ChIP-Seq and RNA-Seq Reveal an AmrZ-Mediated Mechanism for Cyclic di-GMP Synthesis and Biofilm Development by
Pathogenic bacteria such as Pseudomonas aeruginosa utilize a wide variety of systems to sense and respond to the changing conditions during an infection. When a stress is sensed, signals are transmitted to impact expression of many genes that allow the bacterium to adapt to the changing conditions. AmrZ is a protein that regulates production of several virulence-associated gene products, though we predicted that its role in virulence was more expansive than previously described. Transcription factors such as AmrZ often affect the expression of a gene by binding and promoting or inhibiting expression of the target gene. Two global techniques were utilized to determine where AmrZ binds in the genome, and what effect AmrZ has once bound. This approach revealed that AmrZ represses the production of a signaling molecule called cyclic diguanylate, which is known to induce the formation of difficult to treat communities of bacteria called biofilms. This study also identified many novel targets of AmrZ to promote future studies of this regulator. Collectively, these data can be utilized to develop treatments to inhibit biofilm formation during devastating chronic infections.
Vyšlo v časopise:
ChIP-Seq and RNA-Seq Reveal an AmrZ-Mediated Mechanism for Cyclic di-GMP Synthesis and Biofilm Development by. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003984
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1003984
Souhrn
Pathogenic bacteria such as Pseudomonas aeruginosa utilize a wide variety of systems to sense and respond to the changing conditions during an infection. When a stress is sensed, signals are transmitted to impact expression of many genes that allow the bacterium to adapt to the changing conditions. AmrZ is a protein that regulates production of several virulence-associated gene products, though we predicted that its role in virulence was more expansive than previously described. Transcription factors such as AmrZ often affect the expression of a gene by binding and promoting or inhibiting expression of the target gene. Two global techniques were utilized to determine where AmrZ binds in the genome, and what effect AmrZ has once bound. This approach revealed that AmrZ represses the production of a signaling molecule called cyclic diguanylate, which is known to induce the formation of difficult to treat communities of bacteria called biofilms. This study also identified many novel targets of AmrZ to promote future studies of this regulator. Collectively, these data can be utilized to develop treatments to inhibit biofilm formation during devastating chronic infections.
Zdroje
1. WisplinghoffH, BischoffT, TallentSM, SeifertH, WenzelRP, et al. (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39: 309–317 doi:10.1086/421946
2. RichardsMJ, EdwardsJR, CulverDH, GaynesRP (1999) Nosocomial infections in medical intensive care units in the United States. Crit Care Med 27: 887.
3. Hall-StoodleyL, CostertonJW, StoodleyP (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2: 95–108 doi:10.1038/nrmicro821
4. TartAH, WozniakDJ (2008) Shifting paradigms in Pseudomonas aeruginosa biofilm research. Curr Top Microbiol Immunol 322: 193–206.
5. EvansDJ, BrownMRW, AllisonDG, GilbertP (1990) Susceptibility of bacterial biofilms to tobramycin: role of specific growth rate and phase in the division cycle. J Antimicrob Chemother 25: 585–591 doi:10.1093/jac/25.4.585
6. HentzerM, TeitzelGM, BalzerGJ, HeydornA, MolinS, et al. (2001) Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 183: 5395–5401.
7. AlkawashMA, SoothillJS, SchillerNL (2006) Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. APMIS 114: 131–138 doi:_10.1111/j.1600-0463.2006.apm_356.x
8. DaviesDG, ParsekMR, PearsonJP, IglewskiBH, CostertonJW, et al. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295–298.
9. O'TooleGA, KolterR (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28: 449–461.
10. WebbJS, ThompsonLS, JamesS, CharltonT, Tolker-NielsenT, et al. (2003) Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol 185: 4585–4592.
11. ShroutJD, ChoppDL, JustCL, HentzerM, GivskovM, et al. (2006) The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol Microbiol 62: 1264–1277 doi:10.1111/j.1365-2958.2006.05421.x
12. O'TooleGA, KolterR (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295–304.
13. WorlitzschD, TarranR, UlrichM, SchwabU, CekiciA, et al. (2002) Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109: 317–325 doi:10.1172/JCI13870
14. HassettDJ, SuttonMD, SchurrMJ, HerrAB, CaldwellCC, et al. (2009) Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol 17: 130–138 doi:10.1016/j.tim.2008.12.003
15. DrenkardE, AusubelFM (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740–743 doi:10.1038/416740a
16. LeidJG, WillsonCJ, ShirtliffME, HassettDJ, ParsekMR, et al. (2005) The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J Immunol 175: 7512–7518.
17. NguyenD, Joshi-DatarA, LepineF, BauerleE, OlakanmiO, et al. (2011) Active Starvation Responses Mediate Antibiotic Tolerance in Biofilms and Nutrient-Limited Bacteria. Science 334: 982–986 doi:10.1126/science.1211037
18. WaligoraEA, RamseyDM, PryorEE, LuH, HollisT, et al. (2010) AmrZ beta-sheet residues are essential for DNA binding and transcriptional control of Pseudomonas aeruginosa virulence genes. J Bacteriol 192: 5390–5401 doi:10.1128/JB.00711-10
19. JonesCJ, RyderCR, MannEE, WozniakDJ (2013) AmrZ modulates Pseudomonas aeruginosa biofilm architecture by directly repressing transcription of the psl operon. J Bacteriol 195: 1637–1644 doi:10.1128/JB.02190-12
20. TartAH, WolfgangMC, WozniakDJ (2005) The alternative sigma factor AlgT represses Pseudomonas aeruginosa flagellum biosynthesis by inhibiting expression of fleQ. J Bacteriol 187: 7955–7962 doi:10.1128/JB.187.23.7955-7962.2005
21. TartAH, BlanksMJ, WozniakDJ (2006) The AlgT-dependent transcriptional regulator AmrZ (AlgZ) inhibits flagellum biosynthesis in mucoid, nonmotile Pseudomonas aeruginosa cystic fibrosis isolates. J Bacteriol 188: 6483–6489 doi:10.1128/JB.00636-06
22. RamseyDM, BaynhamPJ, WozniakDJ (2005) Binding of Pseudomonas aeruginosa AlgZ to sites upstream of the algZ promoter leads to repression of transcription. J Bacteriol 187: 4430–4443 doi:10.1128/JB.187.13.4430-4443.2005
23. PryorEE, WaligoraEA, XuB, Dellos-NolanS, WozniakDJ, et al. (2012) The transcription factor AmrZ utilizes multiple DNA binding modes to recognize activator and repressor sequences of Pseudomonas aeruginosa virulence genes. PLoS Pathog 8: e1002648 doi:10.1371/journal.ppat.1002648
24. BaynhamPJ, WozniakDJ (1996) Identification and characterization of AlgZ, an AlgT-dependent DNA-binding protein required for Pseudomonas aeruginosa algD transcription. Mol Microbiol 22: 97–108.
25. BaynhamPJ, BrownAL, HallLL, WozniakDJ (1999) Pseudomonas aeruginosa AlgZ, a ribbon-helix-helix DNA-binding protein, is essential for alginate synthesis and algD transcriptional activation. Mol Microbiol 33: 1069–1080.
26. BaynhamPJ, RamseyDM, GvozdyevBV, CordonnierEM, WozniakDJ (2006) The Pseudomonas aeruginosa ribbon-helix-helix DNA-binding protein AlgZ (AmrZ) controls twitching motility and biogenesis of type IV pili. J Bacteriol 188: 132–140 doi:10.1128/JB.188.1.132-140.2006
27. DaviesBW, BogardRW, MekalanosJJ (2011) Mapping the regulon of Vibrio cholerae ferric uptake regulator expands its known network of gene regulation. Proc Natl Acad Sci U S A 108: 12467–12472 doi:10.1073/pnas.1107894108
28. GalaganJ, LyubetskayaA, GomesA (2013) ChIP-Seq and the complexity of bacterial transcriptional regulation. Curr Top Microbiol Immunol 363: 43–68 doi:__10.1007/82_2012_257
29. StarkeyM, HickmanJH, MaL, ZhangN, De LongS, et al. (2009) Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 191: 3492–3503 doi:10.1128/JB.00119-09
30. BorleeBR, GoldmanAD, MurakamiK, SamudralaR, WozniakDJ, et al. (2010) Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75: 827–842 doi:10.1111/j.1365-2958.2009.06991.x
31. BoydCD, O'TooleGA (2012) Second messenger regulation of biofilm formation: breakthroughs in understanding c-di-GMP effector systems. Annu Rev Cell Dev Biol 28: 439–462 doi:10.1146/annurev-cellbio-101011-155705
32. HickmanJW, TifreaDF, HarwoodCS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102: 14422–14427 doi:10.1073/pnas.0507170102
33. Christensen LD, van Gennip M, Rybtke MT, Wu H, Chiang WC, et al. (2013) Clearance of Pseudomonas aeruginosa foreign-body biofilm infections through reduction of the c-di-GMP level in the bacteria. Infect Immun [epub ahead of print]. doi:10.1128/IAI.00332-13.
34. HausslerS (2003) Highly adherent small-colony variants of I in cystic fibrosis lung infection. J Med Microbiol 52: 295–301 doi:10.1099/jmm.0.05069-0
35. KirisitsMJ, ProstL, StarkeyM, ParsekMR (2005) Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71: 4809–4821 doi:10.1128/AEM.71.8.4809-4821.2005
36. MaloneJG, WilliamsR, ChristenM, JenalU, SpiersAJ, et al. (2007) The structure-function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain. Microbiology 153: 980–994 doi:10.1099/mic.0.2006/002824-0
37. HickmanJW, HarwoodCS (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69: 376–389 doi:10.1111/j.1365-2958.2008.06281.x
38. BaraquetC, MurakamiK, ParsekMR, HarwoodCS (2012) The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP. Nucleic Acids Res 40: 7207–7218 doi:10.1093/nar/gks384
39. IrieY, BorleeBR, O'ConnorJR, HillPJ, HarwoodCS, et al. (2012) Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 109: 20632–20636 doi:10.1073/pnas.1217993109
40. MoscosoJA, MikkelsenH, HeebS, WilliamsP, FillouxA (2011) The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ Microbiol 13: 3128–3138 doi:10.1111/j.1462-2920.2011.02595.x
41. Frangipani E, Visaggio D, Heeb S, Kaever V, Cámara M, et al. (2013) The Gac/Rsm and cyclic-di-GMP signalling networks coordinately regulate iron uptake in Pseudomonas aeruginosa. Environ Microbiol [epub ahead of print] doi:10.1111/1462-2920.12164.
42. RömlingU, GalperinMY, GomelskyM (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77: 1–52 doi:10.1128/MMBR.00043-12
43. YuH, MuddM, BoucherJC, SchurrMJ, DereticV (1997) Identification of the algZ gene upstream of the response regulator algR and its participation in control of alginate production in Pseudomonas aeruginosa. J Bacteriol 179: 187–193.
44. CastangS, McManusHR, TurnerKH, DoveSL (2008) H-NS family members function coordinately in an opportunistic pathogen. Proc Natl Acad Sci U S A 105: 18947–18952 doi:10.1073/pnas.0808215105
45. GilbertKB, KimTH, GuptaR, GreenbergEP, SchusterM (2009) Global position analysis of the Pseudomonas aeruginosa quorum-sensing transcription factor LasR. Mol Microbiol 73: 1072–1085 doi:10.1111/j.1365-2958.2009.06832.x
46. HeinzS, BennerC, SpannN, BertolinoE, LinYC, et al. (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. MolCell 38: 576–589 doi:10.1016/j.molcel.2010.05.004
47. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106 doi:10.1186/gb-2010-11-10-r106
48. StitesSW, WaltersB, O'Brien-LadnerAR, BaileyK, WesseliusLJ (1998) Increased iron and ferritin content of sputum from patients with cystic fibrosis or chronic bronchitis. Chest 114: 814–819.
49. StitesSW, PlautzMW, BaileyK, O'Brien-LadnerAR, WesseliusLJ (1999) Increased concentrations of iron and isoferritins in the lower respiratory tract of patients with stable cystic fibrosis. Am J Respir Crit Care Med 160: 796–801 doi:10.1164/ajrccm.160.3.9811018
50. PalmerKL, AyeLM, WhiteleyM (2007) Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol 189: 8079–8087 doi:10.1128/JB.01138-07
51. OglesbyAG, FarrowJM, LeeJH, TomarasAP, GreenbergEP, et al. (2008) The Influence of Iron on Pseudomonas aeruginosa Physiology: A REGULATORY LINK BETWEEN IRON AND QUORUM SENSING. J Biol Chem 283: 15558–15567 doi:10.1074/jbc.M707840200
52. JimenezPN, KochG, ThompsonJA, XavierKB, CoolRH, et al. (2012) The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76: 46–65 doi:10.1128/MMBR.05007-11
53. MougousJD, CuffME, RaunserS, ShenA, ZhouM, et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312: 1526–1530 doi:10.1126/science.1128393
54. LesicB, StarkeyM, HeJ, HazanR, RahmeLG (2009) Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 155: 2845–2855 doi:10.1099/mic.0.029082-0
55. HoodRD, SinghP, HsuF, GüvenerT, CarlMA, et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7: 25–37 doi:10.1016/j.chom.2009.12.007
56. RussellAB, HoodRD, BuiNK, LeRouxM, VollmerW, et al. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475: 343–347 doi:10.1038/nature10244
57. FriskA, JyotJ, AroraSK, RamphalR (2002) Identification and Functional Characterization of flgM, a Gene Encoding the Anti-Sigma 28 Factor in Pseudomonas aeruginosa. J Bacteriol 184: 1514–1521 doi:10.1128/JB.184.6.1514-1521.2002
58. DötschA, EckweilerD, SchniederjansM, ZimmermannA, JensenV, et al. (2012) The Pseudomonas aeruginosa transcriptome in planktonic cultures and static biofilms using RNA sequencing. PLoS ONE 7: e31092 doi:10.1371/journal.pone.0031092.s006
59. PotvinE, SanschagrinF, LevesqueRC (2008) Sigma factors in Pseudomonas aeruginosa. FEMS Microbiol Rev 32: 38–55 doi:10.1111/j.1574-6976.2007.00092.x
60. KulasakaraH, LeeV, BrencicA, LiberatiN, UrbachJ, et al. (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3“-5”)-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103: 2839–2844 doi:10.1073/pnas.0511090103
61. QiuD, DamronFH, MimaT, SchweizerHP, YuHD (2008) PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl Environ Microbiol 74: 7422–7426 doi:10.1128/AEM.01369-08
62. JohnsonDS, MortazaviA, MyersRM, WoldB (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science 316: 1497–1502 doi:10.1126/science.1141319
63. NagalakshmiU, WangZ, WaernK, ShouC, RahaD, et al. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344–1349 doi:10.1126/science.1158441
64. PerkinsTT, DaviesMR, KlemmEJ, RowleyG, WilemanT, et al. (2012) ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization. Mol Microbiol 87: 526–538 doi:10.1111/mmi.12111
65. LiaoJ, SchurrMJ, SauerK (2013) The MerR-like regulator BrlR confers biofilm tolerance by activating multidrug-efflux pumps in Pseudomonas aeruginosa biofilms. J Bacteriol 195(15): 3352–63 doi:10.1128/JB.00318-13
66. BalasubramanianD, KumariH, JaricM, FernandezM, TurnerKH, et al. (2013) Deep sequencing analyses expands the Pseudomonas aeruginosa AmpR regulon to include small RNA-mediated regulation of iron acquisition, heat shock and oxidative stress response. Nucleic Acids Res 42(2): 979–98 doi:10.1093/nar/gkt942
67. GalaganJE, MinchK, PetersonM, LyubetskayaA, AziziE, et al. (2013) The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 499: 178–183 doi:10.1038/nature12337
68. LeeVT, MatewishJM, KesslerJL, HyodoM, HayakawaY, et al. (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65: 1474–1484 doi:10.1111/j.1365-2958.2007.05879.x
69. StoltzDA, MeyerholzDK, PezzuloAA, RamachandranS, RoganMP, et al. (2010) Cystic fibrosis pigs develop lung disease and exhibit defective bacterial eradication at birth. Sci Transl Med 2: 29ra31 doi:10.1126/scitranslmed.3000928
70. HenggeR (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263–273 doi:10.1038/nrmicro2109
71. SondermannH, ShikumaNJ, YildizFH (2012) You've come a long way: c-di-GMP signaling. Curr Opin Microbiol 15: 140–146 doi:10.1016/j.mib.2011.12.008
72. HechtGB, NewtonA (1995) Identification of a novel response regulator required for the swarmer-to-stalked-cell transition in Caulobacter crescentus. J Bacteriol 177: 6223–6229.
73. PaulR, AbelS, WassmannP, BeckA, HeerklotzH, et al. (2007) Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J Biol Chem 282: 29170–29177 doi:10.1074/jbc.M704702200
74. GuvenerZT, HarwoodCS (2007) Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66: 1459–1473 doi:10.1111/j.1365-2958.2007.06008.x
75. HuangyutithamV, GuvenerZT, HarwoodCS (2013) Subcellular clustering of the phosphorylated WspR response regulator protein stimulates its diguanylate cyclase activity. MBio 4: e00242–13 doi:10.1128/mBio.00242-13
76. PaulR, WeiserS, AmiotNC, ChanC, SchirmerT, et al. (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18: 715–727 doi:10.1101/gad.289504
77. KlausenM, HeydornA, RagasP, LambertsenL, Aaes-JørgensenA, et al. (2003) Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48: 1511–1524.
78. KlausenM, Aaes-JørgensenA, MolinS, Tolker-NielsenT (2003) Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50: 61–68.
79. OverhageJ, SchemionekM, WebbJS, RehmBHA (2005) Expression of the psl operon in Pseudomonas aeruginosa PAO1 biofilms: PslA performs an essential function in biofilm formation. Appl Environ Microbiol 71: 4407–4413 doi:10.1128/AEM.71.8.4407-4413.2005
80. ToutainCM, CaizzaNC, ZegansME, O'TooleGA (2007) Roles for flagellar stators in biofilm formation by Pseudomonas aeruginosa. Res Microbiol 158: 471–477 doi:10.1016/j.resmic.2007.04.001
81. Byrd MS, Pang B, Mishra M, Swords WE, Wozniak DJ (2010) The Pseudomonas aeruginosa exopolysaccharide Psl facilitates surface adherence and NF-kappaB activation in A549 cells. MBio 1 pii: e00140-10. doi:10.1128/mBio.00140-10.
82. ByrdMS, PangB, HongW, WaligoraEA, JuneauRA, et al. (2011) Direct evaluation of Pseudomonas aeruginosa biofilm mediators in a chronic infection model. Infect Immun 79: 3087–3095 doi:10.1128/IAI.00057-11
83. YangL, HuY, LiuY, ZhangJ, UlstrupJ, et al. (2011) Distinct roles of extracellular polymeric substances in Pseudomonas aeruginosa biofilm development. Environ Microbiol 13: 1705–1717 doi:10.1111/j.1462-2920.2011.02503.x
84. YangL, HengzhuangW, WuH, DamkiærS, JochumsenN, et al. (2012) Polysaccharides serve as scaffold of biofilms formed by mucoid Pseudomonas aeruginosa. FEMS Immunol Med Microbiol 65: 366–376 doi:10.1111/j.1574-695X.2012.00936.x
85. WangS, ParsekMR, WozniakDJ, MaLZ (2013) A spider web strategy of type IV pili-mediated migration to build a fibre-like Psl polysaccharide matrix in Pseudomonas aeruginosa biofilms. Environ Microbiol 15(8): 2238–53 doi:10.1111/1462-2920.12095
86. GoodmanAL, KulasekaraB, RietschA, BoydD, SmithRS, et al. (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7: 745–754 doi:10.1016/j.devcel.2004.08.020
87. GoodmanAL, MerighiM, HyodoM, VentreI, FillouxA, et al. (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23: 249–259 doi:10.1101/gad.1739009
88. BurrowesE, BaysseC, AdamsC, O'GaraF (2006) Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152: 405–418 doi:10.1099/mic.0.28324-0
89. MannEE, WozniakDJ (2011) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36: 893–916 doi:10.1111/j.1574-6976.2011.00322.x
90. WalkerTS, TomlinKL, WorthenGS, PochKR, LieberJG, et al. (2005) Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils. Infect Immun 73: 3693–3701 doi:10.1128/IAI.73.6.3693-3701.2005
91. MishraM, ByrdMS, SergeantS, AzadAK, ParsekMR, et al. (2012) Pseudomonas aeruginosa Psl polysaccharide reduces neutrophil phagocytosis and the oxidative response by limiting complement-mediated opsonization. Cell Microbiol 14: 95–106 doi:10.1111/j.1462-5822.2011.01704.x
92. YoungRL, MalcolmKC, KretJE, CaceresSM, PochKR, et al. (2011) Neutrophil extracellular trap (NET)-mediated killing of Pseudomonas aeruginosa: evidence of acquired resistance within the CF airway, independent of CFTR. PLoS ONE 6: e23637 doi:10.1371/journal.pone.0023637
93. GovanJR, DereticV (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60: 539–574.
94. LearnDB, BrestelEP, SeetharamaS (1987) Hypochlorite scavenging by Pseudomonas aeruginosa alginate. Infect Immun 55: 1813–1818.
95. PedersenSS, KharazmiA, EspersenF, HøibyN (1990) Pseudomonas aeruginosa alginate in cystic fibrosis sputum and the inflammatory response. Infect Immun 58: 3363–3368.
96. MaiGT, SeowWK, PierGB, McCormackJG, ThongYH (1993) Suppression of lymphocyte and neutrophil functions by Pseudomonas aeruginosa mucoid exopolysaccharide (alginate): reversal by physicochemical, alginase, and specific monoclonal antibody treatments. Infect Immun 61: 559–564.
97. HoangTT, Karkhoff-SchweizerRR, KutchmaAJ, SchweizerHP (1998) 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 212: 77–86.
98. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press. 2028 p.
99. WinsorGL, LamDKW, FlemingL, LoR, WhitesideMD, et al. (2011) Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res 39: D596–D600 doi:10.1093/nar/gkq869
100. KelleyLA, SternbergMJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363–371 doi:10.1038/nprot.2009.2
101. HeydornA, NielsenAT, HentzerM, SternbergC, GivskovM, et al. (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146 (Pt 10): 2395–2407.
102. StoverCK, PhamXQ, ErwinAL, MizoguchiSD, WarrenerP, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959–964 doi:10.1038/35023079
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 3
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Cytomegalovirus m154 Hinders CD48 Cell-Surface Expression and Promotes Viral Escape from Host Natural Killer Cell Control
- Human African Trypanosomiasis and Immunological Memory: Effect on Phenotypic Lymphocyte Profiles and Humoral Immunity
- Conflicting Interests in the Pathogen–Host Tug of War: Fungal Micronutrient Scavenging Versus Mammalian Nutritional Immunity
- DHX36 Enhances RIG-I Signaling by Facilitating PKR-Mediated Antiviral Stress Granule Formation