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Volume 161, Issue 7

Elastin degradation product isodesmosine is a chemoattractant for Free

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 The Authors
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2015-07-01
2024-04-24
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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 7477–91 [View Article][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 cirrhosisJ Hepatol 27993–1002 [View Article][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 serumBioanalysis 51991–2001 [View Article][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 mutantAppl Environ Microbiol 737793–7795 [View Article][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 epitheliumAm J Respir Cell Mol Biol 426–32 [View Article][PubMed]. [Google Scholar]
  6. Andonova M., Urumova V. (2013). Immune surveillance mechanisms of the skin against the stealth infection strategy of Pseudomonas aeruginosa-reviewComp Immunol Microbiol Infect Dis 36433–448 [View Article][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 elastaseMicrobiology 160547–555 [View Article][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 BiologyPart 1: E. coli, plasmids, and bacteriophages.New YorkWiley. [Google Scholar]
  9. Barber R., Primrose S., Dodd G. (1979). Photoaffinity labelling of a tyrosine chemoreceptor in Pseudomonas aeruginosa FEBS Lett 10543–46 [View Article][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 diseaseAnal Chem 819454–9461 [View Article][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 fibrosisAm Rev Respir Dis 132529–535[PubMed]. [Google Scholar]
  13. Craven R.C., Montie T.C. (1981). Motility and chemotaxis of three strains of Pseudomonas aeruginosa used for virulence studiesCan J Microbiol 27458–460 [View Article][PubMed]. [Google Scholar]
  14. Craven R., Montie T.C. (1985). Regulation of Pseudomonas aeruginosa chemotaxis by the nitrogen sourceJ Bacteriol 164544–549[PubMed]. [Google Scholar]
  15. Debelle L., Tamburro A.M. (1999). Elastin: molecular description and functionInt J Biochem Cell Biol 31261–272 [View Article][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 analysisJ Chromatogr A 1266103–109 [View Article][PubMed]. [Google Scholar]
  17. Greenlee K.J., Werb Z., Kheradmand F. (2007). Matrix metalloproteinases in lung: multiple, multifarious, and multifacetedPhysiol Rev 8769–98 [View Article][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 phenotypesMethods Mol Biol 8281–11 [View Article][PubMed]. [Google Scholar]
  19. Hamilton P.B., Shelley G. (1971). Chemotactic response to amino acids by Pseudomonas aeruginosa in a semisolid nitrate mediumJ Bacteriol 108596–598[PubMed]. [Google Scholar]
  20. Holloway B.W., Krishnapillai V., Morgan A.F. (1979). Chromosomal genetics of Pseudomonas Microbiol Rev 4373–102[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 231247–252 [View Article][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 diseaseThorax 67502–508 [View Article][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 gradientBiosens Bioelectron 26351–356 [View Article][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 spectrometryAnal Biochem 31825–29 [View Article][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 trichloroethyleneJ Bacteriol 1886700–6702 [View Article][PubMed]. [Google Scholar]
  26. Kim H.-E., Shitashiro M., Kuroda A., Takiguchi N., Kato J. (2007). Ethylene chemotaxis in Pseudomonas aeruginosa and other Pseudomonas speciesMicrobes Environ 22186–189 [View Article]. [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) venomToxins (Basel) 3900–910 [View Article][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 ratsAm J Respir Crit Care Med 166496–500 [View Article][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 1777019–7025[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 fibrosisChest 1361561–1568 [View Article][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 exacerbationPediatr Pulmonol 47856–863 [View Article][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 studiesAnal Biochem 436127–136 [View Article][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 sputumProc Natl Acad Sci U S A 10012941–12943 [View Article][PubMed]. [Google Scholar]
  34. Ma S., Lin Y.Y., Turino G.M. (2007). Measurements of desmosine and isodesmosine by mass spectrometry in COPDChest 1311363–1371 [View Article][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 degradationJ Chromatogr B Analyt Technol Biomed Life Sci 8791893–1898 [View Article][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 degradationAnal Biochem 440158–165 [View Article][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 urineJ Chromatogr A 130873–78 [View Article][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. 70San DiegoElsevier 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-independentRespir Res 12148 [View Article][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 diseaseAm J Respir Crit Care Med 177853–860 [View Article][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 quantitationJ Chromatogr A 132613–19 [View Article][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 aneurysmBiol Pharm Bull 22854–857 [View Article][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 trichloroethyleneAppl Environ Microbiol 664098–4104 [View Article][PubMed]. [Google Scholar]
  44. Partridge S.M., Elsden D.F., Thomas J. (1963). Constitution of the cross-linkages in elastinNature 1971297–1298 [View Article][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 animalsScience 2681899–1902 [View Article][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 881230–1243 [View Article][PubMed]. [Google Scholar]
  47. Rosenbloom J., Abrams W.R., Mecham R. (1993). Extracellular matrix 4: the elastic fiberFASEB J 71208–1218[PubMed]. [Google Scholar]
  48. Sampedro I., Parales R.E., Krell T., Hill J.E. (2014). Pseudomonas chemotaxisFEMS MicrobiolRev [View Article]. [Google Scholar]
  49. Schweizer H.P. (1991). Escherichia-Pseudomonas shuttle vectors derived from pUC18/19Gene 97 97109–112 [View Article][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 99396–402 [View Article][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 mutantsCan J Microbiol 391079–1083 [View Article][PubMed]. [Google Scholar]
  52. Stanier R.Y., Palleroni N.J., Doudoroff M. (1966). The aerobic pseudomonads: a taxonomic studyJ Gen Microbiol 43159–271 [View Article][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 131672–681[PubMed]. [Google Scholar]
  54. Stockley R.A. (2002). Neutrophils and the pathogenesis of COPDChest 121151S–155S [View Article][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 1433223–3229 [View Article][PubMed]. [Google Scholar]
  56. Thomas J., Elsden D.F., Partridge S.M. (1963). Partial structure of 2 major degradation products from cross-linkages in elastinNature 200651–652 [View Article][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 modelClin Microbiol Infect 10705–708 [View Article][PubMed]. [Google Scholar]
  58. Umeda H., Aikawa M., Libby P. (2011). Liberation of desmosine and isodesmosine as amino acids from insoluble elastin by elastolytic proteasesBiochem Biophys Res Commun 411281–286 [View Article][PubMed]. [Google Scholar]
  59. Urbán Z., Boyd C.D. (2000). Elastic-fiber pathologies: primary defects in assembly-and secondary disorders in transport and deliveryAm J Hum Genet 674–7 [View Article][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 desmosineOrg Lett 161672–1675 [View Article][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 1008484–8489 [View Article][PubMed]. [Google Scholar]
  62. Wright J.L., Farmer S.G., Churg A. (2002). Synthetic serine elastase inhibitor reduces cigarette smoke-induced emphysema in guinea pigsAm J Respir Crit Care Med 166954–960 [View Article][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 1823400–3404 [View Article][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 complexesImmunol Lett 160186–194 [View Article][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 80Antimicrob Agents Chemother 564112–4122 [View Article][PubMed]. [Google Scholar]
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Elastin degradation product isodesmosine is a chemoattractant for Pseudomonas aeruginosa
Microbiology 161, 1496 (2015); https://doi.org/10.1099/mic.0.000090
/content/journal/micro/10.1099/mic.0.000090
/content/journal/micro/10.1099/mic.0.000090
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