Host Responses to Biofilm

Progress in Molecular Biology and Translational Science

Volumn 142, Issue , 2016, Pages 193-239

  Watters, C ^a   Fleming, D ^b   Bishop, D ^a   Rumbaugh, K P ^b  

^a NAVAL MEDICAL RESEARCH CENTER   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

bacterial immune response; biofilms; EPS matrix; extracellular DNA; Lactobacillus biofilms; M2 macrophages; neutrophil lysis; probiotics; Pseudomonas aeruginosa; Staphylococcus aureus

Indexed keywords

BACTERIAL DNA; EXOPOLYSACCHARIDE; EXOPROTEIN; PROBIOTIC AGENT; PROTEIN; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; BIOFILM; CHRONIC INFLAMMATION; COMMENSAL; GUT IMMUNITY; HOST CELL; HUMAN; IMMUNE RESPONSE; IMMUNITY; MACROPHAGE; MEMBRANE VESICLE; MONOCYTE; NEUTROPHIL; NONHUMAN; OUTER MEMBRANE; SKIN IMMUNITY; VAGINAL IMMUNITY; ANIMAL; BIOLOGICAL MODEL; DRUG EFFECTS; HOST PATHOGEN INTERACTION; IMMUNE SYSTEM; IMMUNOLOGY; MICROBIOLOGY; SKIN;

ANIMALS; BIOFILMS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE SYSTEM; MODELS, BIOLOGICAL; PROBIOTICS; SKIN;

EID: 84994174604     PISSN: 18771173     EISSN: 18780814     Source Type: Book Series    
DOI: 10.1016/bs.pmbts.2016.05.007     Document Type: Chapter

References (211)

1. 1 Flemming, H.C., Wingender, J., The biofilm matrix. Nat Rev Microbiol 8:9 (2010), 623–633.
2. 2 Wingender, J., Strathmann, M., Rode, A., Leis, A., Flemming, H.C., Isolation and biochemical characterization of extracellular polymeric substances from Pseudomonas aeruginosa. Methods Enzymol 336 (2001), 302–314.
3. 3 Bales, P.M., Renke, E.M., May, S.L., Shen, Y., Nelson, D.C., Purification and characterization of biofilm-associated EPS exopolysaccharides from ESKAPE organisms and other pathogens. PLoS One, 8(6), 2013, e67950.
4. 4 Limoli, D.H., Jones, C.J., Wozniak, D.J., Bacterial extracellular polysaccharides in biofilm formation and function. Microbiol Spectr, 3(3), 2015.
5. 5 Murofushi, Y., Villena, J., Morie, K., et al. The toll-like receptor family protein RP105/MD1 complex is involved in the immunoregulatory effect of exopolysaccharides from Lactobacillus plantarum N14. Mol Immunol 64:1 (2015), 63–75.
6. 6 Raffatellu, M., Chessa, D., Wilson, R.P., Dusold, R., Rubino, S., Baumler, A.J., The Vi capsular antigen of Salmonella enterica serotype Typhi reduces Toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect Immun 73:6 (2005), 3367–3374.
7. 7 Bylund, J., Burgess, L.A., Cescutti, P., Ernst, R.K., Speert, D.P., Exopolysaccharides from Burkholderia cenocepacia inhibit neutrophil chemotaxis and scavenge reactive oxygen species. J Biol Chem 281:5 (2006), 2526–2532.
8. 8 Pier, G.B., Coleman, F., Grout, M., Franklin, M., Ohman, D.E., Role of alginate O acetylation in resistance of mucoid Pseudomonas aeruginosa to opsonic phagocytosis. Infect Immun 69:3 (2001), 1895–1901.
9. 9 Leid, J.G., Willson, C.J., Shirtliff, M.E., Hassett, D.J., Parsek, M.R., Jeffers, A.K., The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J Immunol 175:11 (2005), 7512–7518.
10. 10 Aslam, S.N., Newman, M.A., Erbs, G., et al. Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Curr Biol 18:14 (2008), 1078–1083.
11. 11 Lin, M.H., Yang, Y.L., Chen, Y.P., et al. A novel exopolysaccharide from the biofilm of Thermus aquaticus YT-1 induces the immune response through Toll-like receptor 2. J Biol Chem 286:20 (2011), 17736–17745.
12. 12 Graveline, R., Segura, M., Radzioch, D., Gottschalk, M., TLR2-dependent recognition of Streptococcus suis is modulated by the presence of capsular polysaccharide which modifies macrophage responsiveness. Int Immunol 19:4 (2007), 375–389.
13. 13 Zhao, G., Usui, M.L., Lippman, S.I., et al. Biofilms and inflammation in chronic wounds. Adv Wound Care 2:7 (2013), 389–399.
14. 14 Attinger, C., Wolcott, R., Clinically Addressing Biofilm in Chronic Wounds. Adv Wound Care 1:3 (2012), 127–132.
15. 15 Lovewell, R.R., Patankar, Y.R., Berwin, B., Mechanisms of phagocytosis and host clearance of Pseudomonas aeruginosa. Am J Physiol Lung Cell Mol Physiol 306:7 (2014), L591–L603.
16. 16 Mishra, M., Byrd, M.S., Sergeant, S., et al. Pseudomonas aeruginosa Psl polysaccharide reduces neutrophil phagocytosis and the oxidative response by limiting complement-mediated opsonization. Cellular Microbiol 14:1 (2012), 95–106.
17. 17 Okshevsky, M., Meyer, R.L., The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit Rev Microbiol 41:3 (2015), 341–352.
18. 18 Das, T., Sehar, S., Manefield, M., The roles of extracellular DNA in the structural integrity of extracellular polymeric substance and bacterial biofilm development. Environ Microbiol Rep 5:6 (2013), 778–786.
19. 19 Jakubovics, N.S., Shields, R.C., Rajarajan, N., Burgess, J.G., Life after death: the critical role of extracellular DNA in microbial biofilms. Lett Appl Microbiol 57:6 (2013), 467–475.
20. 20 Whitchurch, C.B., Tolker-Nielsen, T., Ragas, P.C., Mattick, J.S., Extracellular DNA required for bacterial biofilm formation. Science., 295(5559), 2002, 1487.
21. 21 Alhede, M., Bjarnsholt, T., Givskov, M., Alhede, M., Pseudomonas aeruginosa biofilms: mechanisms of immune evasion. Adv Appl Microbiol 86 (2014), 1–40.
22. 22 Krieg, A.M., CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 20 (2002), 709–760.
23. 23 Krieg, A.M., Wagner, H., Causing a commotion in the blood: immunotherapy progresses from bacteria to bacterial DNA. Immunol Today 21:10 (2000), 521–526.
24. 24 Krieg, A.M., Yi, A.K., Matson, S., et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374:6522 (1995), 546–549.
25. 25 Trevani, A.S., Chorny, A., Salamone, G., et al. Bacterial DNA activates human neutrophils by a CpG-independent pathway. Eu J Immunol 33:11 (2003), 3164–3174.
26. 26 Jensen, P.O., Bjarnsholt, T., Phipps, R., et al. Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology 153:Pt 5 (2007), 1329–1338.
27. 27 Bjarnsholt, T., Jensen, P.O., Fiandaca, M.J., et al. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr Pulmonol 44:6 (2009), 547–558.
28. 28 Fuxman Bass, J.I., Russo, D.M., Gabelloni, M.L., et al. Extracellular DNA: a major proinflammatory component of Pseudomonas aeruginosa biofilms. J Immunol 184:11 (2010), 6386–6395.
29. 29 Mulcahy, H., Charron-Mazenod, L., Lewenza, S., Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog, 4(11), 2008, e1000213.
30. 30 Brinkmann, V., Reichard, U., Goosmann, C., et al. Neutrophil extracellular traps kill bacteria. Science 303:5663 (2004), 1532–1535.
31. 31 Jiao, Y., Cody, G.D., Harding, A.K., et al. Characterization of extracellular polymeric substances from acidophilic microbial biofilms. Appl Environ Microbiol 76:9 (2010), 2916–2922.
32. 32 Lasa, I., Penades, J.R., Bap: a family of surface proteins involved in biofilm formation. Res Microbiol 157:2 (2006), 99–107.
33. 33 Speziale, P., Pietrocola, G., Foster, T.J., Geoghegan, J.A., Protein-based biofilm matrices in Staphylococci. Front Cell Infect Microbiol, 4, 2014, 171.
34. 34 Muthukrishnan, G., Quinn, G.A., Lamers, R.P., et al. Exoproteome of Staphylococcus aureus reveals putative determinants of nasal carriage. J Proteome Res 10:4 (2011), 2064–2078.
35. 35 Zhang, X., Bishop, P.L., Biodegradability of biofilm extracellular polymeric substances. Chemosphere 50:1 (2003), 63–69.
36. 36 Kaplan, J.B., Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J Dent Res 89:3 (2010), 205–218.
37. 37 Goodman, S.D., Obergfell, K.P., Jurcisek, J.A., et al. Biofilms can be dispersed by focusing the immune system on a common family of bacterial nucleoid-associated proteins. Mucosal Immunol 4:6 (2011), 625–637.
38. 38 Borlee, B.R., Goldman, A.D., Murakami, K., Samudrala, R., Wozniak, D.J., Parsek, M.R., Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75:4 (2010), 827–842.
39. 39 Passmore, I.J., Nishikawa, K., Lilley, K.S., Bowden, S.D., Chung, J.C., Welch, M., Mep72, a metzincin protease that is preferentially secreted by biofilms of Pseudomonas aeruginosa. J Bacteriol 197:4 (2015), 762–773.
40. 40 Lourenco, A., de Las Heras, A., Scortti, M., Vazquez-Boland, J., Frank, J.F., Brito, L., Comparison of Listeria monocytogenes Exoproteomes from biofilm and planktonic state: Lmo2504, a protein associated with biofilms. Appl Environ Microbiol 79:19 (2013), 6075–6082.
41. 41 Dharmaprakash, A., Mutt, E., Jaleel, A., Ramanathan, S., Thomas, S., Proteome profile of a pandemic Vibrio parahaemolyticus SC192 strain in the planktonic and biofilm condition. Biofouling 30:6 (2014), 729–739.
42. 42 Carvalhais, V., Cerveira, F., Vilanova, M., Cerca, N., Vitorino, R., An immunoproteomic approach for characterization of dormancy within Staphylococcus epidermidis biofilms. Mol Immunol 65:2 (2015), 429–435.
43. 43 Yi, L., Wang, Y., Ma, Z., et al. Biofilm formation of Streptococcus equi ssp. zooepidemicus and comparative proteomic analysis of biofilm and planktonic cells. Curr Microbiol 69:3 (2014), 227–233.
44. 44 Zijnge, V., Kieselbach, T., Oscarsson, J., Proteomics of protein secretion by Aggregatibacter actinomycetemcomitans. PLoS One, 7(7), 2012, e41662.
45. 45 Panaro, M.A., Acquafredda, A., Sisto, M., Lisi, S., Maffione, A.B., Mitolo, V., Biological role of the N-formyl peptide receptors. Immunopharmacol Immunotoxicol 28:1 (2006), 103–127.
46. 46 He, H.Q., Troksa, E.L., Caltabiano, G., Pardo, L., Ye, R.D., Structural determinants for the interaction of formyl peptide receptor 2 with peptide ligands. J Biol Chem 289:4 (2014), 2295–2306.
47. 47 Schiffmann, E., Corcoran, B.A., Wahl, S.M., N-formylmethionyl peptides as chemoattractants for leucocytes. Proc Natl Acad Sci USA 72:3 (1975), 1059–1062.
48. 48 Nauseef, W.M., How human neutrophils kill and degrade microbes: an integrated view. Immunol Rev 219 (2007), 88–102.
49. 49 Zhang, Q., Raoof, M., Chen, Y., et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464:7285 (2010), 104–107.
50. 50 Takeda, K., Akira, S., Toll-like receptors in innate immunity. Int Immunol 17:1 (2005), 1–14.
51. 51 Brady, R.A., Leid, J.G., Camper, A.K., Costerton, J.W., Shirtliff, M.E., Identification of Staphylococcus aureus proteins recognized by the antibody-mediated immune response to a biofilm infection. Infect Immun 74:6 (2006), 3415–3426.
52. 52 Enany, S., Yoshida, Y., Magdeldin, S., et al. Two dimensional electrophoresis of the exo-proteome produced from community acquired methicillin resistant Staphylococcus aureus belonging to clonal complex 80. Microbiol Res 168:8 (2013), 504–511.
53. 53 Gil, C., Solano, C., Burgui, S., et al. Biofilm matrix exoproteins induce a protective immune response against Staphylococcus aureus biofilm infection. Infect Immun 82:3 (2014), 1017–1029.
54. 54 Sadowska, B., Wieckowska-Szakiel, M., Paszkiewicz, M., Rozalska, B., The immunomodulatory activity of Staphylococcus aureus products derived from biofilm and planktonic cultures. Arch Immunol Ther Exp 61:5 (2013), 413–420.
55. 55 Sanui, T., Gregory, R.L., Analysis of Streptococcus mutans biofilm proteins recognized by salivary immunoglobulin A. Oral Microbiol Immunol 24:5 (2009), 361–368.
56. 56 Purschke, F.G., Hiller, E., Trick, I., Rupp, S., Flexible survival strategies of Pseudomonas aeruginosa in biofilms result in increased fitness compared with Candida albicans. Mol Cell Proteomics 11:12 (2012), 1652–1669.
57. 57 Bostanci, N., Bao, K., Wahlander, A., Grossmann, J., Thurnheer, T., Belibasakis, G.N., Secretome of gingival epithelium in response to subgingival biofilms. Mol Oral Microbiol 30:4 (2015), 323–335.
58. 58 Schooling, S.R., Beveridge, T.J., Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188:16 (2006), 5945–5957.
59. 59 Couto, N., Schooling, S.R., Dutcher, J.R., Barber, J., Proteome profiles of outer membrane vesicles and extracellular matrix of Pseudomonas aeruginosa biofilms. J Proteome Res 14:10 (2015), 4207–4222.
60. 60 Ellis, T.N., Leiman, S.A., Kuehn, M.J., Naturally produced outer membrane vesicles from Pseudomonas aeruginosa elicit a potent innate immune response via combined sensing of both lipopolysaccharide and protein components. Infect Immun 78:9 (2010), 3822–3831.
61. 61 Kulp, A., Kuehn, M.J., Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64 (2010), 163–184.
62. 62 Toyofuku, M., Roschitzki, B., Riedel, K., Eberl, L., Identification of proteins associated with the Pseudomonas aeruginosa biofilm extracellular matrix. J Proteome Res 11:10 (2012), 4906–4915.
63. 63 Ng, W.L., Bassler, B.L., Bacterial quorum-sensing network architectures. Annu Rev Genet 43 (2009), 197–222.
64. 64 Everett JA, Rumbaugh KP. Biofilms, Quorum Sensing and Crosstalk in Medically Important Microbes. In: Elsevier; 2015:235–247. Molecular Medical Microbiology; vol. 1.
65. 65 Rumbaugh, K.P., Kaufmann, G.F., Exploitation of host signaling pathways by microbial quorum sensing signals. Curr Opin Microbiol 15:2 (2012), 162–168.
66. 66 Lowery, C.A., Dickerson, T.J., Janda, K.D., Interspecies and interkingdom communication mediated by bacterial quorum sensing. Chem Soc Rev 37:7 (2008), 1337–1346.
67. 67 Massion, P.P., Inoue, H., Richman-Eisenstat, J., et al. Novel Pseudomonas product stimulates interleukin-8 production in airway epithelial cells in vitro. J Clin Invest 93:1 (1994), 26–32.
68. 68 Smith, R.S., Fedyk, E.R., Springer, T.A., Mukaida, N., Iglewski, B.H., Phipps, R.P., IL-8 production in human lung fibroblasts and epithelial cells activated by the Pseudomonas autoinducer N-3-oxododecanoyl homoserine lactone is transcriptionally regulated by NF-kappa B and activator protein-2. J Immunol 167:1 (2001), 366–374.
69. 69 Shiner, E.K., Terentyev, D., Bryan, A., et al. Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling. Cell Microbiol 8:10 (2006), 1601–1610.
70. 70 Tateda, K., Ishii, Y., Horikawa, M., et al. The Pseudomonas aeruginosa autoinducer N-3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect Immun 71:10 (2003), 5785–5793.
71. 71 Schwarzer, C., Wong, S., Shi, J., et al. Pseudomonas aeruginosa Homoserine lactone activates store-operated cAMP and cystic fibrosis transmembrane regulator-dependent Cl- secretion by human airway epithelia. J Biol Chem 285:45 (2010), 34850–34863.
72. 72 Holban, A.M., Bleotu, C., Chifiriuc, M.C., Bezirtzoglou, E., Lazar, V., Role of Pseudomonas aeruginosa quorum sensing (QS) molecules on the viability and cytokine profile of human mesenchymal stem cells. Virulence 5:2 (2014), 303–310.
73. 73 Li, H., Wang, L., Ye, L., et al. Influence of Pseudomonas aeruginosa quorum sensing signal molecule N-(3-oxododecanoyl) homoserine lactone on mast cells. Med Microbiol Immunol 198:2 (2009), 113–121.
74. 74 Jacobi, C.A., Schiffner, F., Henkel, M., et al. Effects of bacterial N-acyl homoserine lactones on human Jurkat T lymphocytes-OdDHL induces apoptosis via the mitochondrial pathway. Int J Med Microbiol 299:7 (2009), 509–519.
75. 75 Kravchenko, V.V., Kaufmann, G.F., Mathison, J.C., et al. N-(3-Oxo-acyl)homoserine lactones signal cell activation through a mechanism distinct from the canonical pathogen-associated molecular pattern recognition receptor pathways. J Biol Chem 281:39 (2006), 28822–28830.
76. 76 Sperandio, V., Torres, A.G., Jarvis, B., Nataro, J.P., Kaper, J.B., Bacteria-host communication: the language of hormones. Proc Natl Acad Sci USA 100:15 (2003), 8951–8956.
77. 77 Lyte, M., Microbial endocrinology and infectious disease in the 21st century. Trends Microbiol 12:1 (2004), 14–20.
78. 78 Shiner, E.K., Rumbaugh, K.P., Williams, S.C., Interkingdom signaling: deciphering the language of acyl homoserine lactones. FEMS Microbiol Rev 29:5 (2005), 935–947.
79. 79 Rumbaugh, K.P., Convergence of hormones and autoinducers at the host/pathogen interface. Anal Bioanal Chem 387:2 (2007), 425–435.
80. 80 Jahoor, A., Patel, R., Bryan, A., et al. Peroxisome proliferator-activated receptors mediate host cell proinflammatory responses to Pseudomonas aeruginosa autoinducer. J Bacteriol 190:13 (2008), 4408–4415.
81. 81 Cooley, M.A., Whittall, C., Rolph, M.S., Pseudomonas signal molecule 3-oxo-C12-homoserine lactone interferes with binding of rosiglitazone to human PPARgamma. Microbes Infect 12:3 (2010), 231–237.
82. 82 Lee, R.J., Xiong, G., Kofonow, J.M., et al. T2R38 taste receptor polymorphisms underlie susceptibility to upper respiratory infection. J Clin Invest 122:11 (2012), 4145–4159.
83. 83 Karlsson, T., Musse, F., Magnusson, K.E., Vikstrom, E., N-Acylhomoserine lactones are potent neutrophil chemoattractants that act via calcium mobilization and actin remodeling. J Leukoc Biol 91:1 (2012), 15–26.
84. 84 Romling, U., Galperin, M.Y., Gomelsky, M., Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1 (2013), 1–52.
85. 85 Jenal, U., Malone, J., Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40 (2006), 385–407.
86. 86 Romling, U., Cyclic di-GMP, an established secondary messenger still speeding up. Environ Microbiol 14:8 (2012), 1817–1829.
87. 87 Commichau, F.M., Dickmanns, A., Gundlach, J., Ficner, R., Stulke, J., A jack of all trades: the multiple roles of the unique essential second messenger cyclic di-AMP. Mol Microbiol 97:2 (2015), 189–204.
88. 88 Valle, J., Solano, C., Garcia, B., Toledo-Arana, A., Lasa, I., Biofilm switch and immune response determinants at early stages of infection. Trends Microbiol 21:8 (2013), 364–371.
89. 89 McWhirter, S.M., Barbalat, R., Monroe, K.M., et al. A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J Exp Med 206:9 (2009), 1899–1911.
90. 90 Woodward, J.J., Iavarone, A.T., Portnoy, D.A., c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328:5986 (2010), 1703–1705.
91. 91 Jayaseelan, S., Ramaswamy, D., Dharmaraj, S., Pyocyanin: production, applications, challenges and new insights. World J Microbiol Biotechnol 30:4 (2014), 1159–1168.
92. 92 Manago, A., Becker, K.A., Carpinteiro, A., et al. Pseudomonas aeruginosa pyocyanin induces neutrophil death via mitochondrial reactive oxygen species and mitochondrial acid sphingomyelinase. Antioxid Redox Signal 22:13 (2015), 1097–1110.
93. 93 Das, T., Manefield, M., Pyocyanin promotes extracellular DNA release in Pseudomonas aeruginosa. PLoS One, 7(10), 2012, e46718.
94. 94 Das, T., Kutty, S.K., Kumar, N., Manefield, M., Pyocyanin facilitates extracellular DNA binding to Pseudomonas aeruginosa influencing cell surface properties and aggregation. PLoS One, 8(3), 2013, e58299.
95. 95 Rada, B., Jendrysik, M.A., Pang, L., et al. Pyocyanin-enhanced neutrophil extracellular trap formation requires the NADPH oxidase. PLoS One, 8(1), 2013, e54205.
96. 96 Logters, T., Margraf, S., Altrichter, J., et al. The clinical value of neutrophil extracellular traps. Med Microbiol Immunol 198:4 (2009), 211–219.
97. 97 Garcia-Romo, G.S., Caielli, S., Vega, B., et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med, 3(73), 2011, 73ra20.
98. 98 Manzenreiter, R., Kienberger, F., Marcos, V., et al. Ultrastructural characterization of cystic fibrosis sputum using atomic force and scanning electron microscopy. J Cyst Fibros 11:2 (2012), 84–92.
99. 99 Fothergill, J.L., Panagea, S., Hart, C.A., Walshaw, M.J., Pitt, T.L., Winstanley, C., Widespread pyocyanin over-production among isolates of a cystic fibrosis epidemic strain. BMC Microbiol, 7, 2007, 45.
100. 100 Lau, G.W., Hassett, D.J., Ran, H., Kong, F., The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10:12 (2004), 599–606.
101. 101 Dowd, S.E., Wolcott, R.D., Sun, Y., McKeehan, T., Smith, E., Rhoads, D., Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One, 3(10), 2008, e3326.
102. 102 Wolcott, R.D., Hanson, J.D., Rees, E.J., et al. Analysis of the chronic wound microbiota of 2,963 patients by 16S rDNA pyrosequencing. Wound Repair Regen, 2015.
103. 103 Rumbaugh, K.P., Diggle, S.P., Watters, C.M., Ross-Gillespie, A., Griffin, A.S., West, S.A., Quorum sensing and the social evolution of bacterial virulence. Curr Biol 19:4 (2009), 341–345.
104. 104 Gjodsbol, K., Christensen, J.J., Karlsmark, T., Jorgensen, B., Klein, B.M., Krogfelt, K.A., Multiple bacterial species reside in chronic wounds: a longitudinal study. Int Wound J 3:3 (2006), 225–231.
105. 105 Sun, Y., Dowd, S.E., Smith, E., Rhoads, D.D., Wolcott, R.D., In vitro multispecies Lubbock chronic wound biofilm model. Wound Repair Regen 16:6 (2008), 805–813.
106. 106 DeLeon, S., Clinton, A., Fowler, H., Everett, J., Horswill, A.R., Rumbaugh, K.P., Synergistic interactions of Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro wound model. Infect Immun 82:11 (2014), 4718–4728.
107. 107 Freudenberg, M.A., Tchaptchet, S., Keck, S., et al. Lipopolysaccharide sensing an important factor in the innate immune response to Gram-negative bacterial infections: benefits and hazards of LPS hypersensitivity. Immunobiology 213:3–4 (2008), 193–203.
108. 108 Summers, C., Rankin, S.M., Condliffe, A.M., Singh, N., Peters, A.M., Chilvers, E.R., Neutrophil kinetics in health and disease. Trends Immunol 31:8 (2010), 318–324.
109. 109 De Filippo, K., Dudeck, A., Hasenberg, M., et al. Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation. Blood 121:24 (2013), 4930–4937.
110. 110 Miyamoto, M., Prause, O., Sjostrand, M., Laan, M., Lotvall, J., Linden, A., Endogenous IL-17 as a mediator of neutrophil recruitment caused by endotoxin exposure in mouse airways. J Immunol 170:9 (2003), 4665–4672.
111. 111 Witko-Sarsat, V., Rieu, P., Descamps-Latscha, B., Lesavre, P., Halbwachs-Mecarelli, L., Neutrophils: molecules, functions and pathophysiological aspects. Lab Invest 80:5 (2000), 617–653.
112. 112 Amulic, B., Cazalet, C., Hayes, G.L., Metzler, K.D., Zychlinsky, A., Neutrophil function: from mechanisms to disease. Annu Rev Immunol 30 (2012), 459–489.
113. 113 van Kessel, K.P., Bestebroer, J., van Strijp, J.A., Neutrophil-mediated phagocytosis of Staphylococcus aureus. Front Immunol, 5, 2014, 467.
114. 114 Berger, M., Inflammation in the lung in cystic fibrosis. a vicious cycle that does more harm than good?. Clin Rev Allergy 9:1–2 (1991), 119–142.
115. 115 Cox, G., Crossley, J., Xing, Z., Macrophage engulfment of apoptotic neutrophils contributes to the resolution of acute pulmonary inflammation in vivo. Am J Resp Cell Mol Biol 12:2 (1995), 232–237.
116. 116 Gunther, F., Wabnitz, G.H., Stroh, P., et al. Host defence against Staphylococcus aureus biofilms infection: phagocytosis of biofilms by polymorphonuclear neutrophils (PMN). Mol Immunol 46:8–9 (2009), 1805–1813.
117. 117 Meyle, E., Stroh, P., Gunther, F., Hoppy-Tichy, T., Wagner, C., Hansch, G.M., Destruction of bacterial biofilms by polymorphonuclear neutrophils: relative contribution of phagocytosis, DNA release, and degranulation. The International journal of artificial organs 33:9 (2010), 608–620.
118. 118 Stroh, P., Gunther, F., Meyle, E., Prior, B., Wagner, C., Hansch, G.M., Host defence against Staphylococcus aureus biofilms by polymorphonuclear neutrophils: oxygen radical production but not phagocytosis depends on opsonisation with immunoglobulin G. Immunobiology 216:3 (2011), 351–357.
119. 119 Bernthal, N.M., Pribaz, J.R., Stavrakis, A.I., et al. Protective role of IL-1beta against post-arthroplasty Staphylococcus aureus infection. J Orthop Res 29:10 (2011), 1621–1626.
120. 120 Nguyen KT, Seth AK, Hong SJ, et al. Deficient cytokine expression and neutrophil oxidative burst contribute to impaired cutaneous wound healing in diabetic, biofilm-containing chronic wounds. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society; 2013;21(6):833–841.
121. 121 Hanses, F., Park, S., Rich, J., Lee, J.C., Reduced neutrophil apoptosis in diabetic mice during staphylococcal infection leads to prolonged Tnfalpha production and reduced neutrophil clearance. PloS One, 6(8), 2011, e23633.
122. 122 Kristian, S.A., Birkenstock, T.A., Sauder, U., Mack, D., Gotz, F., Landmann, R., Biofilm formation induces C3a release and protects Staphylococcus epidermidis from IgG and complement deposition and from neutrophil-dependent killing. J Infect Dis 197:7 (2008), 1028–1035.
123. 123 Domenech, M., Ramos-Sevillano, E., Garcia, E., Moscoso, M., Yuste, J., Biofilm formation avoids complement immunity and phagocytosis of Streptococcus pneumoniae. Infect Immun 81:7 (2013), 2606–2615.
124. 124 Jensen, E.T., Kharazmi, A., Lam, K., Costerton, J.W., Hoiby, N., Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms. Infect Immun 58:7 (1990), 2383–2385.
125. 125 Jensen, E.T., Kharazmi, A., Hoiby, N., Costerton, J.W., Some bacterial parameters influencing the neutrophil oxidative burst response to Pseudomonas aeruginosa biofilms. APMIS 100:8 (1992), 727–733.
126. 126 Jesaitis, A.J., Franklin, M.J., Berglund, D., et al. Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J Immunol 171:8 (2003), 4329–4339.
127. 127 Alhede, M., Kragh, K.N., Qvortrup, K., et al. Phenotypes of non-attached Pseudomonas aeruginosa aggregates resemble surface attached biofilm. PLoS One, 6(11), 2011, e27943.
128. 128 Dusane, D.H., Zinjarde, S.S., Venugopalan, V.P., McLean, R.J., Weber, M.M., Rahman, P.K., Quorum sensing: implications on rhamnolipid biosurfactant production. Biotechnol Genet Eng Rev 27 (2010), 159–184.
129. 129 Morici, L.A., Carterson, A.J., Wagner, V.E., et al. Pseudomonas aeruginosa AlgR represses the Rhl quorum-sensing system in a biofilm-specific manner. J Bacteriol 189:21 (2007), 7752–7764.
130. 130 Bjarnsholt, T., Jensen, P.O., Burmolle, M., et al. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:Pt 2 (2005), 373–383.
131. 131 Alhede, M., Bjarnsholt, T., Jensen, P.O., et al. Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiology 155:Pt 11 (2009), 3500–3508.
132. 132 Jakobsen, T.H., van Gennip, M., Phipps, R.K., et al. Ajoene, a sulfur-rich molecule from garlic, inhibits genes controlled by quorum sensing. Antimicrob Agents Chemother 56:5 (2012), 2314–2325.
133. 133 van Gennip, M., Christensen, L.D., Alhede, M., et al. Interactions between polymorphonuclear leukocytes and Pseudomonas aeruginosa biofilms on silicone implants in vivo. Infect Immun 80:8 (2012), 2601–2607.
134. 134 Walker, T.S., Tomlin, K.L., Worthen, G.S., et al. Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils. Infect Immun 73:6 (2005), 3693–3701.
135. 135 Chiang, W.C., Nilsson, M., Jensen, P.O., et al. Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 57:5 (2013), 2352–2361.
136. 136 Watters, C., Everett, J.A., Haley, C., Clinton, A., Rumbaugh, K.P., Insulin treatment modulates the host immune system to enhance Pseudomonas aeruginosa wound biofilms. Infect Immun. 82:1 (2014), 92–100.
137. 137 Dale, D.C., Boxer, L., Liles, W.C., The phagocytes: neutrophils and monocytes. Blood 112:4 (2008), 935–945.
138. 138 Shi, C., Pamer, E.G., Monocyte recruitment during infection and inflammation. Nat Rev Immunol 11:11 (2011), 762–774.
139. 139 Schroder, K., Hertzog, P.J., Ravasi, T., Hume, D.A., Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75:2 (2004), 163–189.
140. 140 Gordon, S., Alternative activation of macrophages. Nat Rev Immunol 3:1 (2003), 23–35.
141. 141 Mosser, D.M., Edwards, J.P., Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:12 (2008), 958–969.
142. 142 Colucci-Guyon, E., Tinevez, J.Y., Renshaw, S.A., Herbomel, P., Strategies of professional phagocytes in vivo: unlike macrophages, neutrophils engulf only surface-associated microbes. J Cell Sci 124:Pt 18 (2011), 3053–3059.
143. 143 Myrvik, Q.N., Wagner, W., Barth, E., Wood, P., Gristina, A.G., Effects of extracellular slime produced by Staphylococcus epidermidis on oxidative responses of rabbit alveolar macrophages. J Invest Surg 2:4 (1989), 381–389.
144. 144 Schommer, N.N., Christner, M., Hentschke, M., Ruckdeschel, K., Aepfelbacher, M., Rohde, H., Staphylococcus epidermidis uses distinct mechanisms of biofilm formation to interfere with phagocytosis and activation of mouse macrophage-like cells 774A.1. Infect Immun 79:6 (2011), 2267–2276.
145. 145 Cerca, F., Andrade, F., Franca, A., et al. Staphylococcus epidermidis biofilms with higher proportions of dormant bacteria induce a lower activation of murine macrophages. J Med Microbiol 60:Pt 12 (2011), 1717–1724.
146. 146 Mittal, R., Sharma, S., Chhibber, S., Harjai, K., Effect of macrophage secretory products on elaboration of virulence factors by planktonic and biofilm cells of Pseudomonas aeruginosa. Comp Immunol Microbiol Infect Dis 29:1 (2006), 12–26.
147. 147 Chandra, J., McCormick, T.S., Imamura, Y., Mukherjee, P.K., Ghannoum, M.A., 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 75:5 (2007), 2612–2620.
148. 148 Scherr, T.D., Hanke, M.L., Huang, O., et al. Staphylococcus aureus biofilms induce macrophage dysfunction through leukocidin AB and alpha-toxin. mBio, 6(4), 2015.
149. 149 Thurlow, L.R., Hanke, M.L., Fritz, T., et al. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J Immunol 186:11 (2011), 6585–6596.
150. 150 Hanke, M.L., Angle, A., Kielian, T., MyD88-dependent signaling influences fibrosis and alternative macrophage activation during Staphylococcus aureus biofilm infection. PloS One, 7(8), 2012, e42476.
151. 151 Hanke, M.L., Heim, C.E., Angle, A., Sanderson, S.D., Kielian, T., Targeting macrophage activation for the prevention and treatment of Staphylococcus aureus biofilm infections. J Immunol 190:5 (2013), 2159–2168.
152. 152 Stephen, T.L., Groneck, L., Kalka-Moll, W.M., The modulation of adaptive immune responses by bacterial zwitterionic polysaccharides. Int J Microbiol, 2010, 2010, 917075.
153. 153 Heim, C.E., Vidlak, D., Scherr, T.D., Hartman, C.W., Garvin, K.L., Kielian, T., IL-12 promotes myeloid-derived suppressor cell recruitment and bacterial persistence during Staphylococcus aureus orthopedic implant infection. J Immunol 194:8 (2015), 3861–3872.
154. 154 Peck, A., Mellins, E.D., Precarious balance: Th17 cells in host defense. Infect Immun 78:1 (2010), 32–38.
155. 155 Aujla, S.J., Dubin, P.J., Kolls, J.K., Th17 cells and mucosal host defense. Semin Immunol 19:6 (2007), 377–382.
156. 156 Jensen, L.K., Jensen, H.E., Koch, J., Bjarnsholt, T., Eickhardt, S., Shirtliff, M., Specific antibodies to Staphylococcus aureus biofilm are present in serum from pigs with osteomyelitis. In Vivo 29:5 (2015), 555–560.
157. 157 Prabhakara, R., Harro, J.M., Leid, J.G., Harris, M., Shirtliff, M.E., Murine immune response to a chronic Staphylococcus aureus biofilm infection. Infect Immun 79:4 (2011), 1789–1796.
158. 158 Prabhakara, R., Harro, J.M., Leid, J.G., Keegan, A.D., Prior, M.L., Shirtliff, M.E., Suppression of the inflammatory immune response prevents the development of chronic biofilm infection due to methicillin-resistant Staphylococcus aureus. Infect Immun 79:12 (2011), 5010–5018.
159. 159 Heim, C.E., Vidlak, D., Scherr, T.D., et al. Myeloid-derived suppressor cells contribute to Staphylococcus aureus orthopedic biofilm infection. J Immunol 192:8 (2014), 3778–3792.
160. 160 Rieu, A., Aoudia, N., Jego, G., et al. The biofilm mode of life boosts the anti-inflammatory properties of Lactobacillus. Cell Microbiol 16:12 (2014), 1836–1853.
161. 161 Jones, S.E., Versalovic, J., Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol, 9, 2009, 35.
162. 162 Sonal Sekhar, M., Unnikrishnan, M.K., Vijayanarayana, K., Rodrigues, G.S., Mukhopadhyay, C., Topical application/formulation of probiotics: will it be a novel treatment approach for diabetic foot ulcer?. Med Hypotheses 82:1 (2014), 86–88.
163. 163 Lebeer, S., Verhoeven, T.L., Perea Velez, M., Vanderleyden, J., De Keersmaecker, S.C., Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol 73:21 (2007), 6768–6775.
164. 164 Kubota, H., Senda, S., Nomura, N., Tokuda, H., Uchiyama, H., Biofilm formation by lactic acid bacteria and resistance to environmental stress. J Biosci Bioeng 106:4 (2008), 381–386.
165. 165 Bove, P., Capozzi, V., Garofalo, C., Rieu, A., Spano, G., Fiocco, D., Inactivation of the ftsH gene of Lactobacillus plantarum WCFS1: effects on growth, stress tolerance, cell surface properties and biofilm formation. Microbiol Res 167:4 (2012), 187–193.
166. 166 Vong, L., Lorentz, R.J., Assa, A., Glogauer, M., Sherman, P.M., Probiotic Lactobacillus rhamnosus inhibits the formation of neutrophil extracellular traps. J Immunol 192:4 (2014), 1870–1877.
167. 167 Kubota, H., Senda, S., Tokuda, H., Uchiyama, H., Nomura, N., Stress resistance of biofilm and planktonic Lactobacillus plantarum subsp. plantarum JCM 1149. Food Microbiol 26:6 (2009), 592–597.
168. 168 Dong, H., Rowland, I., Yaqoob, P., Comparative effects of six probiotic strains on immune function in vitro. Br J Nutr 108:3 (2012), 459–470.
169. 169 Alander, M., Satokari, R., Korpela, R., et al. Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl Environ Microbiol 65:1 (1999), 351–354.
170. 170 Schultz, M., Gottl, C., Young, R.J., Iwen, P., Vanderhoof, J.A., Administration of oral probiotic bacteria to pregnant women causes temporary infantile colonization. J Pediatr Gastroenterol Nutr 38:3 (2004), 293–297.
171. 171 Jalilsood, T., Baradaran, A., Song, A.A., et al. Inhibition of pathogenic and spoilage bacteria by a novel biofilm-forming Lactobacillus isolate: a potential host for the expression of heterologous proteins. Microb Cell Fact, 14, 2015, 96.
172. 172 Donnet-Hughes, A., Rochat, F., Serrant, P., Aeschlimann, J.M., Schiffrin, E.J., Modulation of nonspecific mechanisms of defense by lactic acid bacteria: effective dose. J Dairy Sci 82:5 (1999), 863–869.
173. 173 Baiu, D.C., Prechl, J., Tchorbanov, A., et al. Modulation of the humoral immune response by antibody-mediated antigen targeting to complement receptors and Fc receptors. J Immunol 162:6 (1999), 3125–3130.
174. 174 Arunachalam, K., Gill, H.S., Chandra, R.K., Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur J Clin Nutr 54:3 (2000), 263–267.
175. 175 Ramos, A.N., Gobbato, N., Rachid, M., Gonzalez, L., Yantorno, O., Valdez, J.C., Effect of Lactobacillus plantarum and Pseudomonas aeruginosa culture supernatants on polymorphonuclear damage and inflammatory response. Int Immunopharmacol 10:2 (2010), 247–251.
176. 176 Marin-Esteban, V., Turbica, I., Dufour, G., et al. Afa/Dr diffusely adhering Escherichia coli strain C1845 induces neutrophil extracellular traps that kill bacteria and damage human enterocyte-like cells. Infect Immun. 80:5 (2012), 1891–1899.
177. 177 Wong, S.L., Demers, M., Martinod, K., et al. Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med 21:7 (2015), 815–819.
178. 178 Menegazzo, L., Ciciliot, S., Poncina, N., et al. NETosis is induced by high glucose and associated with type 2 diabetes. Acta Diabetol 52:3 (2015), 497–503.
179. 179 Malickova, K., Duricova, D., Bortlik, M., et al. Impaired deoxyribonuclease I activity in patients with inflammatory bowel diseases. Autoimmune Dis, 2011, 2011, 945861.
180. 180 Aoudia, N., Rieu, A., Briandet, R., et al. Biofilms of Lactobacillus plantarum and Lactobacillus fermentum: Effect on stress responses, antagonistic effects on pathogen growth and immunomodulatory properties. Food Microbiol 53:Pt A (2016), 51–59.
181. 181 Kretz-Remy, C., Mehlen, P., Mirault, M.E., Arrigo, A.P., Inhibition of I kappa B-alpha phosphorylation and degradation and subsequent NF-kappa B activation by glutathione peroxidase overexpression. J Cell Biol 133:5 (1996), 1083–1093.
182. 182 Bergonzelli, G.E., Granato, D., Pridmore, R.D., Marvin-Guy, L.F., Donnicola, D., Corthesy-Theulaz, I.E., GroEL of Lactobacillus johnsonii La1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori. Infect Immun. 74:1 (2006), 425–434.
183. 183 Torres-Maravilla, E., Lenoir, M., Mayorga-Reyes, L., et al. Identification of novel anti-inflammatory probiotic strains isolated from pulque. Appl Microbiol Biotechnol 100:1 (2015), 385–396.
184. 184 Kim, S.O., Sheikh, H.I., Ha, S.D., Martins, A., Reid, G., G-CSF-mediated inhibition of JNK is a key mechanism for Lactobacillus rhamnosus-induced suppression of TNF production in macrophages. Cell Microbiol 8:12 (2006), 1958–1971.
185. 185 Martins, A.J., Spanton, S., Sheikh, H.I., Kim, S.O., The anti-inflammatory role of granulocyte colony-stimulating factor in macrophage-dendritic cell crosstalk after Lactobacillus rhamnosus GR-1 exposure. J Leukoc Biol 89:6 (2011), 907–915.
186. 186 Mackowiak, P.A., Recycling metchnikoff: probiotics, the intestinal microbiome and the quest for long life. Front Public Health, 1, 2013, 52.
187. 187 Elisa Guerrieri SdN, Patrizia Messi, Carla Sabia, Ramona Iseppi, Immacolata Anacarso, Moreno Bondi. Use of lactic acid bacteria (LAB) biofilms for the control of Listeria monocytogenes. Food Control. 2009;20(9):861–865.
188. 188 Russo, P., Iturria, I., Mohedano, M.L., et al. Zebrafish gut colonization by mCherry-labelled lactic acid bacteria. Appl Microbiol Biotechnol 99:8 (2015), 3479–3490.
189. 189 Lebeer, S., Verhoeven, T.L., Claes, I.J., et al. FISH analysis of Lactobacillus biofilms in the gastrointestinal tract of different hosts. Lett Appl Microbiol 52:3 (2011), 220–226.
190. 190 Ventolini, G., Vaginal Lactobacillus: biofilm formation in vivo—clinical implications. Int J Womens Health 7 (2015), 243–247.
191. 191 Marrazzo, J.M., Vaginal biofilms and bacterial vaginosis: of mice and women. J Infect Dis 207:10 (2013), 1481–1483.
192. 192 Machado, A., Jefferson, K.K., Cerca, N., Interactions between Lactobacillus crispatus and bacterial vaginosis (BV)-associated bacterial species in initial attachment and biofilm formation. Int J Mol Sci 14:6 (2013), 12004–12012.
193. 193 Castro, J., Henriques, A., Machado, A., Henriques, M., Jefferson, K.K., Cerca, N., Reciprocal interference between Lactobacillus spp. and Gardnerella vaginalis on initial adherence to epithelial cells. Int J Med Sci 10:9 (2013), 1193–1198.
194. 194 Ogunshe, A.A., Omotoso, M.A., Bello, V.B., The in vitro antimicrobial activities of metabolites from Lactobacillus strains on Candida species implicated in Candida vaginitis. MJMS 18:4 (2011), 13–25.
195. 195 Pelzer, E.S., Allan, J.A., Waterhouse, M.A., Ross, T., Beagley, K.W., Knox, C.L., Microorganisms within human follicular fluid: effects on IVF. PloS One, 8(3), 2013, e59062.
196. 196 Moore, D.E., Soules, M.R., Klein, N.A., Fujimoto, V.Y., Agnew, K.J., Eschenbach, D.A., Bacteria in the transfer catheter tip influence the live-birth rate after in vitro fertilization. Fertil Steril 74:6 (2000), 1118–1124.
197. 197 Romero, R., Schaudinn, C., Kusanovic, J.P., et al. Detection of a microbial biofilm in intraamniotic infection. Am J Obstet Gynecol, 198(1), 2008 135 e131-135.
198. 198 Satokari, R., Gronroos, T., Laitinen, K., Salminen, S., Isolauri, E., Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol 48:1 (2009), 8–12.
199. 199 Fichorova, R.N., Onderdonk, A.B., Yamamoto, H., et al. Maternal microbe-specific modulation of inflammatory response in extremely low-gestational-age newborns. mBio 2:1 (2011), e00280–e00310.
200. 200 Romero, R., Mazor, M., Wu, Y.K., Avila, C., Oyarzun, E., Mitchell, M.D., Bacterial endotoxin and tumor necrosis factor stimulate prostaglandin production by human decidua. Prostaglandins Leukot Essent Fatty Acids 37:3 (1989), 183–186.
201. 201 Yeganegi, M., Watson, C.S., Martins, A., et al. Effect of Lactobacillus rhamnosus GR-1 supernatant and fetal sex on lipopolysaccharide-induced cytokine and prostaglandin-regulating enzymes in human placental trophoblast cells: implications for treatment of bacterial vaginosis and prevention of preterm labor. Am J Obstet Gynecol, 200(5), 2009 532 e531-538.
202. 202 Yeganegi, M., Leung, C.G., Martins, A., et al. Lactobacillus rhamnosus GR-1 stimulates colony-stimulating factor 3 (granulocyte) (CSF3) output in placental trophoblast cells in a fetal sex-dependent manner. Biol Reprod 84:1 (2011), 18–25.
203. 203 Yang, S., Li, W., Challis, J.R., Reid, G., Kim, S.O., Bocking, A.D., Probiotic Lactobacillus rhamnosus GR-1 supernatant prevents lipopolysaccharide-induced preterm birth and reduces inflammation in pregnant CD-1 mice. Am J Obstet Gynecol, 211(1), 2014 44 e41–44 e12.
204. 204 Gueniche, A., Bastien, P., Ovigne, J.M., et al. Bifidobacterium longum lysate, a new ingredient for reactive skin. Exp Dermatol 19:8 (2010), e1–e8.
205. 205 Roy, S., Elgharably, H., Sinha, M., et al. Mixed-species biofilm compromises wound healing by disrupting epidermal barrier function. J Pathol 233:4 (2014), 331–343.
206. 206 Ouwehand, A.C., Batsman, A., Salminen, S., Probiotics for the skin: a new area of potential application?. Lett Appl Microbiol 36:5 (2003), 327–331.
207. 207 Prince, T., McBain, A.J., O'Neill, C.A., Lactobacillus reuteri protects epidermal keratinocytes from Staphylococcus aureus-induced cell death by competitive exclusion. Appl Environ Microbiol 78:15 (2012), 5119–5126.
208. 208 Mohammedsaeed, W., McBain, A.J., Cruickshank, S.M., O'Neill, C.A., Lactobacillus rhamnosus GG inhibits the toxic effects of Staphylococcus aureus on epidermal keratinocytes. Appl Environ Microbiol 80:18 (2014), 5773–5781.
209. 209 Sultana, R., McBain, A.J., O'Neill, C.A., Strain-dependent augmentation of tight-junction barrier function in human primary epidermal keratinocytes by Lactobacillus and Bifidobacterium lysates. Appl Environ Microbiol 79:16 (2013), 4887–4894.
210. 210 Mohammedsaeed, W., Cruickshank, S., McBain, A.J., O'Neill, C.A., Lactobacillus rhamnosus GG lysate increases re-epithelialization of keratinocyte scratch assays by promoting migration. Sci Rep, 5, 2015, 16147.
211. 211 Zahedi, F., Heydari Nasrabadi, M., Tajabadi Ebrahimi, M., Aboutalebi, H., Comparison of the effects of Lactobacillus brevis and Lactobacillus plantarum on cutaneous wound healing in rats. Afr J Microbiol Res 5:24 (2011), 4226–4233.