Pseudomonas aeruginosa outer membrane vesicles triggered by human mucosal fluid and lysozyme can prime host tissue surfaces for bacterial adhesion

Frontiers in Microbiology

Volumn 7, Issue JUN, 2016, Pages

  Metruccio, Matteo M E ^a   Evans, David J ^a,b   Gabriel, Manal M ^c   Kadurugamuwa, Jagath L ^d   Fleiszig, Suzanne M J ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TOURO UNIVERSITY CALIFORNIA   (United States)

^c Alcon Research Ltd   (United States)

^d Alcon Researc   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adhesion; Cornea; Epithelium; Human tears; Lysozyme; Microbial keratitis; Pseudomonas aeruginosa outer membrane vesicles

Indexed keywords

ANTIINFECTIVE AGENT; LYSOZYME;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM ADHERENCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE VESICLE; MOUSE; NONHUMAN; NORMAL HUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PSEUDOMONAS AERUGINOSA; RETINA TEAR; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84979988066     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00871     Document Type: Article

References (73)

1. Alarcon, I., Kwan, L., Yu, C., Evans, D. J., and Fleiszig, S. M. J. (2009). Role of the corneal epithelial basement membrane in ocular defense against Pseudomonas aeruginosa. Infect. Immun. 77, 3264-3271. doi: 10.1128/IAI.00111-09
2. Alarcon, I., Tam, C., Mun, J. J., LeDue, J., Evans, D. J., and Fleiszig, S. M. J. (2011). Factors impacting corneal epithelial barrier function against Pseudomonas aeruginosa traversal. Invest. Ophthalmol. Vis. Sci. 52, 1368-1377. doi: 10.1167/iovs.10-6125
3. Augustin, D. K., Heimer, S. R., Tam, C., Li, W. Y., Le Due, J. M., Evans, D. J., et al. (2011). Role of defensins in corneal epithelial barrier function against Pseudomonas aeruginosa traversal. Infect. Immun. 79, 595-605. doi: 10.1128/IAI.00854-10
4. Bauman, S. J., and Kuehn, M. J. (2006). Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect. 8, 2400-2408. doi: 10.1016/j.micinf.2006.05.001
5. Baumgarten, T., Sperling, S., Seifert, J., von Bergen, M., Steiniger, F., Wick, L. Y., et al. (2012). Membrane vesicle formation as a multiple-stress response mechanism enhances Pseudomonas putida DOT-T1E cell surface hydrophobicity and biofilm formation. Appl. Environ. Microbiol. 78, 6217-6224. doi: 10.1128/AEM.01525-12
6. Beveridge, T. J., Makin, S. A., Kadurugamuwa, J. L., and Li, Z. (1997). Interactions between biofilms and the environment. FEMS Microbiol. Rev. 20, 291-303. doi: 10.1111/j.1574-6976.1997.tb00315.x
7. Bloemberg, G. V., O'Toole, G. A., Lugtenberg, B. J., and Kolter, R. (1997). Green fluorescent protein as a marker for Pseudomonas spp. Appl. Environ. Microbiol. 63, 4543-4551.
8. Bomberger, J. M., Maceachran, D. P., Coutermarsh, B. A., Ye, S., O'Toole, G. A., and Stanton, B. A. (2009). Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 5:e1000382. doi: 10.1371/journal.ppat.1000382
9. Bomberger, J. M., Ye, S., Maceachran, D. P., Koeppen, K., Barnaby, R. L., O'Toole, G. A., et al. (2011). A Pseudomonas aeruginosa toxin that hijacks the host ubiquitin proteolytic system. PLoS Pathog. 7:e1001325. doi: 10.1371/journal.ppat.1001325
10. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., et al. (2004). Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535. doi: 10.1126/science.1092385
11. Callewaert, L., Aertsen, A., Deckers, D., Vanoirbeek, K. G. A., Vanderkelen, L., Van Herreweghe, J. M., et al. (2008). A new family of lysozyme inhibitors contributing to lysozyme tolerance in gram-negative bacteria. PLoS Pathog. 4:e1000019. doi: 10.1371/journal.ppat.1000019
12. Chi, B., Qi, M., and Kuramitsu, H. K. (2003). Role of dentilisin in Treponema denticola epithelial cell layer penetration. Res. Microbiol. 154, 637-643. doi: 10.1016/j.resmic.2003.08.001
13. Cowell, B. A., Willcox, M. D., and Schneider, R. P. (1997). Growth of gram-negative bacteria in a simulated ocular environment. Aust. N. Z. J. Ophthalmol. 25(Suppl. 1), S23-S26. doi: 10.1111/j.1442-9071.1997.tb01748.x
14. Derde, M., Nau, F., Guérin-Dubiard, C., Lechevalier, V., Paboeuf, G., Jan, S., et al. (2015). Native and dry-heated lysozyme interactions with membrane lipid monolayers: lipid packing modifications of a phospholipid mixture, model of the Escherichia coli cytoplasmic membrane. Biochim. Biophys. Acta 1848, 1065-1073. doi: 10.1016/j.bbamem.2015.01.008
15. Dorward, D. W., Garon, C. F., and Judd, R. C. (1989). Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J. Bacteriol. 171, 2499-2505.
16. Evans, D. J., and Fleiszig, S. M. J. (2013). Why does the healthy cornea resist Pseudomonas aeruginosa infection? Am. J. Ophthalmol. 155, 961.e-970.e. doi: 10.1016/j.ajo.2013.03.001
17. Flanagan, J. L., and Willcox, M. D. P. (2009). Role of lactoferrin in the tear film. Biochimie 91, 35-43. doi: 10.1016/j.biochi.2008.07.007
18. Frias, A., Manresa, A., de Oliveira, E., Lopez-Iglesias, C., and Mercade, E. (2010). Membrane vesicles: a common feature in the extracellular matter of cold-adapted antarctic bacteria. Microb. Ecol. 59, 476-486. doi: 10.1007/s00248-009-9622-9
19. Hahn, N., Eisen, R. J., Eisen, L., and Lane, R. S. (2005). Ketamine-medetomidine anesthesia with atipamezole reversal: practical anesthesia for rodents under field conditions. Lab Anim. 34, 48-51. doi: 10.1038/laban0205-48
20. Hall, B., Jones, L., and Forrest, J. A. (2014). Kinetics of competitive adsorption between lysozyme and lactoferrin on silicone hydrogel contact lenses and the effect on lysozyme activity. Curr. Eye Res. 40, 622-631. doi: 10.3109/02713683.2014.946518
21. Hanlon, S. D., Smith, C. W., Sauter, M. N., and Burns, A. R. (2014). Integrin-dependent neutrophil migration in the injured mouse cornea. Exp. Eye Res. 120, 61-70. doi: 10.1016/j.exer.2014.01.004
22. Kadurugamuwa, J. L., and Beveridge, T. J. (1995). Virulence Factors Are Released From Pseudomonas-Aeruginosa in association with membrane-vesicles during normal growth and exposure to gentamicin-a novel mechanism of enzyme-secretion. J. Bacteriol. 177, 3998-4008.
23. Kadurugamuwa, J. L., and Beveridge, T. J. (1996). Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J. Bacteriol. 178, 2767-2774.
24. Kadurugamuwa, J. L., and Beveridge, T. J. (1997). Natural release of virulence factors in membrane vesicles by Pseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release. J. Antimicrob. Chemother. 40, 615-621. doi: 10.1093/jac/40.5.615
25. Kadurugamuwa, J. L., and Beveridge, T. J. (1998). Delivery of the non-membrane-permeative antibiotic gentamicin into mammalian cells by using Shigella flexneri membrane vesicles. Antimicrob. Agents Chemother. 42, 1476-1483.
26. Kamiya, H., Ehara, T., and Matsumoto, T. (2012). Inhibitory effects of lactoferrin on biofilm formation in clinical isolates of Pseudomonas aeruginosa. J. Infect. Chemother. 18, 47-52. doi: 10.1007/s10156-011-0287-1
27. Katsui, N., Tsuchido, T., Hiramatsu, R., Fujikawa, S., Takano, M., and Shibasaki, I. (1982). Heat-induced blebbing and vesiculation of the outer membrane of Escherichia coli. J. Bacteriol. 151, 1523-1531.
28. Kuo, I.-H., Carpenter-Mendini, A., Yoshida, T., McGirt, L. Y., Ivanov, A. I., Barnes, K. C., et al. (2013). Activation of epidermal toll-like receptor 2 enhances tight junction function: implications for atopic dermatitis and skin barrier repair. J. Invest. Dermatol. 133, 988-998. doi: 10.1038/jid.2012.437
29. Macdonald, I. A., and Kuehn, M. J. (2013). Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa. J. Bacteriol. 195, 2971-2981. doi: 10.1128/JB.02267-12
30. Maltseva, I. A., Fleiszig, S. M. J., Evans, D. J., Kerr, S., Sidhu, S. S., McNamara, N. A., et al. (2007). Exposure of human corneal epithelial cells to contact lenses in vitro suppresses the upregulation of human beta-defensin-2 in response to antigens of Pseudomonas aeruginosa. Exp. Eye Res. 85, 142-153. doi: 10.1016/j.exer.2007.04.001
31. Mannucci, L. L., Moro, F., Cosani, A., and Palumbo, M. (1985). Conformational state of lacrimal proteins adsorbed on contact lenses. Curr. Eye Res. 4, 734-736. doi: 10.3109/02713688509017675
32. Mantelli, F., Mauris, J., and Argüeso, P. (2013). The ocular surface epithelial barrier and other mechanisms of mucosal protection: from allergy to infectious diseases. Curr. Opin. Allergy Clin. Immunol. 13, 563-568. doi: 10.1097/ACI.0b013e3283645899
33. Maredia, R., Devineni, N., Lentz, P., Dallo, S. F., Yu, J., Guentzel, N., et al. (2012). Vesiculation from Pseudomonas aeruginosa under SOS. Sci. World J. 2012:402919. doi: 10.1100/2012/402919
34. Mashburn, L. M., and Whiteley, M. (2005). Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437, 422-425. doi: 10.1038/nature03925
35. Masinick, S. A., Montgomery, C. P., Montgomery, P. C., and Hazlett, L. D. (1997). Secretory IgA inhibits Pseudomonas aeruginosa binding to cornea and protects against keratitis. Invest. Ophthalmol. Vis. Sci. 38, k910-918.
36. McDermott, A. M. (2009). The role of antimicrobial peptides at the ocular surface. Ophthalmic Res. 41, 60-75. doi: 10.1159/000187622
37. McDermott, A. M., Redfern, R. L., Zhang, B., Pei, Y., Huang, L., and Proske, R. J. (2003). Defensin expression by the cornea: multiple signalling pathways mediate IL-1beta stimulation of hBD-2 expression by human corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 44, 1859-1865. doi: 10.1167/iovs.02-0787
38. Mun, J. J., Tam, C., Kowbel, D., Hawgood, S., Barnett, M. J., Evans, D. J., et al. (2009). Clearance of Pseudomonas aeruginosa from a healthy ocular surface involves surfactant protein D and is compromised by bacterial elastase in a murine null-infection model. Infect. Immun. 77, 2392-2398. doi: 10.1128/IAI.00173-09
39. Murphy, K., Park, A. J., Hao, Y., Brewer, D., Lam, J. S., and Khursigara, C. M. (2014). Influence of O polysaccharides on biofilm development and outer membrane vesicle biogenesis in Pseudomonas aeruginosa PAO1. J. Bacteriol. 196, 1306-1317. doi: 10.1128/JB.01463-13
40. Nagaraju, K., Motukupally, S. R., Garg, P., Sharma, S., Ali, M. H., and Willcox, M. D. P. (2014). Microbial analyses of contact lens-associated microbial keratitis. Optom. Vis. Sci. 91, 47-53. doi: 10.1097/OPX.0000000000000082
41. Namork, E., and Brandtzaeg, P. (2002). Fatal meningococcal septicaemia with "blebbing" meningococcus. Lancet 360:1741. doi: 10.1016/S0140-6736(02)11721-1
42. Ni, M., Evans, D. J., Hawgood, S., Anders, E. M., Sack, R. A., and Fleiszig, S. M. J. (2005). Surfactant protein D is present in human tear fluid and the cornea and inhibits epithelial cell invasion by Pseudomonas aeruginosa. Infect. Immun. 73, 2147-2156. doi: 10.1128/IAI.73.4.2147-2156.2005
43. Park, A. J., Surette, M. D., and Khursigara, C. M. (2014). Antimicrobial targets localize to the extracellular vesicle-associated proteome of Pseudomonas aeruginosa grown in a biofilm. Front. Microbiol. 5:464. doi: 10.3389/fmicb.2014.00464
44. Pellegrini, A., Thomas, U., von Fellenberg, R., and Wild, P. (1992). Bactericidal activities of lysozyme and aprotinin against gram-negative and gram-positive bacteria related to their basic character. J. Appl. Bacteriol. 72, 180-187. doi: 10.1111/j.1365-2672.1992.tb01821.x
45. Peuravuori, H., Aho, V. V., Aho, H. J., Collan, Y., and Saari, K. M. (2006). Bactericidal/permeability-increasing protein in lacrimal gland and in tears of healthy subjects. Graefes Arch. Clin. Exp. Ophthalmol. 244, 143-148. doi: 10.1007/s00417-005-0062-z
46. Pier, G. B., Grout, M., Zaidi, T. S., and Goldberg, J. B. (1996). How mutant CFTR may contribute to Pseudomonas aeruginosa infection in cystic fibrosis. Am. J. Respir. Crit. Care Med. 154, S175-S182. doi: 10.1164/ajrccm/154.4_Pt_2.S175
47. Preston, M. J., Fleiszig, S. M., Zaidi, T. S., Goldberg, J. B., Shortridge, V. D., Vasil, M. L., et al. (1995). Rapid and sensitive method for evaluating Pseudomonas aeruginosa virulence factors during corneal infections in mice. Infect. Immun. 63, 3497-3501.
48. Renelli, M., Matias, V., Lo, R. Y., and Beveridge, T. J. (2004). DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 150, 2161-2169. doi: 10.1099/mic.0.26841-0
49. Robertson, D. M., Li, L., Fisher, S., Pearce, V. P., Shay, J. W., Wright, W. E., et al. (2005). Characterization of growth and differentiation in a telomerase-immortalized human corneal epithelial cell line. Invest. Ophthalmol. Vis. Sci. 46, 470-478. doi: 10.1167/iovs.04-0528
50. Rumbo, C., Fernández-Moreira, E., Merino, M., Poza, M., Mendez, J. A., Soares, N. C., et al. (2011). Horizontal transfer of the OXA-24 carbapenemase gene via outer membrane vesicles: a new mechanism of dissemination of carbapenem resistance genes in Acinetobacter baumannii. Antimicrob. Agents Chemother. 55, 3084-3090. doi: 10.1128/AAC.00929-10
51. Sakata, M., Sack, R. A., Sathe, S., Holden, B., and Beaton, A. R. (1997). Polymorphonuclear leukocyte cells and elastase in tears. Curr. Eye Res. 16, 810-819. doi: 10.1076/ceyr.16.8.810.8992
52. Schertzer, J. W., and Whiteley, M. (2013). Bacterial outer membrane vesicles in trafficking, communication and the host-pathogen interaction. J. Mol. Microbiol. Biotechnol. 23, 118-130. doi: 10.1159/000346770
53. Schooling, S. R., and Beveridge, T. J. (2006). Membrane vesicles: an overlooked component of the matrices of biofilms. J. Bacteriol. 188, 5945-5957. doi: 10.1128/JB.00257-06
54. Schooling, S. R., Hubley, A., and Beveridge, T. J. (2009). Interactions of DNA with biofilm-derived membrane vesicles. J. Bacteriol. 191, 4097-4102. doi: 10.1128/JB.00717-08
55. Selinger, D. S., Selinger, R. C., and Reed, W. P. (1979). Resistance to infection of the external eye: the role of tears. Surv. Ophthalmol. 24, 33-38. doi: 10.1016/0039-6257(79)90145-0
56. Shan, Q., Dwyer, M., Rahman, S., and Gadjeva, M. (2014). Distinct Susceptibilities of Corneal Pseudomonas aeruginosa clinical isolates to neutrophil extracellular trap-mediated immunity. Infect. Immun. 82, 4135-4143. doi: 10.1128/IAI.02169-14
57. Singer, J. T., Phennicie, R. T., Sullivan, M. J., Porter, L. A., Shaffer, V. J., and Kim, C. H. (2010). Broad-host-range plasmids for red fluorescent protein labeling of gram-negative bacteria for use in the zebrafish model system. Appl. Environ. Microbiol. 76, 3467-3474. doi: 10.1128/AEM.01679-09
58. Stapleton, F., and Carnt, N. (2012). Contact lens-related microbial keratitis: how have epidemiology and genetics helped us with pathogenesis and prophylaxis. Eye (Lond.) 26, 185-193. doi: 10.1038/eye.2011.288
59. Stapleton, F., and Dart, J. (1995). Pseudomonas keratitis associated with biofilm formation on a disposable soft contact lens. Br. J. Ophthalmol. 79, 864-865. doi: 10.1136/bjo.79.9.864
60. Stapleton, F., Dart, J. K. G., Seal, D. V., and Matheson, M. (2009). Epidemiology of Pseudomonas aeruginosa keratitis in contact lens wearers. Epidemiol. Infect. 114:395. doi: 10.1017/S0950268800052109
61. Sullivan, A. B., Tam, K. P. C., Metruccio, M. M. E., Evans, D. J., and Fleiszig, S. M. J. (2015). The importance of the Pseudomonas aeruginosa type III secretion system in epithelium traversal depends upon conditions of host susceptibility. Infect. Immun. 83, 1629-1640. doi: 10.1128/IAI.02329-14
62. Tam, C., LeDue, J., Mun, J. J., Herzmark, P., Robey, E. A., Evans, D. J., et al. (2011). 3D quantitative imaging of unprocessed live tissue reveals epithelial defense against bacterial adhesion and subsequent traversal requires MyD88. PLoS ONE 6:e24008. doi: 10.1371/journal.pone.0024008
63. Tam, C., Mun, J. J., Evans, D. J., and Fleiszig, S. M. J. (2010). The impact of inoculation parameters on the pathogenesis of contact lens-related infectious keratitis. Investig. Ophthalmol. Vis. Sci. 51, 3100-3106. doi: 10.1167/iovs.09-4593
64. Tan, T. T., Morgelin, M., Forsgren, A., and Riesbeck, K. (2007). Haemophilus influenzae survival during complement-mediated attacks is promoted by Moraxella catarrhalis outer membrane vesicles. J. Infect. Dis. 195, 1661-1670. doi: 10.1086/517611
65. Thompson, S. S., Naidu, Y. M., and Pestka, J. J. (1985). Ultrastructural localization of an extracellular protease in Pseudomonas fragi by using the peroxidase-antiperoxidase reaction. Appl. Environ. Microbiol. 50, 1038-1042.
66. Toyofuku, M., Roschitzki, B., Riedel, K., and Eberl, L. (2012). Identification of proteins associated with the pseudomonas aeruginosa biofilm extracellular matrix. J. Proteome Res. 11, 4906-4915. doi: 10.1021/pr300395j
67. Ulluwishewa, D., Anderson, R. C., McNabb, W. C., Moughan, P. J., Wells, J. M., and Roy, N. C. (2011). Regulation of tight junction permeability by intestinal bacteria and dietary components. J. Nutr. 141, 769-776. doi: 10.3945/jn.110.135657
68. Willcox, M., Sharma, S., Naduvilath, T. J., Sankaridurg, P. R., Gopinathan, U., and Holden, B. A. (2011). External ocular surface and lens microbiota in contact lens wearers with corneal infiltrates during extended wear of hydrogel lenses. Eye Contact Lens 37, 90-95. doi: 10.1097/ICL.0b013e31820d12db
69. Yonezawa, H., Osaki, T., Kurata, S., Fukuda, M., Kawakami, H., Ochiai, K., et al. (2009). Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol. 9:197. doi: 10.1186/1471-2180-9-197
70. Yu, H., and Kim, K. S. (2012). YgfZ contributes to secretion of cytotoxic necrotizing factor 1 into outer-membrane vesicles in Escherichia coli. Microbiology 158, 612-621. doi: 10.1099/mic.0.054122-0
71. Yuki, T., Yoshida, H., Akazawa, Y., Komiya, A., Sugiyama, Y., and Inoue, S. (2011). Activation of TLR2 enhances tight junction barrier in epidermal keratinocytes. J. Immunol. 187, 3230-3237. doi: 10.4049/jimmunol.1100058
72. Zaidi, T. S., Fleiszig, S. M., Preston, M. J., Goldberg, J. B., and Pier, G. B. (1996). Lipopolysaccharide outer core is a ligand for corneal cell binding and ingestion of Pseudomonas aeruginosa. Invest. Ophthalmol. Vis. Sci. 37, 976-986.
73. Zhou, L., Huang, L. Q., Beuerman, R. W., Grigg, M. E., Li, S. F. Y., Chew, F. T., et al. (2004). Proteomic analysis of human tears: defensin expression after ocular surface surgery. J. Proteome Res. 3, 410-416. doi: 10.1021/pr034065n