How biofilms evade host defenses

Microbiology Spectrum

Volumn 3, Issue 3, 2015, Pages

  Roilides, Emmanuel ^a   Simitsopoulou, Maria ^a   Katragkou, Aspasia ^a,b   Walsh, Thomas J ^b  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; ANTIINFECTIVE AGENT;

ANIMAL; BACTERIAL COUNT; BACTERIUM; BIOFILM; DRUG EFFECTS; FUNGUS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNE EVASION; IMMUNOLOGY; PATHOGENICITY;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIFUNGAL AGENTS; BACTERIA; BIOFILMS; COLONY COUNT, MICROBIAL; FUNGI; HUMANS; IMMUNE EVASION;

EID: 84959045766     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.MB-0012-2014     Document Type: Article

References (92)

1. Costerton JW, Geesey GG, Cheng KJ. 1978. How bacteria stick. Sci Am 238:86-95.
2. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu Rev Microbiol 49:711-745.
3. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
4. Donlan RM, Costerton JW. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167-193.
5. Mack D, Becker P, Chatterjee I, Dobinsky S, Knobloch JK, Peters G, Rohde H, Herrmann M. 2004. Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol 294:203-212.
6. Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J. 2009. Our current understanding of fungal biofilms. Crit Rev Microbiol 35:340-355.
7. Wei Q, Ma LZ. 2013. Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int J Mol Sci 14:20983-21005.
8. Palkova Z, Vachova L. 2006. Life within a community: benefit to yeast long-term survival. FEMS Microbiol Rev 30:806-824.
9. Donlan RM. 2001. Biofilms and device-associated infections. Emerg Infect Dis 7:277-281.
10. Salta M, Wharton JA, Blache Y, Stokes KR, Briand JF. 2013. Marine biofilms on artificial surfaces: structure and dynamics. Environ Microbiol. [Epub ahead of print.] doi:10.1111/1462-2920.12186.
11. Abdallah M, Benoliel C, Drider D, Dhulster P, Chihib NE. 2014. Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Arch Microbiol. [Epub ahead of print.] doi:10.1007/s00203-014-0983-1.
12. Otto M. 2008. Staphylococcal biofilms. Curr Top Microbiol Immunol 322:207-228.
13. Fey PD, Olson ME. 2010. Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol 5:917-933.
14. Moorthy S, Watnick PI. 2004. Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Mol Microbiol 52:573-587.
15. Caiazza NC, Merritt JH, Brothers KM, O'Toole GA. 2007. Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189:3603-3612.
16. Walsh TJ, Schlegel R, Moody M, Costerton JW, Salcman M. 1986. Ventriculo-atrial shunt infection due to Cryptococcus neoformans: an ultrastructural and quantitative microbiological study. Neurosurgery 18: 373-375.
17. Martinez LR, Casadevall A. 2005. Specific antibody can prevent fungal biofilm formation and this effect correlates with protective efficacy. Infect Immun 73:6350-6362.
18. Zhao X, Oh SH, Yeater KM, Hoyer LL. 2005. Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function within the Als family. Microbiology 151:1619-1630.
19. Castano I, Pan SJ, Zupancic M, Hennequin C, Dujon B, Cormack BP. 2005. Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol Microbiol 55:1246-1258.
20. 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.
21. Davey ME, Caiazza NC, O'Toole GA. 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027-1036.
22. Rajendran R, Williams C, Lappin DF, Millington O, Martins M, Ramage G. 2013. Extracellular DNA release acts as an antifungal resistance mechanism in mature Aspergillus fumigatus biofilms. Eukaryot Cell 12:420-429.
23. Shopova I, Bruns S, Thywissen A, Kniemeyer O, Brakhage AA, Hillmann F. 2013. Extrinsic extracellular DNA leads to biofilm formation and colocalizes with matrix polysaccharides in the human pathogenic fungus Aspergillus fumigatus. Front Microbiol 4:141.
24. Krappmann S, Ramage G. 2013. A sticky situation: extracellular DNA shapes Aspergillus fumigatus biofilms. Front Microbiol 4:159.
25. 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. doi:10.1371/journal.ppat.1000828.
26. Wang R, Khan BA, Cheung GY, Bach TH, Jameson-LeeM, Kong KF, Queck SY, Otto M. 2011. Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. J Clin Invest 121:238-248.
27. Periasamy S, Joo HS, Duong AC, Bach TH, Tan VY, Chatterjee SS, Cheung GY, Otto M. 2012. How Staphylococcus aureus biofilms develop their characteristic structure. Proc Natl Acad Sci USA 109:1281-1286.
28. Harriott MM, Noverr MC. 2009. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 53:3914-3922.
29. Demuyser L, Jabra-Rizk MA, Van Dijck P. 2014. Microbial cell surface proteins and secreted metabolites involved in multispecies biofilms. Pathog Dis 70:219-230.
30. ShirtliffME, Peters BM, Jabra-Rizk MA. 2009. Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett 299:1-8.
31. Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW, ShirtliffME. 2010. Microbial interactions and differential protein expression in Staphylococcus aureus-Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol 59:493-503.
32. Wolcott R, Costerton JW, Raoult D, Cutler SJ. 2013. The polymicrobial nature of biofilm infection. Clin Microbiol Infect 19:107-112.
33. Mowat E, Rajendran R, Williams C, McCulloch E, Jones B, Lang S, Ramage G. 2010. Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation. FEMS Microbiol Lett 313:96-102.
34. Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF, Melton DM, Beachey EH. 1985. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22:996-1006.
35. 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.
36. Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M. 2011. Evaluation of different detection methods of biofilm formation in the clinical isolates. Braz J Infect Dis 15:305-311.
37. TaffHT, Nett JE, Andes DR. 2012. Comparative analysis of Candida biofilm quantitation assays. Med Mycol 50:214-218. 38.Mowat E, Butcher J, Lang S, Williams C, RamageG. 2007. Development of a simple model for studying the effects of antifungal agents on multicellular communities of Aspergillus fumigatus. JMed Microbiol 56:1205-1212.
38. Mowat E, Butcher J, Lang S, Williams C, RamageG. 2007. Development of a simple model for studying the effects of antifungal agents on multicellular communities of Aspergillus fumigatus. JMed Microbiol 56:1205-1212
39. Sontakke S, Cadenas MB, Maggi RG, Diniz PP, Breitschwerdt EB. 2009. Use of broad range 16S rDNA PCR in clinical microbiology. J Microbiol Methods 76:217-225.
40. Pontes DS, Lima-Bittencourt CI, Chartone-Souza E, AmaralNascimento AM. 2007. Molecular approaches: advantages and artifacts in assessing bacterial diversity. J Ind Microbiol Biotechnol 34:463-473.
41. Rhoads DD, Wolcott RD, Sun Y, Dowd SE. 2012. Comparison of culture and molecular identification of bacteria in chronic wounds. Int J Mol Sci 13:2535-2550.
42. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K. 2000. Immunobiology of dendritic cells. Annu Rev Immunol 18:767-811.
43. Gantner BN, Simmons RM, Canavera SJ, Akira S, Underhill DM. 2003. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med 197:1107-1117.
44. Romani L. 2011. Immunity to fungal infections. Nat Rev Immunol 11:275-288.
45. Norrby-Teglund A, Johansson L. 2013. Beyond the traditional immune response: bacterial interaction with phagocytic cells. Int J Antimicrob Agents 42(Suppl):S13-S16.
46. Singh PK, Parsek MR, Greenberg EP, Welsh MJ. 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417: 552-555.
47. Overhage J, Campisano A, Bains M, Torfs EC, Rehm BH, Hancock RE. 2008. Human host defense peptide LL-37 prevents bacterial biofilm formation. Infect Immun 76:4176-4182.
48. Britigan BE, Hayek MB, Doebbeling BN, Fick RB Jr. 1993. Transferrin and lactoferrin undergo proteolytic cleavage in the Pseudomonas aeruginosa-infected lungs of patients with cystic fibrosis. Infect Immun 61:5049-5055.
49. Schmidtchen A, Frick IM, Andersson E, Tapper H, Bjorck L. 2002. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol Microbiol 46:157-168.
50. Jensen PO, Givskov M, Bjarnsholt T, Moser C. 2010. The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol Med Microbiol 59:292-305.
51. Meyle E, Stroh P, Gunther F, Hoppy-Tichy T, Wagner C, Hansch GM. 2010. Destruction of bacterial biofilms by polymorphonuclear neutrophils: relative contribution of phagocytosis, DNA release, and degranulation. Int J Artif Organs 33:608-620.
52. Gunther F, Wabnitz GH, Stroh P, Prior B, Obst U, Samstag Y, Wagner C, Hansch GM. 2009. Host defense against Staphylococcus aureus biofilms infection: phagocytosis of biofilms by polymorphonuclear neutrophils (PMN). Mol Immunol 46:1805-1813.
53. Meyle E, Brenner-Weiss G, Obst U, Prior B, Hansch GM. 2012. Immune defense against S. epidermidis biofilms: components of the extracellular polymeric substance activate distinct bactericidal mechanisms of phagocytic cells. Int J Artif Organs 35:700-712.
54. Chandra J, McCormick TS, Imamura Y, Mukherjee PK, Ghannoum MA. 2007. Interaction of Candida albicans with adherent human peripheral blood mononuclear cells increases C. albicans biofilm formation and results in differential expression of pro-and anti-inflammatory cytokines. Infect Immun 75:2612-2620.
55. Katragkou A, Kruhlak MJ, Simitsopoulou M, Chatzimoschou A, Taparkou A, Cotten CJ, Paliogianni F, Diza-Mataftsi E, Tsantali C, Walsh TJ, Roilides E. 2010. Interactions between human phagocytes and Candida albicans biofilms alone and in combination with antifungal agents. J Infect Dis 201:1941-1949.
56. Martinez LR, Casadevall A. 2006. Cryptococcus neoformans cells in biofilms are less susceptible than planktonic cells to antimicrobial molecules produced by the innate immune system. Infect Immun 74: 6118-6123.
57. Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, ShirtliffME. 2011. Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence 2:445-459.
58. Leid JG, ShirtliffME, Costerton JW, Stoodley P. 2002. Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect Immun 70:6339-6345.
59. Guenther F, Stroh P, Wagner C, Obst U, Hansch GM. 2009. Phagocytosis of staphylococci biofilms by polymorphonuclear neutrophils: S. aureus and S. epidermidis differ with regard to their susceptibility towards the host defense. Int J Artif Organs 32:565-573.
60. Thurlow LR, Hanke ML, Fritz T, Angle A, Aldrich A, Williams SH, Engebretsen IL, Bayles KW, Horswill AR, Kielian T. 2011. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J Immunol 186:6585-6596.
61. Stroh P, Gunther F, Meyle E, Prior B, Wagner C, Hansch GM. 2011. Host defense against Staphylococcus aureus biofilms by polymorphonuclear neutrophils: oxygen radical production but not phagocytosis depends on opsonisation with immunoglobulin G. Immunobiology 216:351-357.
62. Cerca N, Jefferson KK, Oliveira R, Pier GB, Azeredo J. 2006. Comparative antibody-mediated phagocytosis of Staphylococcus epidermidis cells grown in a biofilm or in the planktonic state. Infect Immun 74:4849-4855.
63. Hanke ML, Kielian T. 2012. Deciphering mechanisms of staphylococcal biofilm evasion of host immunity. Front Cell Infect Microbiol 2:62.
64. Hanke ML, Heim CE, Angle A, Sanderson SD, Kielian T. 2013. Targeting macrophage activation for the prevention and treatment of Staphylococcus aureus biofilm infections. J Immunol 190:2159-2168.
65. Alhede M, Bjarnsholt T, Givskov M, Alhede M. 2014. Pseudomonas aeruginosa biofilms: mechanisms of immune evasion. Adv Appl Microbiol 86:1-40.
66. Jensen ET, Kharazmi A, Lam K, Costerton JW, Hoiby N. 1990. Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms. Infect Immun 58:2383-2385.
67. Jesaitis AJ, Franklin MJ, Berglund D, Sasaki M, Lord CI, Bleazard JB, Duffy JE, Beyenal H, Lewandowski Z. 2003. Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J Immunol 171:4329-4339.
68. Bjarnsholt T, Jensen PO, Burmolle M, Hentzer M, Haagensen JA, Hougen HP, Calum H, Madsen KG, Moser C, Molin S, Hoiby N, Givskov M. 2005. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:373-383.
69. Walker TS, Tomlin KL, Worthen GS, Poch KR, Lieber JG, Saavedra MT, Fessler MB, Malcolm KC, Vasil ML, Nick JA. 2005. Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils. Infect Immun 73:3693-3701.
70. Parks QM, Young RL, Poch KR, Malcolm KC, Vasil ML, Nick JA. 2009. Neutrophil enhancement of Pseudomonas aeruginosa biofilm development: human F-actin and DNA as targets for therapy. J Med Microbiol 58:492-502.
71. Watt AP, Courtney J, Moore J, Ennis M, Elborn JS. 2005. Neutrophil cell death, activation and bacterial infection in cystic fibrosis. Thorax 60:659-664.
72. Leid JG, Willson CJ, ShirtliffME, Hassett DJ, Parsek MR, Jeffers AK. 2005. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J Immunol 175:7512-7518.
73. Jensen ET, Kharazmi A, Hoiby N, Costerton JW. 1992. Some bacterial parameters influencing the neutrophil oxidative burst response to Pseudomonas aeruginosa biofilms. APMIS 100:727-733.
74. Jensen PO, Bjarnsholt T, Phipps R, Rasmussen TB, Calum H, Christoffersen L, Moser C, Williams P, Pressler T, Givskov M, Hoiby N. 2007. Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology 153:1329-1338.
75. Alhede M, Bjarnsholt T, Jensen PO, Phipps RK, Moser C, Christophersen L, Christensen LD, van Gennip M, Parsek M, Hoiby N, Rasmussen TB, Givskov M. 2009. Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiology 155:3500-3508.
76. Van Gennip M, Christensen LD, Alhede M, Phipps R, Jensen PO, Christophersen L, Pamp SJ, Moser C, Mikkelsen PJ, Koh AY, Tolker-Nielsen T, Pier GB, Hoiby N, Givskov M, Bjarnsholt T. 2009. Inactivation of the rhlA gene in Pseudomonas aeruginosa prevents rhamnolipid production, disabling the protection against polymorphonuclear leukocytes. APMIS 117:537-546.
77. Roilides E, Walsh T. 2004. Recombinant cytokines in augmentation and immunomodulation of host defenses against Candida spp. Med Mycol 42:1-13.
78. Xie Z, ThompsonA, Sobue T, Kashleva H, XuH, Vasilakos J, Dongari-Bagtzoglou A. 2012. Candida albicans biofilms do not trigger reactive oxygen species and evade neutrophil killing. J Infect Dis 206:1936-1945.
79. Katragkou A, Simitsopoulou M, Chatzimoschou A, Georgiadou E, Walsh TJ, Roilides E. 2011. Effects of interferon-gamma and granulocyte colony-stimulating factor on antifungal activity of human polymorphonuclear neutrophils against Candida albicans grown as biofilms or planktonic cells. Cytokine 55:330-334.
80. Nett J, Lincoln L, Marchillo K, Andes D. 2007. Beta-1, 3 glucan as a test for central venous catheter biofilm infection. J Infect Dis 195:1705-1712.
81. 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.
82. 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.
83. Luo G, Ibrahim AS, Spellberg B, Nobile CJ, Mitchell AP, Fu Y. 2010. Candida albicans Hyr1p confers resistance to neutrophil killing and is a potential vaccine target. J Infect Dis 201:1718-1728.
84. Giard JC, Riboulet E, Verneuil N, Sanguinetti M, Auffray Y, Hartke A. 2006. Characterization of Ers, a PrfA-like regulator of Enterococcus faecalis. FEMS Immunol Med Microbiol 46:410-418.
85. Gentry-Weeks CR, Karkhoff-Schweizer R, Pikis A, Estay M, Keith JM. 1999. Survival of Enterococcus faecalis in mouse peritoneal macrophages. Infect Immun 67:2160-2165.
86. Daw K, Baghdayan AS, Awasthi S, Shankar N. 2012. Biofilm and planktonic Enterococcus faecalis elicit different responses from host phagocytes in vitro. FEMS Immunol Med Microbiol 65:270-282.
87. Mathew S, Yaw-Chyn L, Kishen A. 2010. Immunogenic potential of Enterococcus faecalis biofilm under simulated growth conditions. J Endod 36:832-836.
88. Chotirmall SH, McElvaney NG. 2014. Fungi in the cystic fibrosis lung: bystanders or pathogens? Int J Biochem Cell Biol 52:161-173.
89. Roilides E, Simitsopoulou M. 2010. Local innate host response and filamentous fungi in patientswith cystic fibrosis. MedMycol 48(Suppl 1):S22-S31.
90. Tasina E, Simitsopoulou M, Roilides E. 2012. The innate immune response to filamentous fungi in patients with cystic fibrosis. CML Cystic Fibrosis 2:29-39.
91. Kreindler JL, Steele C, Nguyen N, Chan YR, Pilewski JM, Alcorn JF, Vyas YM, Aujla SJ, Finelli P, BlanchardM, Zeigler SF, Logar A, Hartigan E, Kurs-Lasky M, Rockette H, Ray A, Kolls JK. 2010. Vitamin D3 attenuates Th2 responses to Aspergillus fumigatus mounted by CD4+ T cells from cystic fibrosis patients with allergic bronchopulmonary aspergillosis. J Clin Invest 120:3242-3254.
92. Nett J, Andes D. 2006. Candida albicans biofilm development, modeling a host-pathogen interaction. Curr Opin Microbiol 9:340-345.