMed] [CrossRef]
22. Hawser SP,, Douglas LJ . 1994. Biofilm formation by Candida species on the surface of catheter materials in vitro . Infect Immun 62 : 915– 921.[PubMed]
23. Imamura Y,, Chandra J,, Mukherjee PK,, Abdul Lattif A,, Szczotka-Flynn LB,, Pearlman E,, Lass JH,, O’Donnell K,, Ghannoum MA . 2008. Fusarium and Candida albicans biofilms on soft contact lenses: model development, influence of lens type and susceptibility to lens care solutions. Antimicrob Agents Chemother 52 : 171– 182.[PubMed] [CrossRef]
24. Nikawa H,, Yamamoto T,, Hamada T . 1995. Effect of components of resilient denture-lining materials on the growth, acid production and colonization of Candida albicans . J Oral Rehabil 22 : 817– 824.[PubMed] [CrossRef]
25. Ramage G,, Vande WK,, Wickes BL,, Lopez-Ribot JL . 2001. Biofilm formation by Candida dubliniensis . J Clin Microbiol 39 : 3234– 3240.[PubMed] [CrossRef]
26. Samaranayake YH,, Ye J,, Yau JYY,, Cheung BPK,, Samaranayake LP . 2005. In vitro method to study antifungal perfusion in Candida biofilms. J Clin Microbiol 43 : 818– 825.[PubMed] [CrossRef]
27. Everaert EP,, van de Belt-Gritter B,, van der Mei HC,, Busscher HJ,, Verkerke GJ,, Dijk F,, Mahieu HF,, Reitsma A . 1998. In vitro and in vivo microbial adhesion and growth on argon plasma-treated silicone rubber voice prostheses. J Mater Sci Mater Med 9 : 147– 157.[PubMed] [CrossRef]
28. van der Mei HC,, Free RH,, Elving GJ,, van Weissenbruch R,, Albers FW,, Busscher HJ . 2000. Effect of probiotic bacteria on prevalence of yeasts in oropharyngeal biofilms on silicone rubber voice prostheses in vitro . J Med Microbiol 49 : 713– 718.[PubMed]
29. Chandra J,, Mukherjee PK,, Ghannoum MA . 2008. In vitro growth and analysis of Candida biofilms. Nat Protoc 3 : 1909– 1924.[PubMed] [CrossRef]
30. 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]
31. Nweze EI,, Ghannoum A,, Chandra J,, Ghannoum MA,, Mukherjee PK . 2012. Development of a 96-well catheter-based microdilution method to test antifungal susceptibility of Candida biofilms. J Antimicrob Chemother 67 : 149– 153.[PubMed] [CrossRef]
32. Nweze EI,, Ghannoum A,, Chandra J,, Ghannoum MA,, Mukherjee PK . 2010. Microdilution method to test antifungal susceptibility of biofilms (BFs) formed by Candida (CA) on catheters. Presented at the 50th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC); Abstract Number M-1101; Sep 12-15. Boston, MA, American Society for Microbiology.
33. Ceri H,, Olson ME,, Stremick C,, Read RR,, Morck D,, Buret A . 1999. The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37 : 1771– 1776.[PubMed]
34. Almshawit H,, Macreadie I,, Grando D . 2014. A simple and inexpensive device for biofilm analysis. J Microbiol Methods 98 : 59– 63.[PubMed] [CrossRef]
35. Harrison JJ,, Ceri H,, Yerly J,, Rabiei M,, Hu Y,, Martinuzzi R,, Turner RJ . 2007. Metal ions may suppress or enhance cellular differentiation in Candida albicans and Candida tropicalis biofilms. Appl Environ Microbiol. [Epub ahead of print.] doi:AEM.02711-06.
36. Parahitiyawa NB,, Samaranayake YH,, Samaranayake LP,, Ye J,, Tsang PW,, Cheung BP,, Yau JY,, Yeung SK . 2006. Interspecies variation in Candida biofilm formation studied using the Calgary biofilm device. APMIS 114 : 298– 306.[PubMed] [CrossRef]
37. Harrison JJ,, Turner RJ,, Ceri H . 2007. A subpopulation of Candida albicans and Candida tropicalis biofilm cells are highly tolerant to chelating agents. FEMS Microbiol Lett 272 : 172– 181.[PubMed] [CrossRef]
38. Srinivasan A,, Uppuluri P,, Lopez-Ribot J,, Ramasubramanian AK . 2011. Development of a high-throughput Candida albicans biofilm chip. PLoS One 6 : e19036. doi:10.3791/3845. [CrossRef]
39. Coenye T . 2010. Response of sessile cells to stress: from changes in gene expression to phenotypic adaptation. FEMS Immunol Med Microbiol 59 : 239– 252.[CrossRef]
40. Andes DR,, 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]
41. 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]
42. Zumbuehl A,, Ferreira L,, Kuhn D,, Astashkina A,, Long L,, Yeo Y,, Iaconis T,, Ghannoum M,, Fink GR,, Langer R,, Kohane DS . 2007. Antifungal hydrogels. Proc Natl Acad Sci USA 104 : 12994– 12998.[PubMed] [CrossRef]
43. Mukherjee PK,, Chandra J,, Yu C,, Sun Y,, Pearlman E,, Ghannoum MA . 2012. Characterization of Fusarium keratitis outbreak isolates: contribution of biofilms to antimicrobial resistance and pathogenesis. Invest Ophthalmol Vis Sci 53 : 4450– 4457.[PubMed] [CrossRef]
44. Sun Y,, Chandra J,, Mukherjee PK,, Szczotka-Flynn L,, Ghannoum M,, Pearlman E . 2010. A murine model of contact lens associated Fusarium keratitis. Invest Ophthalmol Vis Sci 51 : 1511– 1516.[PubMed] [CrossRef]
45. Chang DC,, Grant GB,, O’Donnell K,, Wannemuehler KA,, Noble-Wang J,, Rao CY,, Jacobson LM,, Crowell CS,, Sneed RS,, Lewis FM,, Schaffzin JK,, Kainer MA,, Genese CA,, Alfonso EC,, Jones DB,, Srinivasan A,, Fridkin SK,, Park BJ . 2006. Multistate outbreak of Fusarium keratitis associated with use of a contact lens solution. JAMA 296 : 953– 963.[PubMed] [CrossRef]
46. Donnio A,, Van Nuoi DNG,, Catanese M,, Desbois N,, Ayeboua L,, Merle H . 2007. Outbreak of keratomycosis attributable to Fusarium solani in the French West Indies. Am J Ophthalmol 143 : 356– 358.[PubMed] [CrossRef]
47. Khor WB,, Aung T,, Saw SM,, Wong TY,, Tambyah PA,, Tan AL,, Beuerman R,, Lim L,, Chan WK,, Heng WJ,, Lim J,, Loh RS,, Lee SB,, Tan DT . 2006. An outbreak of Fusarium keratitis associated with contact lens wear in Singapore. JAMA 295 : 2867– 2873.[PubMed] [CrossRef]
48. Tournu H,, Van Dijck P . 2012. Candida biofilms and the host: models and new concepts for eradication. Int J Microbiol. doi:10.1155/2012/845352. [CrossRef]
49. Dongari-Bagtzoglou A,, Kashleva H,, Dwivedi P,, Diaz P,, Vasilakos J . 2009. Characterization of mucosal Candida albicans biofilms. PLoS ONE 4 : e7967. doi:10.1371/journal.pone.0007967. [CrossRef]
50. Harriott MM,, Lilly EA,, Rodriguez TE,, Fidel PL Jr,, Noverr MC . 2010. Candida albicans forms biofilms on the vaginal mucosa. Microbiology 156 : 3635– 3644.[PubMed] [CrossRef]
51. Lazarus HM,, Lowder JN,, Herzig RH . 1983. Occlusion and infection in Broviac catheters during intensive cancer therapy. Cancer 52 : 2342– 2348.[CrossRef]
52. 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]
53. Hall-Stoodley L,, Costerton JW,, Stoodley P . 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2 : 95– 108.[PubMed] [CrossRef]
54. Hall-Stoodley L,, Stoodley P . 2002. Developmental regulation of microbial biofilms. Curr Opin Biotechnol 13 : 228– 233.[CrossRef]
55. Kolenbrander PE . 2000. Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol 54 : 413– 437.[PubMed] [CrossRef]
56. Kolenbrander PE,, Palmer RJ,, Periasamy S,, Jakubovics NS . 2010. Oral multispecies biofilm development and the key role of cell–cell distance. Nat Rev Microbiol 8 : 471– 480.[PubMed] [CrossRef]
57. Busscher HJ,, Geertsema-Doornbusch GI,, van der Mei HC . 1997. Adhesion to silicone rubber of yeasts and bacteria isolated from voice prostheses: influence of salivary conditioning films. J Biomed Mater Res 34 : 201– 209.[CrossRef]
58. Millsap KW,, Bos R,, Busscher HJ,, van der Mei HC . 1999. Surface aggregation of Candida albicans on glass in the absence and presence of adhering Streptococcus gordonii in a parallel-plate flow chamber: a surface thermodynamical analysis based on acid-base interactions. J Colloid Interface Sci 212 : 495– 502.[PubMed] [CrossRef]
59. Roosjen A,, Boks NP,, van der Mei HC,, Busscher HJ,, Norde W . 2005. Influence of shear on microbial adhesion to PEO-brushes and glass by convective-diffusion and sedimentation in a parallel plate flow chamber. Colloids Surf B Biointerfaces 46 : 1– 6.[PubMed] [CrossRef]
60. Millsap KW,, Bos R,, van der Mei HC,, Busscher HJ . 1999. Adhesion and surface-aggregation of Candida albicans from saliva on acrylic surfaces with adhering bacteria as studied in a parallel plate flow chamber. Antonie Van Leeuwenhoek 75 : 351– 359.[PubMed] [CrossRef]
61. Zimmermann K,, Bernhardt J,, Knoke M,, Bernhardt H . 2002. Influence of voriconazole and fluconazole on Candida albicans in long-time continuous flow culture. Mycoses 45 : 41– 46.[PubMed] [CrossRef]
62. Suci PA,, Tyler BJ . 2002. Action of chlorhexidine digluconate against yeast and filamentous forms in an early-stage Candida albicans biofilm. Antimicrob Agents Chemother 46 : 3522– 3531.[CrossRef]
63. Hawser SP,, Baillie GS,, Douglas LJ . 1998. Production of extracellular matrix by Candida albicans biofilms. J Med Microbiol 47 : 253– 256.[PubMed] [CrossRef]
64. Al-Fattani MA,, Douglas LJ . 2006. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55 : 999– 1008.[PubMed] [CrossRef]
65. Elving GJ,, van der Mei HC,, Busscher HJ,, van Weissenbruch R,, Albers FW . 2001. Air-flow resistances of silicone rubber voice prostheses after formation of bacterial and fungal biofilms. J Biomed Mater Res 58 : 421– 426. [PubMed] [CrossRef]
66. Elving GJ,, van der Mei HC,, Busscher HJ,, van Weissenbruch R,, Albers FW . 2002. Comparison of the microbial composition of voice prosthesis biofilms from patients requiring frequent versus infrequent replacement. Ann Otol Rhinol Laryngol 111 : 200– 203.[PubMed] [CrossRef]
67. 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 C. albicans to form biofilms. Appl Environ Microbiol 71 : 8795– 8801.[PubMed] [CrossRef]
68. Estivill D,, Arias A,, Torres-Lana A,, Carrillo-Munoz AJ,, Arevalo MP . 2011. Biofilm formation by five species of Candida on three clinical materials. J Microbiol Methods 86 : 238– 242.[PubMed] [CrossRef]
69. Richards S,, Russell C . 1987. The effect of sucrose on the colonization of acrylic by Candida albicans in pure and mixed culture in an artificial mouth. J Appl Bacteriol 62 : 421– 427.[PubMed] [CrossRef]
70. Swindell K,, Lattif AA,, Chandra J,, Mukherjee PK,, Ghannoum MA . 2009. Parenteral lipid emulsion induces germination of Candida albicans and increases biofilm formation on medical catheter surfaces. J Infect Dis 200 : 473– 480.[PubMed] [CrossRef]
71. Samaranayake YH,, Cheung BP,, Yau JY,, Yeung SK,, Samaranayake LP . 2013. Human serum promotes Candida albicans biofilm growth and virulence gene expression on silicone biomaterial. PLoS One 8 : e62902. doi:10.1371/journal.pone.0062902. [CrossRef]
72. Branchini ML,, Pfaller MA,, Rhine-Chalberg J,, Frempong T,, Isenberg HD . 1994. Genotypic variation and slime production among blood and catheter isolates of Candida parapsilosis . J Clin Microbiol 32 : 452– 456.[PubMed]
73. Pfaller MA,, Messer SA,, Hollis RJ . 1995. Variations in DNA subtype, antifungal susceptibility, and slime production among clinical isolates of Candida parapsilosis . Diagn Microbiol Infect Dis 21 : 9– 14.[CrossRef]
74. Kuhn DM,, Chandra J,, Mukherjee PK,, Ghannoum MA . 2002. Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces. Infect Immun 70 : 878– 888.[PubMed] [CrossRef]
75. Silva S,, Henriques M,, Martins A,, Oliveira R,, Williams D,, Azeredo J . 2009. Biofilms of non- Candida albicans Candida species: quantification, structure and matrix composition. Med Mycol 47 : 681– 689.[PubMed] [CrossRef]
76. Lattif AA,, Mukherjee PK,, Chandra J,, Swindell K,, Lockhart SR,, Diekema DJ,, Pfaller MA,, Ghannoum MA . 2010. Characterization of biofilms formed by Candida parapsilosis, C. metapsilosis, and C. orthopsilosis . Int J Med Microbiol 300 : 265– 270.[PubMed] [CrossRef]
77. Holmes AR,, Cannon RD,, Jenkinson HF . 1995. Interactions of Candida albicans with bacteria and salivary molecules in oral biofilms. J Ind Microbiol 15 : 208– 213.[PubMed] [CrossRef]
78. Reid G,, Tieszer C,, Lam D . 1995. Influence of lactobacilli on the adhesion of Staphylococcus aureus and Candida albicans to fibers and epithelial cells. J Ind Microbiol 15 : 248– 253.[PubMed] [CrossRef]
79. Webb BC,, Willcox MD,, Thomas CJ,, Harty DW,, Knox KW . 1995. The effect of sodium hypochlorite on potential pathogenic traits of Candida albicans and other Candida species. Oral Microbiol Immunol 10 : 334– 341.[PubMed] [CrossRef]
80. Adam B,, Baillie GS,, Douglas LJ . 2002. Mixed species biofilms of Candida albicans and Staphylococcus epidermidis . J Med Microbiol 51 : 344– 349.[PubMed]
81. El-Azizi MA,, Starks SE,, Khardori N . 2004. Interactions of Candida albicans with other Candida spp. and bacteria in the biofilms. J Appl Microbiol 96 : 1067– 1073.[PubMed] [CrossRef]
82. Hogan DA,, Kolter R . 2002. Pseudomonas - Candida interactions: an ecological role for virulence factors. Science 296 : 2229– 2232.[PubMed] [CrossRef]
83. Hogan DA,, Vik A,, Kolter R . 2004. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54 : 1212– 1223.[PubMed] [CrossRef]
84. Park SJ,, Han KH,, Park JY,, Choi SJ,, Lee KH . 2014. Influence of bacterial presence on biofilm formation of Candida albicans . Yonsei Med J 55 : 449– 458.[PubMed] [CrossRef]
85. van der Mei HC,, Buijssen KJ,, van der Laan BF,, Ovchinnikova E,, Geertsema-Doornbusch GI,, Atema-Smit J,, van de Belt-Gritter B,, Busscher HJ . 2014. Voice prosthetic biofilm formation and Candida morphogenic conversions in absence and presence of different bacterial strains and species on silicone-rubber. PLoS One 9 : e104508. doi:10.1371/journal.pone.0104508.
86. Holmes AR,, McNab R,, Jenkinson HF . 1996. Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesin-receptor interactions. Infect Immun 64 : 4680– 4685.[PubMed]
87. Vilchez R,, Lemme A,, Ballhausen B,, Thiel V,, Schulz S,, Jansen R,, Sztajer H,, Wagner-Dobler I . 2010. Streptococcus mutans inhibits Candida albicans hyphal formation by the fatty acid signaling molecule trans-2-decenoic acid (SDSF). ChemBioChem 11 : 1552– 1562.[PubMed] [CrossRef]
88. Lindsay AK,, Morales DK,, Liu Z,, Grahl N,, Zhang A,, Willger SD,, Myers LC,, Hogan DA . 2014. Analysis of Candida albicans mutants defective in the Cdk8 module of mediator reveal links between metabolism and biofilm formation. PLoS Genet 10 : e1004567. doi:10.1371/journal.pgen.1004567. [CrossRef]
89. Mear JB,, Kipnis E,, Faure E,, Dessein R,, Schurtz G,, Faure K,, Guery B . 2013. Candida albicans and Pseudomonas aeruginosa interactions: more than an opportunistic criminal association? Med Mal Infect 43 : 146– 151.[PubMed] [CrossRef]
90. Morales DK,, Grahl N,, Okegbe C,, Dietrich LE,, Jacobs NJ,, Hogan DA . 2013. Control of Candida albicans metabolism and biofilm formation by Pseudomonas aeruginosa phenazines. MBio 4 : e00526-12. doi:10.1128/mBio.00526-12. [CrossRef]
91. 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]
92. Lattif AA,, Chandra J,, Chang J,, Liu S,, Zhou G,, Chance MR,, Ghannoum MA,, Mukherjee PK . 2008. Proteomic and pathway analyses reveal phase-dependent over-expression of proteins associated with carbohydrate metabolic pathways in Candida albicans biofilms. Open Proteom J 1 : 5– 26.[CrossRef]
93. Kelly MT,, MacCallum DM,, Clancy SD,, Odds FC,, Brown AJ,, Butler G . 2004. The Candida albicans CaACE2 gene affects morphogenesis, adherence and virulence. Mol Microbiol 53 : 969– 983.[PubMed] [CrossRef]
94. Granger BL,, Flenniken ML,, Davis DA,, Mitchell AP,, Cutler JE . 2005. Yeast wall protein 1 of Candida albicans . Microbiology 151 : 1631– 1644.[PubMed] [CrossRef]
95. Orsi CF,, Borghi E,, Colombari B,, Neglia RG,, Quaglino D,, Ardizzoni A,, Morace G,, Blasi E . 2014. Impact of Candida albicans hyphal wall protein 1 (HWP1) genotype on biofilm production and fungal susceptibility to microglial cells. Microb Pathog 69–70 : 20– 27.[PubMed] [CrossRef]
96. Melo AS,, Padovan AC,, Serafim RC,, Puzer L,, Carmona AK,, Juliano Neto L,, Brunstein A,, Briones MR . 2006. The Candida albicans AAA ATPase homologue of Saccharomyces cerevisiae Rix7p (YLL034c) is essential for proper morphology, biofilm formation and activity of secreted aspartyl proteinases. Genet Mol Res 5 : 664– 687.[PubMed]
97. Dranginis AM,, Rauceo JM,, Coronado JE,, Lipke PN . 2007. A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol Mol Biol Rev 71 : 282– 294.[PubMed] [CrossRef]
98. Zhao X,, Daniels KJ,, Oh SH,, Green CB,, Yeater KM,, Soll DR,, Hoyer LL . 2006. Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152 : 2287– 2299.[PubMed] [CrossRef]
99. Singh V,, Satheesh SV,, Raghavendra ML,, Sadhale PP . 2007. The key enzyme in galactose metabolism, UDP-galactose-4-epimerase, affects cell-wall integrity and morphology in Candida albicans even in the absence of galactose. Fungal Genet Biol 44 : 563– 574.[PubMed] [CrossRef]
100. Bernardo SM,, Khalique Z,, Kot J,, Jones JK,, Lee SA . 2008. Candida albicans VPS1 contributes to protease secretion, filamentation, and biofilm formation. Fungal Genet Biol 45 : 861– 877.[PubMed] [CrossRef]
101. Bernardo SM,, Lee SA . 2010. Candida albicans SUR7 contributes to secretion, biofilm formation, and macrophage killing. BMC Microbiol 10 : 133. [PubMed] [CrossRef]
102. Ferreira C,, Silva S,, Faria-Oliveira F,, Pinho E,, Henriques M,, Lucas C . 2010. Candida albicans virulence and drug-resistance requires the O-acyltransferase Gup1p. BMC Microbiol 10 : 238. [PubMed] [CrossRef]
103. Palanisamy SK,, Ramirez MA,, Lorenz M,, Lee SA . 2010. Candida albicans PEP12 is required for biofilm integrity and in vivo virulence. Eukaryot Cell 9 : 266– 277.[PubMed] [CrossRef]
104. Giacometti R,, Kronberg F,, Biondi RM,, Passeron S . 2011. Candida albicans Tpk1p and Tpk2p isoforms differentially regulate pseudohyphal development, biofilm structure, cell aggregation and adhesins expression. Yeast 28 : 293– 308.[PubMed] [CrossRef]
105. Cleary IA,, Lazzell AL,, Monteagudo C,, Thomas DP,, Saville SP . 2012. BRG1 and NRG1 form a novel feedback circuit regulating Candida albicans hypha formation and virulence. Mol Microbiol 85 : 557– 573.[PubMed] [CrossRef]
106. Banerjee M,, Uppuluri P,, Zhao XR,, Carlisle PL,, Vipulanandan G,, Villar CC,, Lopez-Ribot JL,, Kadosh D . 2013. Expression of UME6, a key regulator of Candida albicans hyphal development, enhances biofilm formation via Hgc1- and Sun41-dependent mechanisms. Eukaryot Cell 12 : 224– 232.[PubMed] [CrossRef]
107. Connolly LA,, Riccombeni A,, Grozer Z,, Holland LM,, Lynch DB,, Andes DR,, Gacser A,, Butler G . 2013. The APSES transcription factor Efg1 is a global regulator that controls morphogenesis and biofilm formation in Candida parapsilosis . Mol Microbiol 90 : 36– 53.[PubMed]
108. Raines SM,, Rane HS,, Bernardo SM,, Binder JL,, Lee SA,, Parra KJ . 2013. Deletion of vacuolar proton-translocating ATPase V(o)a isoforms clarifies the role of vacuolar pH as a determinant of virulence-associated traits in Candida albicans . J Biol Chem 288 : 6190– 6201.[PubMed] [CrossRef]
109. Herrero-de-Dios C,, Alonso-Monge R,, Pla J . 2014. The lack of upstream elements of the Cek1 and Hog1 mediated pathways leads to a synthetic lethal phenotype upon osmotic stress in Candida albicans . Fungal Genet Biol 69 : 31– 42.[PubMed] [CrossRef]
110. Pannanusorn S,, Ramirez-Zavala B,, Lunsdorf H,, Agerberth B,, Morschhauser J,, Romling U . 2014. Characterization of biofilm formation and the role of BCR1 in clinical isolates of Candida parapsilosis . Eukaryot Cell 13 : 438– 451.[PubMed] [CrossRef]
111. Tan X,, Fuchs BB,, Wang Y,, Chen W,, Yuen GJ,, Chen RB,, Jayamani E,, Anastassopoulou C,, Pukkila-Worley R,, Coleman JJ,, Mylonakis E . 2014. The role of Candida albicans SPT20 in filamentation, biofilm formation and pathogenesis. PLoS One 9 : e94468. doi:10.1371/journal.pone.0094468. [CrossRef]
112. Zhang B,, Yu Q,, Jia C,, Wang Y,, Xiao C,, Dong Y,, Xu N,, Wang L,, Li M . 2015. The actin-related protein Sac1 is required for morphogenesis and cell wall integrity in Candida albicans . Fungal Genet Biol. [Epub ahead of print.] doi:10.1016/j.fgb.2014.12.007. [CrossRef]
113. Nigam S,, Ciccoli R,, Ivanov I,, Sczepanski M,, Deva R . 2011. On mechanism of quorum sensing in Candida albicans by 3(R)-hydroxy-tetradecaenoic acid. Curr Microbiol 62 : 55– 63.[PubMed] [CrossRef]
114. Deveau A,, Hogan DA . 2011. Linking quorum sensing regulation and biofilm formation by Candida albicans . Methods Mol Biol 692 : 219– 233.[PubMed] [CrossRef]
115. Pammi M,, Liang R,, Hicks JM,, Barrish J,, Versalovic J . 2011. Farnesol decreases biofilms of Staphylococcus epidermidis and exhibits synergy with nafcillin and vancomycin. Pediatr Res 70 : 578– 583.[PubMed] [CrossRef]
116. Weber K,, Schulz B,, Ruhnke M . 2010. The quorum-sensing molecule E,E-farnesol: its variable secretion and its impact on the growth and metabolism of Candida species . Yeast 27 : 727– 739.[PubMed] [CrossRef]
117. Yu LH,, Wei X,, Ma M,, Chen XJ,, Xu SB . 2012. Possible inhibitory molecular mechanism of farnesol on the development of fluconazole resistance in Candida albicans biofilm. Antimicrob Agents Chemother 56 : 770– 775.[PubMed] [CrossRef]
118. Tian J,, Weng LX,, Zhang YQ,, Wang LH . 2013. BDSF inhibits Candida albicans adherence to urinary catheters. Microb Pathog 64 : 33– 38.[PubMed] [CrossRef]
119. Yeater KM,, Chandra J,, Cheng G,, Mukherjee PK,, Zhao X,, Rodriguez-Zas SL,, Kwast KE,, Ghannoum MA,, Hoyer LL . 2007. Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology 153 : 2373– 2385.[PubMed] [CrossRef]
120. Bonhomme J,, Chauvel M,, Goyard S,, Roux P,, Rossignol T,, d’Enfert C . 2011. Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans . Mol Microbiol 80 : 995– 1013.[PubMed] [CrossRef]
121. Baillie GS,, Douglas LJ . 1998. Effect of growth rate on resistance of Candida albicans biofilms to antifungal agents. Antimicrob Agents Chemother 42 : 1900– 1905.[PubMed]
122. Baillie GS,, Douglas LJ . 1998. Iron-limited biofilms of Candida albicans and their susceptibility to amphotericin B. Antimicrob Agents Chemother 42 : 2146– 2149.[PubMed]
123. Hawser SP,, Douglas LJ . 1995. Resistance of Candida albicans biofilms to antifungal agents in vitro . Antimicrob Agents Chemother 39 : 2128– 2131.[PubMed] [CrossRef]
124. Kalya AV,, Ahearn DG . 1995. Increased resistance to antifungal antibiotics of Candida spp. adhered to silicone J Ind Microbiol 14 : 451– 455.[CrossRef]
125. 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]
126. 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]
127. Bernhardt H,, Knoke M,, Bernhardt J . 2003. Changes in Candida albicans colonization and morphology under influence of voriconazole. Mycoses 46 : 370– 374.[PubMed] [CrossRef]
128. 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]
129. Cateau E,, Levasseur P,, Borgonovi M,, Imbert C . 2007. The effect of aminocandin (HMR 3270) on the in-vitro adherence of Candida albicans to polystyrene surfaces coated with extracellular matrix proteins or fibronectin. Clin Microbiol Infect 13 : 311– 315.[PubMed] [CrossRef]
130. Kaneko Y,, Miyagawa S,, Takeda O,, Hakariya M,, Matsumoto S,, Ohno H,, Miyazaki Y . 2013. Real-time microscopic observation of Candida biofilm development and effects due to micafungin and fluconazole. Antimicrob Agents Chemother 57 : 2226– 2230.[PubMed] [CrossRef]
131. Melo AS,, Colombo AL,, Arthington-Skaggs BA . 2007. Paradoxical growth effect of caspofungin observed on biofilms and planktonic cells of five different Candida species. Antimicrob Agents Chemother 51 : 3081– 3088.[PubMed] [CrossRef]
132. Bersan SM,, Galvao LC,, Goes VF,, Sartoratto A,, Figueira GM,, Rehder VL,, Alencar SM,, Duarte RM,, Rosalen PL,, Duarte MC . 2014. Action of essential oils from Brazilian native and exotic medicinal species on oral biofilms. BMC Complement Altern Med 14 : 451. [PubMed] [CrossRef]
133. da Silva PM,, Acosta EJ,, Pinto Lde R,, Graeff M,, Spolidorio DM,, Almeida RS,, Porto VC . 2011. Microscopical analysis of Candida albicans biofilms on heat-polymerised acrylic resin after chlorhexidine gluconate and sodium hypochlorite treatments. Mycoses 54 : e712– e717.[PubMed] [CrossRef]
134. 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]
135. Furletti VF,, Teixeira IP,, Obando-Pereda G,, Mardegan RC,, Sartoratto A,, Figueira GM,, Duarte RM,, Rehder VL,, Duarte MC,, Hofling JF . 2011. Action of Coriandrum sativum L. essential oil upon oral Candida albicans biofilm formation. Evid Based Complement Alternat Med 2011 : 985832. [PubMed] [CrossRef]
136. Lee HJ,, Park HS,, Kim KH,, Kwon TY,, Hong SH . 2011. Effect of garlic on bacterial biofilm formation on orthodontic wire. Angle Orthod 81 : 895– 900.[PubMed] [CrossRef]
137. de Freitas Lima R,, Alves EP,, Rosalen PL,, Ruiz AL,, Teixeira Duarte MC,, Goes VF,, de Medeiros AC,, Pereira JV,, Godoy GP,, Melo de Brito Costa EM . 2014. Antimicrobial and antiproliferative potential of Anadenanthera colubrina (Vell.) Brenan. Evid Based Complement Alternat Med 2014 : 802696.
138. Palmeira-de-Oliveira A,, Gaspar C,, Palmeira-de-Oliveira R,, Silva-Dias A,, Salgueiro L,, Cavaleiro C,, Pina-Vaz C,, Martinez-de-Oliveira J,, Queiroz JA,, Rodrigues AG . 2012. The anti- Candida activity of Thymbra capitata essential oil: effect upon pre-formed biofilm. J Ethnopharmacol 140 : 379– 383.[PubMed] [CrossRef]
139. Raut JS,, Shinde RB,, Chauhan NM,, Karuppayil SM . 2013. Terpenoids of plant origin inhibit morphogenesis, adhesion, and biofilm formation by Candida albicans . Biofouling 29 : 87– 96.[PubMed] [CrossRef]
140. Sudjana AN,, Carson CF,, Carson KC,, Riley TV,, Hammer KA . 2012. Candida albicans adhesion to human epithelial cells and polystyrene and formation of biofilm is reduced by sub-inhibitory Melaleuca alternifolia (tea tree) essential oil. Med Mycol 50 : 863– 870.[PubMed] [CrossRef]
141. Traboulsi RS,, Mukherjee PK,, Chandra J,, Salata RA,, Jurevic R,, Ghannoum MA . 2011. Gentian violet exhibits activity against biofilms formed by oral Candida isolates obtained from HIV-infected patients. Antimicrob Agents Chemother 55 : 3043– 3045.[PubMed] [CrossRef]
142. Villa F,, Pitts B,, Stewart PS,, Giussani B,, Roncoroni S,, Albanese D,, Giordano C,, Tunesi M,, Cappitelli F . 2011. Efficacy of zosteric acid sodium salt on the yeast biofilm model Candida albicans . Microb Ecol 62 : 584– 598.[PubMed] [CrossRef]
143. Basso FG,, Oliveira CF,, Fontana A,, Kurachi C,, Bagnato VS,, Spolidorio DM,, Hebling J,, de Souza Costa CA . 2011. In vitro effect of low-level laser therapy on typical oral microbial biofilms. Braz Dent J 22 : 502– 510.[PubMed] [CrossRef]
144. Chabrier-Rosello Y,, Foster TH,, Perez-Nazario N,, Mitra S,, Haidaris CG . 2005. Sensitivity of Candida albicans germ tubes and biofilms to photofrin-mediated phototoxicity. Antimicrob Agents Chemother 49 : 4288– 4295.[PubMed] [CrossRef]
145. Lopes M,, Alves CT,, Rama Raju B,, Goncalves MS,, Coutinho PJ,, Henriques M,, Belo I . 2014. Application of benzo[a]phenoxazinium chlorides in antimicrobial photodynamic therapy of Candida albicans biofilms. J Photochem Photobiol B 141 : 93– 99.[PubMed] [CrossRef]
146. Machado-de-Sena RM,, Correa L,, Kato IT,, Prates RA,, Senna AM,, Santos CC,, Picanco DA,, Ribeiro MS . 2014. Photodynamic therapy has antifungal effect and reduces inflammatory signals in Candida albicans-induced murine vaginitis. Photodiagnosis Photodyn Ther 11 : 275– 282.[PubMed] [CrossRef]
147. Rossoni RD,, Barbosa JO,, de Oliveira FE,, de Oliveira LD,, Jorge AO,, Junqueira JC . 2014. Biofilms of Candida albicans serotypes A and B differ in their sensitivity to photodynamic therapy. Lasers Med Sci 29 : 1679– 1684.[PubMed] [CrossRef]
148. Farber BF,, Wolff AG . 1993. Salicylic acid prevents the adherence of bacteria and yeast to silastic catheters. J Biomed Mater Res 27 : 599– 602.[PubMed] [CrossRef]
149. Maki DG,, Stolz SM,, Wheeler S,, Mermel LA . 1997. Prevention of central venous catheter-related bloodstream infection by use of an antiseptic-impregnated catheter. A randomized, controlled trial. Ann Intern Med 127 : 257– 266.[CrossRef]
150. Raad I,, Darouiche R,, Hachem R,, Sacilowski M,, Bodey GP . 1995. Antibiotics and prevention of microbial colonization of catheters. Antimicrob Agents Chemother 39 : 2397– 2400.[PubMed] [CrossRef]
151. Zhou L,, Tong Z,, Wu G,, Feng Z,, Bai S,, Dong Y,, Ni L,, Zhao Y . 2010. Parylene coating hinders Candida albicans adhesion to silicone elastomers and denture bases resin. Arch Oral Biol 55 : 401– 409.[PubMed] [CrossRef]
152. 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]
153. Mateus C,, Crow SA Jr,, Ahearn DG . 2004. Adherence of Candida albicans to silicone induces immediate enhanced tolerance to fluconazole. Antimicrob Agents Chemother 48 : 3358– 3366.[PubMed] [CrossRef]
154. Chandra J,, Mukherjee PK,, Mohamed S,, Schinabeck MK,, Ghannoum MA . 2003. Role of antifungal binding in fluconazole resistance of Candida albicans biofilms. Presented at the 43rd ICAAC; Abstract number PMArchive.
155. Beauvais A,, Latgé J-P, . 2015. Aspergillus biofilm in vitro and in vivo . In Ghannoum M,, Parsek M,, Whiteley M,, Mukherjee P (ed), Microbial Biofilms. 2nd ed. ASM Press, Washington, DC, in press.
156. Nett JE,, Andes DR, . 2015. Fungal biofilms: in vivo models for discovery of anti-biofilm drugs. In Ghannoum M,, Parsek M,, Whiteley M,, Mukherjee P (ed), Microbial Biofilms. 2nd ed. ASM Press, Washington, DC, in press.
157. Desai JV,, Mitchell AP, . 2015. Candida albicans biofilm development and its genetic control. In Ghannoum M,, Parsek M,, Whiteley M,, Mukherjee P (ed), Microbial Biofilms. 2nd ed. ASM Press, Washington, DC, in press. [CrossRef]

Tables

Candida Biofilms: Development, Architecture, and Resistance
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Citation: Chandra J, Mukherjee P. 2015. Biofilms: Development, Architecture, and Resistance, p 115-134. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0020-2015
/content/10.1128/9781555817466.chap6.tab6-1
TABLE 1
Summary of -associated biofilm models
Generic image for table
TABLE 1

Summary of -associated biofilm models

Citation: Chandra J, Mukherjee P. 2015. Biofilms: Development, Architecture, and Resistance, p 115-134. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0020-2015
/content/10.1128/9781555817466.chap6.tab6-2
TABLE 2
Summary of -associated biofilm models
Generic image for table
TABLE 2

Summary of -associated biofilm models

Citation: Chandra J, Mukherjee P. 2015. Biofilms: Development, Architecture, and Resistance, p 115-134. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0020-2015

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