1887

Abstract

Previous studies have demonstrated that PAO1 is chemotactic towards proteinogenic amino acids, however, the chemotaxis response of this strain towards non-proteinogenic amino acids and the specific chemoreceptors involved in this response are essentially unknown. In this study, we analysed the chemotactic response of PAO1 towards two degradation products of elastin, the lysine-rich, non-proteinogenic amino acids, desmosine and isodesmosine. We observed that isodesmosine, a potential biomarker for different diseases, served as a chemoattractant for PAO1. A screen of 251methyl-accepting chemotaxis proteins mutants of PAO1 identified PctA as the chemoreceptor for isodesmosine. We also showed that the positive chemotactic response to isodesmosine is potentially common by demonstrating chemoattraction in 12 of 15 diverse (in terms of source of isolation) clinical isolates, suggesting that the chemotactic response to this non-proteinogenic amino acid might be a conserved feature of acute infection isolates and thus could influence the colonization of potential infection sites.

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2015-07-01
2019-10-21
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References

  1. Adler J. . ( 1973;). A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli . J Gen Microbiol 74: 77–91 [CrossRef] [PubMed].
    [Google Scholar]
  2. Afdhal N.H. , Keaveny A.P. , Cohen S.B. , Nunes D.P. , Maldonado N. , O'Brien M. , Stone P.J. . ( 1997;). Urinary assays for desmosine and hydroxylysylpyridinoline in the detection of cirrhosis. J Hepatol 27: 993–1002 [CrossRef] [PubMed].
    [Google Scholar]
  3. Albarbarawi O. , Barton A. , Miller D. , McSharry C. , Chaudhuri R. , Thomson N.C. , Palmer C.N. , Devereux G. , Huang J.T.J. . ( 2013;). Characterization and validation of an isotope-dilution LC-MS/MS method for quantification of total desmosine and isodesmosine in plasma and serum. Bioanalysis 5: 1991–2001 [CrossRef] [PubMed].
    [Google Scholar]
  4. Alvarez-Ortega C. , Harwood C.S. . ( 2007;). Identification of a malate chemoreceptor in Pseudomonas aeruginosa by screening for chemotaxis defects in an energy taxis-deficient mutant. Appl Environ Microbiol 73: 7793–7795 [CrossRef] [PubMed].
    [Google Scholar]
  5. Amitani R. , Wilson R. , Rutman A. , Read R. , Ward C. , Burnett D. , Stockley R.A. , Cole P.J. . ( 1991;). Effects of human neutrophil elastase and Pseudomonas aeruginosa proteinases on human respiratory epithelium. Am J Respir Cell Mol Biol 4: 26–32 [CrossRef] [PubMed].
    [Google Scholar]
  6. Andonova M. , Urumova V. . ( 2013;). Immune surveillance mechanisms of the skin against the stealth infection strategy of Pseudomonas aeruginosa-review. Comp Immunol Microbiol Infect Dis 36: 433–448 [CrossRef] [PubMed].
    [Google Scholar]
  7. Azghani A.O. , Neal K. , Idell S. , Amaro R. , Baker J.W. , Omri A. , Pendurthi U.R. . ( 2014;). Mechanism of fibroblast inflammatory responses to Pseudomonas aeruginosa elastase. Microbiology 160: 547–555 [CrossRef] [PubMed].
    [Google Scholar]
  8. Ausubel F. , Brent R. , Kingston R.E. , Moore D.D. , Setdman J.G. , Smith J.A. , Struhl K. . ( 1993;). Current Protocols in Molecular Biology Part 1: E. coli, plasmids, and bacteriophages. New York; Wiley:.
    [Google Scholar]
  9. Barber R. , Primrose S. , Dodd G. . ( 1979;). Photoaffinity labelling of a tyrosine chemoreceptor in Pseudomonas aeruginosa . FEBS Lett 105: 43–46 [CrossRef] [PubMed].
    [Google Scholar]
  10. Bethesda M. . ( 2011;)., Cystic Fibrosis Foundation Patient Registry 2011. Annual Data Report.
  11. Boutin M. , Ahmad I. , Jauhiainen M. , Lachapelle N. , Rondeau C. , Roy J. , Thibault P. . ( 2009;). NanoLC-MS/MS analyses of urinary desmosine, hydroxylysylpyridinoline and lysylpyridinoline as biomarkers for chronic graft-versus-host disease. Anal Chem 81: 9454–9461 [CrossRef] [PubMed].
    [Google Scholar]
  12. Bruce M.C. , Poncz L. , Klinger J.D. , Stern R.C. , Tomashefski J.F. Jr , Dearborn D.G. . ( 1985;). Biochemical and pathologic evidence for proteolytic destruction of lung connective tissue in cystic fibrosis. Am Rev Respir Dis 132: 529–535 [PubMed].
    [Google Scholar]
  13. Craven R.C. , Montie T.C. . ( 1981;). Motility and chemotaxis of three strains of Pseudomonas aeruginosa used for virulence studies. Can J Microbiol 27: 458–460 [CrossRef] [PubMed].
    [Google Scholar]
  14. Craven R. , Montie T.C. . ( 1985;). Regulation of Pseudomonas aeruginosa chemotaxis by the nitrogen source. J Bacteriol 164: 544–549 [PubMed].
    [Google Scholar]
  15. Debelle L. , Tamburro A.M. . ( 1999;). Elastin: molecular description and function. Int J Biochem Cell Biol 31: 261–272 [CrossRef] [PubMed].
    [Google Scholar]
  16. Ferrari F. , Fumagalli M. , Piccinini P. , Stolk J. , Luisetti M. , Viglio S. , Tinelli C. , Iadarola P. . ( 2012;). Micellar electrokinetic chromatography with laser induced detection and liquid chromatography tandem mass-spectrometry-based desmosine assays in urine of patients with chronic obstructive pulmonary disease: a comparative analysis. J Chromatogr A 1266: 103–109 [CrossRef] [PubMed].
    [Google Scholar]
  17. Greenlee K.J. , Werb Z. , Kheradmand F. . ( 2007;). Matrix metalloproteinases in lung: multiple, multifarious, and multifaceted. Physiol Rev 87: 69–98 [CrossRef] [PubMed].
    [Google Scholar]
  18. Gu L. , Jones A.D. , Last R.L. , Rapid L.C-M.S./.M.S. . ( 2012;). profiling of protein amino acids and metabolically related compounds for large-scale assessment of metabolic phenotypes. Methods Mol Biol 828: 1–11 [CrossRef] [PubMed].
    [Google Scholar]
  19. Hamilton P.B. , Shelley G. . ( 1971;). Chemotactic response to amino acids by Pseudomonas aeruginosa in a semisolid nitrate medium. J Bacteriol 108: 596–598 [PubMed].
    [Google Scholar]
  20. Holloway B.W. , Krishnapillai V. , Morgan A.F. . ( 1979;). Chromosomal genetics of Pseudomonas . Microbiol Rev 43: 73–102 [PubMed].
    [Google Scholar]
  21. Hong C.S. , Shitashiro M. , Kuroda A. , Ikeda T. , Takiguchi N. , Ohtake H. , Kato J. . ( 2004;). Chemotaxis proteins and transducers for aerotaxis in Pseudomonas aeruginosa . FEMS Microbiol Lett 231: 247–252 [CrossRef] [PubMed].
    [Google Scholar]
  22. Huang J.T.J. , Chaudhuri R. , Albarbarawi O. , Barton A. , Grierson C. , Rauchhaus P. , Weir C.J. , Messow M. , Stevens N. , other authors . ( 2012;). Clinical validity of plasma and urinary desmosine as biomarkers for chronic obstructive pulmonary disease. Thorax 67: 502–508 [CrossRef] [PubMed].
    [Google Scholar]
  23. Jeong H.-H. , Lee S.-H. , Kim J.-M. , Kim H.-E. , Kim Y.-G. , Yoo J.Y. , Chang W.-S. , Lee C.-S. . ( 2010;). Microfluidic monitoring of Pseudomonas aeruginosa chemotaxis under the continuous chemical gradient. Biosens Bioelectron 26: 351–356 [CrossRef] [PubMed].
    [Google Scholar]
  24. Kaga N. , Soma S. , Fujimura T. , Seyama K. , Fukuchi Y. , Murayama K. . ( 2003;). Quantification of elastin cross-linking amino acids, desmosine and isodesmosine, in hydrolysates of rat lung by ion-pair liquid chromatography-mass spectrometry. Anal Biochem 318: 25–29 [CrossRef] [PubMed].
    [Google Scholar]
  25. Kim H.-E. , Shitashiro M. , Kuroda A. , Takiguchi N. , Ohtake H. , Kato J. . ( 2006;). Identification and characterization of the chemotactic transducer in Pseudomonas aeruginosa PAO1 for positive chemotaxis to trichloroethylene. J Bacteriol 188: 6700–6702 [CrossRef] [PubMed].
    [Google Scholar]
  26. Kim H.-E. , Shitashiro M. , Kuroda A. , Takiguchi N. , Kato J. . ( 2007;). Ethylene chemotaxis in Pseudomonas aeruginosa and other Pseudomonas species. Microbes Environ 22: 186–189 [CrossRef].
    [Google Scholar]
  27. Komori Y. , Sakai K. , Masuda K. , Nikai A.T. . ( 2011;). Isolation and biochemical characterization of rubelase, a non-hemorrhagic elastase from Crotalus ruber ruber (Red Rattlesnake) venom. Toxins (Basel) 3: 900–910 [CrossRef] [PubMed].
    [Google Scholar]
  28. Kuraki T. , Ishibashi M. , Takayama M. , Shiraishi M. , Yoshida M. . ( 2002;). A novel oral neutrophil elastase inhibitor (ONO-6818) inhibits human neutrophil elastase-induced emphysema in rats. Am J Respir Crit Care Med 166: 496–500 [CrossRef] [PubMed].
    [Google Scholar]
  29. Kuroda A. , Kumano T. , Taguchi K. , Nikata T. , Kato J. , Ohtake H. . ( 1995;). Molecular cloning and characterization of a chemotactic transducer gene in Pseudomonas aeruginosa . J Bacteriol 177: 7019–7025 [PubMed].
    [Google Scholar]
  30. Laguna T.A. , Wagner B.D. , Luckey H.K. , Mann S.A. , Sagel S.D. , Regelmann W. , Accurso F.J. . ( 2009;). Sputum desmosine during hospital admission for pulmonary exacerbation in cystic fibrosis. Chest 136: 1561–1568 [CrossRef] [PubMed].
    [Google Scholar]
  31. Laguna T.A. , Wagner B.D. , Starcher B. , Luckey Tarro H.K. , Mann S.A. , Sagel S.D. , Accurso F.J. . ( 2012;). Urinary desmosine: a biomarker of structural lung injury during CF pulmonary exacerbation. Pediatr Pulmonol 47: 856–863 [CrossRef] [PubMed].
    [Google Scholar]
  32. Lamerz J. , Friedlein A. , Soder N. , Cutler P. , Döbeli H. . ( 2013;). Determination of free desmosine in human plasma and its application in two experimental medicine studies. Anal Biochem 436: 127–136 [CrossRef] [PubMed].
    [Google Scholar]
  33. Ma S. , Lieberman S. , Turino G.M. , Lin Y.Y. . ( 2003;). The detection and quantitation of free desmosine and isodesmosine in human urine and their peptide-bound forms in sputum. Proc Natl Acad Sci U S A 100: 12941–12943 [CrossRef] [PubMed].
    [Google Scholar]
  34. Ma S. , Lin Y.Y. , Turino G.M. . ( 2007;). Measurements of desmosine and isodesmosine by mass spectrometry in COPD. Chest 131: 1363–1371 [CrossRef] [PubMed].
    [Google Scholar]
  35. Ma S. , Turino G.M. , Lin Y.Y. . ( 2011;). Quantitation of desmosine and isodesmosine in urine, plasma, and sputum by LC-MS/MS as biomarkers for elastin degradation. J Chromatogr B Analyt Technol Biomed Life Sci 879: 1893–1898 [CrossRef] [PubMed].
    [Google Scholar]
  36. Ma S. , Turino G.M. , Hayashi T. , Yanuma H. , Usuki T. , Lin Y.Y. . ( 2013;). Stable deuterium internal standard for the isotope-dilution LC-MS/MS analysis of elastin degradation. Anal Biochem 440: 158–165 [CrossRef] [PubMed].
    [Google Scholar]
  37. Miliotis T. , Lindberg C. , Semb K.F. , van Geest M. , Kjellström S. . ( 2013;). Quantitative high-performance liquid chromatography-tandem mass spectrometry method for the analysis of free desmosines in plasma and urine. J Chromatogr A 1308: 73–78 [CrossRef] [PubMed].
    [Google Scholar]
  38. Mithieux S.M. , Weiss A.S. . ( 2005;). Elastin. . In Fibrous Proteins: Coiled-coils, Collagen and Elastomers, pp. 437–461. Edited by Parry D. A. D. , Squire J. M. . 70 San Diego: Elsevier Academic;.[CrossRef]
    [Google Scholar]
  39. Munder A. , Wölbeling F. , Kerber-Momot T. , Wedekind D. , Baumann U. , Gulbins E. , Tümmler B. . ( 2011;). Acute intratracheal Pseudomonas aeruginosa infection in cystic fibrosis mice is age-independent. Respir Res 12: 148 [CrossRef] [PubMed].
    [Google Scholar]
  40. Murphy T.F. , Brauer A.L. , Eschberger K. , Lobbins P. , Grove L. , Cai X. , Sethi S. . ( 2008;). Pseudomonas aeruginosa in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 177: 853–860 [CrossRef] [PubMed].
    [Google Scholar]
  41. Ongay S. , Hendriks G. , Hermans J. , van den Berge M. , ten Hacken N.H.T. , van de Merbel N.C. , Bischoff R. . ( 2014;). Quantification of free and total desmosine and isodesmosine in human urine by liquid chromatography tandem mass spectrometry: a comparison of the surrogate-analyte and the surrogate-matrix approach for quantitation. J Chromatogr A 1326: 13–19 [CrossRef] [PubMed].
    [Google Scholar]
  42. Osakabe T. , Usami E. , Sato A. , Sasaki S. , Watanabe T. , Seyama Y. . ( 1999;). Characteristic change of urinary elastin peptides and desmosine in the aortic aneurysm. Biol Pharm Bull 22: 854–857 [CrossRef] [PubMed].
    [Google Scholar]
  43. Parales R.E. , Ditty J.L. , Harwood C.S. . ( 2000;). Toluene-degrading bacteria are chemotactic towards the environmental pollutants benzene, toluene, and trichloroethylene. Appl Environ Microbiol 66: 4098–4104 [CrossRef] [PubMed].
    [Google Scholar]
  44. Partridge S.M. , Elsden D.F. , Thomas J. . ( 1963;). Constitution of the cross-linkages in elastin. Nature 197: 1297–1298 [CrossRef] [PubMed].
    [Google Scholar]
  45. Rahme L.G. , Stevens E.J. , Wolfort S.F. , Shao J. , Tompkins R.G. , Ausubel F.M. . ( 1995;). Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899–1902 [CrossRef] [PubMed].
    [Google Scholar]
  46. Rico-Jiménez M. , Muñoz-Martínez F. , García-Fontana C. , Fernandez M. , Morel B. , Ortega A. , Ramos J.L. , Krell T. . ( 2013;). Paralogous chemoreceptors mediate chemotaxis towards protein amino acids and the non-protein amino acid gamma-aminobutyrate (GABA). Mol Microbiol 88: 1230–1243 [CrossRef] [PubMed].
    [Google Scholar]
  47. Rosenbloom J. , Abrams W.R. , Mecham R. . ( 1993;). Extracellular matrix 4: the elastic fiber. FASEB J 7: 1208–1218 [PubMed].
    [Google Scholar]
  48. Sampedro I. , Parales R.E. , Krell T. , Hill J.E. . ( 2014;). Pseudomonas chemotaxis. FEMS Microbiol Rev [CrossRef].
    [Google Scholar]
  49. Schweizer H.P. . ( 1991;). Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene 97 97: 109–112 [CrossRef] [PubMed].
    [Google Scholar]
  50. Shitashiro M. , Tanaka H. , Hong C.S. , Kuroda A. , Takiguchi N. , Ohtake H. , Kato J. . ( 2005;). Identification of chemosensory proteins for trichloroethylene in Pseudomonas aeruginosa . J Biosci Bioeng 99: 396–402 [CrossRef] [PubMed].
    [Google Scholar]
  51. Sly L.M. , Worobec E.A. , Perkins R.E. , Phibbs P.V. Jr . ( 1993;). Jr Reconstitution of glucose uptake and chemotaxis in Pseudomonas aeruginosa glucose transport defective mutants. Can J Microbiol 39: 1079–1083 [CrossRef] [PubMed].
    [Google Scholar]
  52. Stanier R.Y. , Palleroni N.J. , Doudoroff M. . ( 1966;). The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43: 159–271 [CrossRef] [PubMed].
    [Google Scholar]
  53. Stinson M.W. , Cohen M.A. , Merrick J.M. . ( 1977;). Purification and properties of the periplasmic glucose-binding protein of Pseudomonas aeruginosa . J Bacteriol 131: 672–681 [PubMed].
    [Google Scholar]
  54. Stockley R.A. . ( 2002;). Neutrophils and the pathogenesis of COPD. Chest 121: 151S–155S [CrossRef] [PubMed].
    [Google Scholar]
  55. Taguchi K. , Fukutomi H. , Kuroda A. , Kato J. , Ohtake H. . ( 1997;). Genetic identification of chemotactic transducers for amino acids in Pseudomonas aeruginosa . Microbiology 143: 3223–3229 [CrossRef] [PubMed].
    [Google Scholar]
  56. Thomas J. , Elsden D.F. , Partridge S.M. . ( 1963;). Partial structure of 2 major degradation products from cross-linkages in elastin. Nature 200: 651–652 [CrossRef] [PubMed].
    [Google Scholar]
  57. Turkay C. , Saba R. , Sahin N. , Altunbas H. , Ozbudak O. , Akkaya B. , Ozbilim G. , Cölbasi I. , Turkay M. , other authors . ( 2004;). Effect of chronic Pseudomonas aeruginosa infection on the development of atherosclerosis in a rat model. Clin Microbiol Infect 10: 705–708 [CrossRef] [PubMed].
    [Google Scholar]
  58. Umeda H. , Aikawa M. , Libby P. . ( 2011;). Liberation of desmosine and isodesmosine as amino acids from insoluble elastin by elastolytic proteases. Biochem Biophys Res Commun 411: 281–286 [CrossRef] [PubMed].
    [Google Scholar]
  59. Urbán Z. , Boyd C.D. . ( 2000;). Elastic-fiber pathologies: primary defects in assembly-and secondary disorders in transport and delivery. Am J Hum Genet 67: 4–7 [CrossRef] [PubMed].
    [Google Scholar]
  60. Usuki T. , Sugimura T. , Komatsu A. , Koseki Y. . ( 2014;). Biomimetic Chichibabin pyridine synthesis of the COPD biomarkers and elastin cross-linkers isodesmosine and desmosine. Org Lett 16: 1672–1675 [CrossRef] [PubMed].
    [Google Scholar]
  61. Wolfgang M.C. , Kulasekara B.R. , Liang X. , Boyd D. , Wu K. , Yang Q. , Miyada C.G. , Lory S. . ( 2003;). Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa . Proc Natl Acad Sci U S A 100: 8484–8489 [CrossRef] [PubMed].
    [Google Scholar]
  62. Wright J.L. , Farmer S.G. , Churg A. . ( 2002;). Synthetic serine elastase inhibitor reduces cigarette smoke-induced emphysema in guinea pigs. Am J Respir Crit Care Med 166: 954–960 [CrossRef] [PubMed].
    [Google Scholar]
  63. Wu H. , Kato J. , Kuroda A. , Ikeda T. , Takiguchi N. , Ohtake H. . ( 2000;). Identification and characterization of two chemotactic transducers for inorganic phosphate in Pseudomonas aeruginosa . J Bacteriol 182: 3400–3404 [CrossRef] [PubMed].
    [Google Scholar]
  64. Yoo D.G. , Floyd M. , Winn M. , Moskowitz S.M. , Rada B. . ( 2014;). NET formation induced by Pseudomonas aeruginosa cystic fibrosis isolates measured as release of myeloperoxidase-DNA and neutrophil elastase-DNA complexes. Immunol Lett 160: 186–194 [CrossRef] [PubMed].
    [Google Scholar]
  65. Zegans M.E. , Wozniak D. , Griffin E. , Toutain-Kidd C.M. , Hammond J.H. , Garfoot A. , Lam J.S. . ( 2012;). Pseudomonas aeruginosa exopolysaccharide Psl promotes resistance to the biofilm inhibitor polysorbate 80. Antimicrob Agents Chemother 56: 4112–4122 [CrossRef] [PubMed].
    [Google Scholar]
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