Host derived inflammatory phospholipids regulate rahU (PA0122) Gene, Protein, and Biofilm Formation in Pseudomonas aeruginosa

Cellular Immunology

Volumn 270, Issue 2, 2011, Pages 95-102

  Rao, Jayasimha ^a,d   DiGiandomenico, Antonio ^d   Artamonov, Mykhaylo ^d   Leitinger, Norbert ^d   Amin, Ashok R ^a,b,c   Goldberg, Joanna B ^d  

^a VIRGINIA TECH CARILION SCHOOL OF MEDICINE   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c WAKE FOREST UNIVERSITY   (United States)

^d UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

Biofilm; Gene expression; Inflammation; Phospholipids; Pseudomonas

Indexed keywords

ARACHIDONIC ACID; BACTERIAL PROTEIN; BACTERIAL VECTOR; BETA GALACTOSIDASE; HOST FACTOR; LYSOPHOSPHATIDYLCHOLINE; OXIDIZED 1 PAMITOYL 2 ARACHIDONOYL SN PHOSPHATIDYLCHOLINE; PHOSPHOLIPASE A2; PHOSPHOLIPID; RAHU PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOFILM; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; INFLAMMATION; INHIBITION KINETICS; LIPID OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PSEUDOMONAS AERUGINOSA; THIN LAYER CHROMATOGRAPHY; WESTERN BLOTTING;

BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION MEDIATORS; MODELS, BIOLOGICAL; MUTATION; OXIDATION-REDUCTION; PHOSPHOLIPIDS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS;

EUKARYOTA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 80051670008     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2011.04.011     Document Type: Article

References (57)

1. Kumagai Y. Pathogen recognition by innate receptors. Infect. Chemother. 2008, 14:86-92.
2. Ishii K.J., Koyama S., Nakagawa A., Coban C., Akira S. Host innate immune receptors and beyond: making sense of microbial infections. Cell Host Microbe 2008, 12:352-363.
3. Kobayashi S.D., Voyich J.M., Burlak C., DeLeo F.R. Neutrophils in the innate immune response. Arch. Immunol. Ther. Exp. 2005, 53:505-517.
4. Machen T.E. Innate immune response in CF airway epithelia: hyperinflammatory?. Am. J. Physiol. Cell. Physiol. 2006, 291:218-230.
5. Netea M.G., Kullberg B.J., Van der Meer J.W. Proinflammatory cytokines in the treatment of bacterial and fungal infections. BioDrugs 2004, 18:9-22.
6. Lawrence T., Willoughby D.A., Gilroy D.W. Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat. Rev. Immunol. 2002, 2:787-795.
7. Serhan C.N., Yacoubian S., Yang R. Anti-inflammatory and proresolving lipid mediators. Annu. Rev. Pathol. 2008, 3:279-312.
8. Leitinger N. Oxidized phospholipids as triggers of inflammation in atherosclerosis. Mol. Nutr. Food Res. 2005, 49:1063-1071.
9. Cole A.L., Subbanagounder G., Mukhopadhyay S., Berliner J.A., Vora D.K. Oxidized phospholipid-induced endothelial cell/monocyte interaction is mediated by a cAMP-dependent R-Ras/PI3-kinase pathway. Arterioscler., Thromb., Vasc. Biol. 2003, 1:1384-1390.
10. Bochkov V.N., Kadl A., Huber J., Gruber F., Binder B.R., Leitinger N. Protective role of phospholipid oxidation products in endotoxin-induced tissue damage. Nature 2002, 419:77-81.
11. Nonas S., Miller I., Kawkitinarong K., Chatchavalvanich S., Gorshkova I., Bochkov V.N., Leitinger N., Natarajan V., Garcia J.G.N., Birukov K.G. Oxidized phospholipids reduce vascular leak and Inflammation in rat model of acute lung injury. Am. J. Respir. Crit. Care Med. 2006, pp 200511-1737OC.
12. Birukov K.G., Leitinger N., Bochkov V.N., Garcia J.G. Signal transduction pathways activated in human pulmonary endothelial cells by OxPAPC, a bioactive component of oxidized lipoproteins. Microvasc. Res. 2004, 67(1):18-28.
13. Hall-Stoodley L., Stoodley P. Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol. 2005, 13(1):7-10.
14. Son M.S., Matthews W.J., Kang Y., Nguyen D.T., Hoang T.T. in vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect. Immun. 2007, 75:5313-5324.
15. Miller R.M., Tomaras A.P., Barker A.P., Voelker D.R., Chan E.D., Vasil A.I., Vasil M.L. Pseudomonas aeruginosa twitching motility-mediated chemotaxis towards phospholipids and fatty acids: specificity and metabolic requirements. J. Bacteriol. 2008, 190:4038-4049.
16. Sadikot R.T., Blackwell T.S., Christman J.W., Prince A.S. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am. J. Respir. Crit. Care Med. 2005, 171:1209-1223.
17. Davies J.C. Pseudomonas aeruginosa in cystic fibrosis: pathogenesis and persistence. Paediatr. Respir. Rev. 2002, 3:128-134.
18. Parsek M.R., Matthew R., K Singh P. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 2003, 57(677):701.
19. Kirov S.M., Webb J.S., O'May C.Y., Reid D.W., Woo J.K.K., Rice S.A., Kjelleberg S. Biofilm differentiation and dispersal in mucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 2007, 153:3264-3274.
20. Mikkelsen H., Duck Z., Lilley K.S., Welch M. Interrelationships between colonies, biofilms, and planktonic cells of Pseudomonas aeruginosa. J. Bacteriol. 2007, 189:2411-2416.
21. Wagner V.E., Iglewski B.H. P. aeruginosa biofilms in CF infection. Clin. Rev. Allergy Immunol. 2008, 35(3):124-134.
22. Landry R.M., An D., Hupp J.T., Singh P.K., Parsek M.R. Mucin-Pseudomonas aeruginosa interactions promote biofilm formation and antibiotic resistance. Mol. Microbiol. 2006, 59(1):142-151.
23. Hentzer M., Teitzel G.M., Balzer G.J., Heydorn A., Molin S., Givskov M., Parsek M.R. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J. Bacteriol. 2001, 183(5395):5401.
24. Hanna S.L., Sherman N.E., Kinter M.T., Goldberg J.B. Comparison of proteins expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatography-tandem mass spectrometry. Microbiology 2000, 146:2495-2508.
25. Rao J., DiGiandomenico A., Unger J., Bao Y., Polanowska-Grabowska R.K., Goldberg J.B. A novel oxidized low-density lipoprotein-binding protein from Pseudomonas aeruginosa. Microbiology 2008, 154:654-665.
26. Kumagai T., Tsutsumi H., Ogawa N., Naito S., Ebina K., Yokota K., Nagata K. Oxidized low-density lipoprotein-binding specificity of the Asp-hemolysin-related synthetic peptides from Aspergillus fumigatus. Biol. Pharm. Bull. 2006, 29(11):2181-2186.
27. Kudo Y., Ootani T., Kumagai T., Fukuchi Y., Ebin K., Yokota K. A novel oxidized low-density lipoprotein-binding protein, Asp-hemolysin, recognizes lysophosphatidylcholine. Biol. Pharm. Bull. 2002, 25(6):787-790.
28. Marchler-Bauer A., Bryant S.H. CD-search: protein domain annotations on the fly. Nucleic Acids Res. 2004, 32(Web Server issue):W327-31.
29. Watson A.D., Leitinger N., Navab M., Faull K.F., Horkko S., Witztum J.L., Palinski W., Schwenke D., Salomon R.G., Sha W., Subbanagounder G., Fogelman A.M., Berliner J.A. Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/endothelial interactions and evidence for their presence in vivo. J. Biol. Chem. 1997, 272:13597-13607.
30. Schweizer H.P. Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker. Mol. Microbiol. 1992, 6(9):1195-1204.
31. Schweizer H.P., Hoang T.T. An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 1995, 158:15-22.
32. Hoang T.T., Karkhoff-Schweizer R.R., Kutchma A.J., Schweizer H.P. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 1998, 212:77-86.
33. Becher A., Schweizer H.P. Integration-proficient Pseudomonas aeruginosa vectors for isolation of single-copy chromosomal lacZ and lux gene fusions. BioTechniques 2000, 29. pp. 948-50, 952.
34. Miller J.H. Experiments in Molecular Genetics 1972, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. Watson A.D., Subbanagounder G., Welsbie D.S., Faull K.F., Navab M., Jung M.E., Fogelman A.M., Berliner J.A. Structural identification of a novel pro-inflammatory epoxyisoprostane phospholipid in mildly oxidized low density lipoprotein. J. Biol. Chem. 1999, 274:24787-24798.
36. Bochkov V.N., Mechtcheriakova D., Lucerna M., Huber J., Malli R., Graier W.F., Hofer E., Binder B.R., Leitinger N. Oxidized phospholipids stimulate tissue factor expression in human endothelial cells via activation of ERK/EGR-1 and Ca(++)/NFAT. Blood 2002, 99:199-206.
37. Gruber F., Oskolkova O., Leitner A., Mildner M., Mlitz V., Lengauer B., Kadl A., Mrass P., Kronke G., Binder B.R., Bochkov V.N., Leitinger N., Tschachler E. Photooxidation generates biologically active phospholipids that induce heme oxygenase-1 in skin cells. J. Biol. Chem. 2007, 282:16934-16941.
38. O'Toole G., Kaplan H.B., Kolter R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 2000, 54:49-79.
39. Fisher R.A. Statistical Methods for Research Workers 1932, Oliver and Boyd, London.
40. Wagner V.E., Bushnell D., Passador L., Brooks A.I., Iglewski B.H. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 2003, 185(7):2080-2095.
41. Leitinger N., Tyner T.R., Oslund L., Rizza C., Subbanagounder G., Lee H., Shih P.T., Mackman N., Tigyi G., Territo M.C., Berliner J.A., Vora D.K. Structurally similar oxidized phospholipids differentially regulate endothelial binding of monocytes and neutrophils. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(21):12010-12015.
42. Leitinger N. Oxidized phospholipids as modulators of inflammation in atherosclerosis. Curr. Opin. Lipidol. 2003, 14:421-430.
43. Han K.H., Hong K.H., Ko J., Rhee K.S., Hong M.K., Kim J.J., Kim Y.H., Park S.J. Lysophosphatidylcholine up-regulates CXCR4 chemokine receptor expression in human CD4 T cells. J. Leukoc. Biol. 2004, 76:195-202.
44. Sakai M., Miyazaki A., Hakamata H., Sato Y., Matsumura T., Kobori S., Shichiri M., Horiuchi S. Lysophosphatidylcholine potentiates the mitogenic activity of modified ldl for human monocyte derived macrophages. Arterioscler. Thromb. Vasc. Biol. 1996, 16:600-605.
45. Kreuzer J., Denger S., Jahn L., Bader J., Ritter K., von Hodenberg E., Kubler W. Ldl stimulates chemotaxis of human monocytes through a cyclooxygenase-dependent pathway. Arterioscler. Thromb. Vasc. Biol. 1996, 16:1481-1487.
46. Panjwani N., Zhao Z., Raizman M.B., Jungalwala F. Pathogenesis of corneal infection: binding of Pseudomonas aeruginosa to specific phospholipids. Infect. Immun. 1996, 64:1819-1825.
47. Laux D.C., Corson J.M., Givskov M., Hentzer M., Moller A., Wosencroft K.A., Olson J.C., Krogfelt K.A., Goldberg J.B., Cohen P.S. Lysophosphatidic acid inhibition of the accumulation of Pseudomonas aeruginosa PAO1 alginate, pyoverdin, elastase and LasA. Microbiology 2002, 148:1709-1723.
48. Wu L., Estrada O., Zaborina O., Bains M., Shen L., Kohler J.E., Patel N., Musch M.W., Chang E.B., Fu Y.X., Jacobs M.A., Nishimura M.I., Hancock R.E.W., Turner J.R., Alverdy J.C. Recognition of host immune activation by Pseudomonas aeruginosa. Science 2005, 309:774-777.
49. Subramanian N., Qadri A. Lysophospholipid sensing triggers secretion of flagellin from pathogenic salmonella. Nat. Immunol. 2006, 7:583-589.
50. Livermore D.M., Struelens M., Amorim J., Baquero F., Bille J., Canton R., Henning S., Gatermann S., Marchese A., Mittermayer H., Nonhoff C., Oakton K.J., Praplan F., Ramos H., Schito G.C., Van Eldere J., Verhaegen J., Verhoef J., Visser M.R. Multicentre evaluation of the VITEK 2 advanced expert system for interpretive reading of antimicrobial resistance tests. J. Antimicrob. Chemother. 2002, 49:289-300.
51. Al Aloul M., Crawley J., Winstanley C., Hart C.A., Ledson M.J., Walshaw M.J. Increased morbidity associated with chronic infection by an epidemic Pseudomonas aeruginosa strain in CF patients. Thorax 2004, 59:334-336.
52. Bodey G.P., Bolivar R., Fainstein V., Jadeja L. Infections caused by Pseudomonas aeruginosa. Rev. Infect. Dis. 1983, 5(2):279-313.
53. Hentzer M., Eberl L., Nielsen J., Givskov M. Quorum sensing: a novel target for the treatment of biofilm infections. BioDrugs 2003, 17(4):241-250.
54. Koh, Priebe G.P., Ray C., Van Rooijen N., Pier G.B. Inescapable need for neutrophils as mediators of cellular innate immunity to acute Pseudomonas aeruginosa pneumonia. Infect. Immun. 2009, 77:5300-5310.
55. 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. 2001, 69(3):1895-1901.
56. van Golde L.M. Potential role of surfactant proteins A and D in innate lung defense against pathogens. Biol. Neonate 1995, 67:2-17.
57. Wu L., Estrada O., Zaborina O., Bains M., Shen L., Kohler J.E., Patel N., Musch M.W., Chang E.B., Fu Y.X., Jacobs M.A., Nishimura M.I., Hancock R.E.W., Turner J.R., Alverdy J.C. Recognition of host immune activation by Pseudomonas aeruginosa. Science 2005, 309:774-777.