Pseudomonas aeruginosa-derived rhamnolipids subvert the host innate immune response through manipulation of the human beta-defensin-2 expression

Cellular Microbiology

Volumn 14, Issue 9, 2012, Pages 1364-1375

  Dössel, Jomtje ^a   Meyer Hoffert, Ulf ^a   Schröder, Jens Michael ^a   Gerstel, Ulrich ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN 2; CALCIUM; INTERLEUKIN 1BETA; INTERLEUKIN 8; PROTEIN KINASE C; RHAMNOLIPID;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; BACTERIUM CULTURE; CALCIUM SIGNALING; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; INTERNALIZATION; KERATINOCYTE; MASS SPECTROMETRY; MEDIATOR RELEASE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; REAL TIME POLYMERASE CHAIN REACTION; SUPERNATANT; WESTERN BLOTTING;

BETA-DEFENSINS; CELLS, CULTURED; FLAGELLIN; GLYCOLIPIDS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, INNATE; INTERLEUKIN-1BETA; KERATINOCYTES; MODELS, BIOLOGICAL; PROTEIN KINASE C; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

EID: 84865345484     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01801.x     Document Type: Article

References (67)

1. Abdel-Mawgoud, A., Lepine, F., and Deziel, E. (2010) Rhamnolipids: diversity of structures, microbial origins and roles. Appl Microbiol Biotechnol 86: 1323-1336.
2. Abtin, A., Eckhart, L., Mildner, M., Gruber, F., Schröder, J.M., and Tschachler, E. (2008) Flagellin is the principal inducer of the antimicrobial peptide S100A7c (psoriasin) in human epidermal keratinocytes exposed to Escherichia coli. FASEB J 22: 2168-2176.
3. Adamo, R., Sokol, S., Soong, G., Gomez, M.I., and Prince, A. (2004) Pseudomonas aeruginosa flagella activate airway epithelial cells through asialoGM1 and toll-like receptor 2 as well as toll-like receptor 5. Am J Respir Cell Mol Biol 30: 627-634.
4. Al Tahhan, R.A., Sandrin, T.R., Bodour, A.A., and Maier, R.M. (2000) Rhamnolipid-induced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl Environ Microbiol 66: 3262-3268.
5. Bai, G., Brusseau, M.L., and Miller, M. (1998) Influence of cation type, ionic strength, and pH on solubilization and mobilization of residual hydrocarbon by a biosurfactant. J Contam Hydrol 30: 265-279.
6. Bardoel, B.W., van der Ent, S., Pel, M.J.C., Tommassen, J., Pieterse, C.M.J., van Kessel, K.P.M., and van Strijp, J.A.G. (2011) Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog 7: e1002206.
7. Bazzi, M.D., and Nelsestuen, G.L. (1987) Association of protein kinase C with phospholipid vesicles. Biochemistry 26: 115-122.
8. Beal, R., and Betts, W.B. (2000) Role of rhamnolipid biosurfactants in the uptake and mineralization of hexadecane in Pseudomonas aeruginosa. J Appl Microbiol 89: 158-168.
9. Benincasa, M., Abalos, A., Oliveira, I., and Manresa, A. (2004) Chemical structure, surface properties and biological activities of the biosurfactant produced by Pseudomonas aeruginosa LBI from soapstock. Antonie Van Leeuwenhoek 85: 1-8.
10. Bhavsar, A.P., Guttman, J.A., and Finlay, B.B. (2007) Manipulation of host-cell pathways by bacterial pathogens. Nature 449: 827-834.
11. Boles, B.R., Thoendel, M., and Singh, P.K. (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57: 1210-1223.
12. Briand, J.P., Muller, S., and Van Regenmortel, M.H.V. (1985) Synthetic peptides as antigens: pitfalls of conjugation methods. J Immunol Methods 78: 59-69.
13. Caiazza, N.C., Shanks, R.M.Q., and O'Toole, G.A. (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187: 7351-7361.
14. Chromek, M., Slamova, Z., Bergman, P., Kovacs, L., Podracka, L., Ehren, I., etal. (2006) The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med 12: 636-641.
15. Clapham, D.E. (2003) TRP channels as cellular sensors. Nature 426: 517-524.
16. Davey, M.E., Caiazza, N.C., and O'Toole, G.A. (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185: 1027-1036.
17. Deziel, E., Lepine, F., Milot, S., and Villemur, R. (2003) rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 149: 2005-2013.
18. Dolmetsch, R.E., Lewis, R.S., Goodnow, C.C., and Healy, J.I. (1997) Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386: 855-858.
19. Fu, Z., Bettega, K., Carroll, S., Buchholz, K.R., and Machen, T.E. (2007) Role of Ca2+ in responses of airway epithelia to Pseudomonas aeruginosa, flagellin, ATP, and thapsigargin. Am J Physiol Lung Cell Mol Physiol 292: L353-L364.
20. Fujita, K., Akino, T., and Yoshioka, H. (1988) Characteristics of heat-stable extracellular hemolysin from Pseudomonas aeruginosa. Infect Immun 56: 1385-1387.
21. Gerstel, U., Czapp, M., Bartels, J., and Schröder, J.M. (2009) Rhamnolipid-induced shedding of flagellin from Pseudomonas aeruginosa provokes hBD-2 and IL-8 response in human keratinocytes. Cell Microbiol 11: 842-853.
22. Haba, E., Pinazo, A., Jauregui, O., Espuny, M.J., Infante, M.R., and Manresa, A. (2003) Physicochemical characterization and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa 47T2 NCBIM 40044. Biotechnol Bioeng 81: 316-322.
23. Harder, J., Bartels, J., Christophers, E., and Schroder, J.M. (1997) A peptide antibiotic from human skin. Nature 387: 861.
24. Harder, J., Meyer-Hoffert, U., Teran, L.M., Schwichtenberg, L., Bartels, J., Maune, S., and Schroder, J.M. (2000) Mucoid Pseudomonas aeruginosa, TNF-alpha, and IL-1beta, but not IL-6, induce human beta-defensin-2 in respiratory epithelia. Am J Respir Cell Mol Biol 22: 714-721.
25. Harder, J., Meyer-Hoffert, U., Wehkamp, K., Schwichtenberg, L., and Schroder, J.M. (2004) Differential gene induction of human [beta]-defensins (hBD-1, -2, -3, and -4) in keratinocytes is inhibited by retinoic acid. J Invest Dermatol 123: 522-529.
26. Häussler, S. (2010) Multicellular signalling and growth of Pseudomonas aeruginosa. Int J Med Microbiol 300: 544-548.
27. Hornef, M.W., Wick, M.J., Rhen, M., and Normark, S. (2002) Bacterial strategies for overcoming host innate and adaptive immune responses. Nat Immunol 3: 1033-1040.
28. Howe, J., Bauer, J., Andrä, J., Schromm, A.B., Ernst, M., Rössle, M., etal. (2006) Biophysical characterization of synthetic rhamnolipids. Eur J Biochem 273: 5101-5112.
29. Ivison, S.M., Graham, N.R., Bernales, C.Q., Kifayet, A., Ng, N., Shobab, L.A., and Steiner, T.S. (2007) Protein kinase D interaction with TLR5 is required for inflammatory signaling in response to bacterial flagellin. J Immunol 178: 5735-5743.
30. Jang, B.C., Lim, K.J., Paik, J.H., Kwon, Y.K., Shin, S.W., Kim, S.C., etal. (2004) Up-regulation of human [beta]-defensin 2 by interleukin-1[beta] in A549 cells: involvement of PI3K, PKC, p38 MAPK, JNK, and NF-[kappa]B. Biochem Biophys Res Commun 320: 1026-1033.
31. Jensen, P.O., Bjarnsholt, T., Phipps, R., Rasmussen, T.B., Calum, H., Christoffersen, L., etal. (2007) Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology 153: 1329-1338.
32. Johnson, M.K., and Boese-Marrazzo, D. (1980) Production and properties of heat-stable extracellular hemolysin from Pseudomonas aeruginosa. Infect Immun 29: 1028-1033.
33. Kawai, T., and Akira, S. (2006) TLR signaling. Cell Death Differ 13: 816-825.
34. Kerr, K.G., and Snelling, A.M. (2009) Pseudomonas aeruginosa: a formidable and ever-present adversary. J Hosp Infect 73: 338-344.
35. Koch, A.K., Kappeli, O., Fiechter, A., and Reiser, J. (1991) Hydrocarbon assimilation and biosurfactant production in Pseudomonas aeruginosa mutants. J Bacteriol 173: 4212-4219.
36. Krisanaprakornkit, S., Kimball, J.R., and Dale, B.A. (2002) Regulation of human beta-defensin-2 in gingival epithelial cells: the involvement of mitogen-activated protein kinase pathways, but not the NF-kappaB transcription factor family. J Immunol 168: 316-324.
37. Kuang, Z., Hao, Y., Hwang, S., Zhang, S., Kim, E., Akinbi, H.T., etal. (2011) The Pseudomonas aeruginosa flagellum confers resistance to pulmonary surfactant protein-A by impacting the production of exoproteases through quorum-sensing. Mol Microbiol 79: 1220-1235.
38. McClure, C.D., and Schiller, N.L. (1992) Effects of Pseudomonas aeruginosa rhamnolipids on human monocyte-derived macrophages. J Leukoc Biol 51: 97-102.
39. McNamara, N., Gallup, M., Sucher, A., Maltseva, I., McKemy, D., and Basbaum, C. (2006) AsialoGM1 and TLR5 cooperate in flagellin-induced nucleotide signaling to activate Erk1/2. Am J Respir Cell Mol Biol 34: 653-660.
40. Meyer-Hoffert, U., Zimmermann, A., Czapp, M., Bartels, J., Koblyakova, Y., Gläser, R., etal. (2011) Flagellin delivery by Pseudomonas aeruginosa rhamnolipids induces the antimicrobial protein psoriasin in human skin. PLoS ONE 6: e16433.
41. Moser, C., Weiner, D.J., Lysenko, E., Bals, R., Weiser, J.N., and Wilson, J.M. (2002) beta-Defensin 1 contributes to pulmonary innate immunity in mice. Infect Immun 70: 3068-3072.
42. Newton, A.C. (1997) Regulation of protein kinase C. Curr Opin Cell Biol 9: 161-167.
43. Nizet, V., Ohtake, T., Lauth, X., Trowbridge, J., Rudisill, J., Dorschner, R.A., etal. (2001) Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414: 454-457.
44. Ochoa-Loza, F.F., Artiola, J.F., and Maier, R.M. (2001)Stability constants for the complexation of various metals with a rhamnolipid biosurfactant. J Environ Qual 30: 479-485.
45. Ogushi, K., Wada, A., Niidome, T., Mori, N., Oishi, K., Nagatake, T., etal. (2001) Salmonella enteritidis FliC (flagella filament protein) induces human beta-defensin-2 mRNA production by Caco-2 cells. J Biol Chem 276: 30521-30526.
46. Overhage, J., Lewenza, S., Marr, A.K., and Hancock, R.E.W. (2007) Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J Bacteriol 189: 2164-2169.
47. Parmely, M., Gale, A., Clabaugh, M., Horvat, R., and Zhou, W.W. (1990) Proteolytic inactivation of cytokines by Pseudomonas aeruginosa. Infect Immun 58: 3009-3014.
48. Pinzon, N., and Ju, L.K. (2009) Analysis of rhamnolipid biosurfactants by methylene blue complexation. Appl Microbiol Biotechnol 82: 975-981.
49. Ramos, H.C., Rumbo, M., and Sirard, J.C. (2004) Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 12: 509-517.
50. Ratner, A.J., Bryan, R., Weber, A., Nguyen, S., Barnes, D., Pitt, A., etal. (2001) Cystic fibrosis pathogens activate Ca2+-dependent mitogen-activated protein kinase signaling pathways in airway epithelial cells. J Biol Chem 276: 19267-19275.
51. Salzman, N.H., Hung, K., Haribhai, D., Chu, H., Karlsson-Sjoberg, J., Amir, E., etal. (2010) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11: 76-82.
52. Schlee, M., Wehkamp, J., Altenhoefer, A., Oelschlaeger, T.A., Stange, E.F., and Fellermann, K. (2007) Induction of human {beta}-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infect Immun 75: 2399-2407.
53. Sierra, G. (1960) Hemolytic effect of a glycolipid produced by Pseudomonas aeruginosa. Antonie Van Leeuwenhoek 26: 189-192.
54. Smith, R.S., and Iglewski, B.H. (2003) P.aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6: 56-60.
55. Stipcevic, T., Piljac, A., and Piljac, G. (2006) Enhanced healing of full-thickness burn wounds using di-rhamnolipid. Burns 32: 24-34.
56. Syldatk, C., Lang, S., Matulovic, U., and Wagner, F. (1985) Production of four interfacial active rhamnolipids from n-alkanes or glycerol by resting cells of Pseudomonas species DSM 2874. Z Naturforsch C 40: 61-67.
57. Tato, C.M., and Hunter, C.A. (2002) Host-pathogen interactions: subversion and utilization of the NF-{kappa}B pathway during infection. Infect Immun 70: 3311-3317.
58. TranVan Nhieu, G., Clair, C., Grompone, G., and Sansonetti, P. (2004) Calcium signalling during cell interactions with bacterial pathogens. Biol Cell 96: 93-101.
59. Van Gennip, M., Christensen, L.D., Alhede, M., Phipps, R., Jensen, P.O., Christophersen, L., etal. (2009) Inactivation of the rhlA gene in Pseudomonas aeruginosa prevents rhamnolipid production, disabling the protection against polymorphonuclear leukocytes. APMIS 117: 537-546.
60. Venturi, V. (2006) Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 30: 274-291.
61. Voss, E., Wehkamp, J., Wehkamp, K., Stange, E.F., Schroder, J.M., and Harder, J. (2006) NOD2/CARD15 mediates induction of the antimicrobial peptide human beta-defensin-2. J Biol Chem 281: 2005-2011.
62. Wang, Q., Downey, G.P., Choi, C., Kapus, A., and McCulloch, C.A. (2003) IL-1 induced release of Ca2+ from internal stores is dependent on cell-matrix interactions and regulates ERK activation. FASEB J 17: 1898-1900.
63. Wehkamp, K., Schwichtenberg, L., Schroder, J.M., and Harder, J. (2006) Pseudomonas aeruginosa- and IL-1beta-mediated induction of human beta-defensin-2 in keratinocytes is controlled by NF-kappaB and AP-1. J Invest Dermatol 126: 121-127.
64. Whitmarsh, A.J., and Davis, R.J. (1996) Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med (Berl) 74: 589-607.
65. Wiedow, O., Harder, J., Bartels, J., Streit, V., and Christophers, E. (1998) Antileukoprotease in human skin: an antibiotic peptide constitutively produced by keratinocytes. Biochem Biophys Res Commun 248: 904-909.
66. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms. Nature 415: 389-395.
67. Zulianello, L., Canard, C., Kohler, T., Caille, D., Lacroix, J.S., and Meda, P. (2006) Rhamnolipids are virulence factors that promote early infiltration of primary human airway epithelia by Pseudomonas aeruginosa. Infect Immun 74: 3134-3147.