Inhibits Virulence through Suppression of Pyochelin and Pyoverdine Biosynthesis
Pseudomonas aeruginosa and Candida albicans are two medically important human pathogens that often co-infect or co-colonize the same human niches, such as the gut. In a normal healthy host, P. aeruginosa and C. albicans can colonize the gut without any significant pathologic sequelae. But in immunocompromised hosts, both pathogens can escape the gut and cause life-threatening disseminated infections. Yet the mechanisms and pathogenic consequences of interactions between these two pathogens within a living mammalian host are not well understood. Here, we use a mouse model of P. aeruginosa and C. albicans gut co-infection to better understand the mechanisms by which C. albicans inhibits P. aeruginosa infection. C. albicans inhibits the expression of P. aeruginosa genes that are vital for iron acquisition. Accordingly, deleting these iron acquisition genes in P. aeruginosa prevents infection. Understanding how microbes interact and antagonize each other may help us identify new potential therapeutic targets for preventing or treating infections.
Vyšlo v časopise:
Inhibits Virulence through Suppression of Pyochelin and Pyoverdine Biosynthesis. PLoS Pathog 11(8): e32767. doi:10.1371/journal.ppat.1005129
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1005129
Souhrn
Pseudomonas aeruginosa and Candida albicans are two medically important human pathogens that often co-infect or co-colonize the same human niches, such as the gut. In a normal healthy host, P. aeruginosa and C. albicans can colonize the gut without any significant pathologic sequelae. But in immunocompromised hosts, both pathogens can escape the gut and cause life-threatening disseminated infections. Yet the mechanisms and pathogenic consequences of interactions between these two pathogens within a living mammalian host are not well understood. Here, we use a mouse model of P. aeruginosa and C. albicans gut co-infection to better understand the mechanisms by which C. albicans inhibits P. aeruginosa infection. C. albicans inhibits the expression of P. aeruginosa genes that are vital for iron acquisition. Accordingly, deleting these iron acquisition genes in P. aeruginosa prevents infection. Understanding how microbes interact and antagonize each other may help us identify new potential therapeutic targets for preventing or treating infections.
Zdroje
1. Hermann C, Hermann J, Munzel U, Ruchel R (1999) Bacterial flora accompanying Candida yeasts in clinical specimens. Mycoses 42: 619–627. 10680438
2. Azoulay E, Timsit JF, Tafflet M, de Lassence A, Darmon M, et al. (2006) Candida colonization of the respiratory tract and subsequent pseudomonas ventilator-associated pneumonia. Chest 129: 110–117. 16424420
3. Bauernfeind A, Bertele RM, Harms K, Horl G, Jungwirth R, et al. (1987) Qualitative and quantitative microbiological analysis of sputa of 102 patients with cystic fibrosis. Infection 15: 270–277. 3117700
4. McAlester G, O'Gara F, Morrissey JP (2008) Signal-mediated interactions between Pseudomonas aeruginosa and Candida albicans. J Med Microbiol 57: 563–569. doi: 10.1099/jmm.0.47705-0 18436588
5. Gupta N, Haque A, Mukhopadhyay G, Narayan RP, Prasad R (2005) Interactions between bacteria and Candida in the burn wound. Burns 31: 375–378. 15774298
6. Marrie TJ, Costerton JW (1984) Scanning and transmission electron microscopy of in situ bacterial colonization of intravenous and intraarterial catheters. J Clin Microbiol 19: 687–693. 6429190
7. Tchekmedyian NS, Newman K, Moody MR, Costerton JW, Aisner J, et al. (1986) Special studies of the Hickman catheter of a patient with recurrent bacteremia and candidemia. Am J Med Sci 291: 419–424. 3717200
8. Hogan DA, Vik A, Kolter R (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54: 1212–1223. 15554963
9. Brand A, Barnes JD, Mackenzie KS, Odds FC, Gow NA (2008) Cell wall glycans and soluble factors determine the interactions between the hyphae of Candida albicans and Pseudomonas aeruginosa. FEMS Microbiol Lett 287: 48–55. doi: 10.1111/j.1574-6968.2008.01301.x 18680523
10. Hogan DA, Kolter R (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296: 2229–2232. 12077418
11. Cugini C, Calfee MW, Farrow JM 3rd, Morales DK, Pesci EC, et al. (2007) Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol 65: 896–906. 17640272
12. de Macedo JL, Santos JB (2005) Bacterial and fungal colonization of burn wounds. Mem Inst Oswaldo Cruz 100: 535–539. 16184232
13. Hughes WT, Kim HK (1973) Mycoflora in cystic fibrosis: some ecologic aspects of Pseudomonas aeruginosa and Candida albicans. Mycopathol Mycol Appl 50: 261–269. 4199669
14. Burns JL, Van Dalfsen JM, Shawar RM, Otto KL, Garber RL, et al. (1999) Effect of chronic intermittent administration of inhaled tobramycin on respiratory microbial flora in patients with cystic fibrosis. J Infect Dis 179: 1190–1196. 10191222
15. Nseir S, Jozefowicz E, Cavestri B, Sendid B, Di Pompeo C, et al. (2007) Impact of antifungal treatment on Candida-Pseudomonas interaction: a preliminary retrospective case-control study. Intensive Care Med 33: 137–142. 17115135
16. Pizzo PA, Poplack D, editors (2011) Principles and Practice of Pediatric Oncology, 6th Edition. Philadelphia: Lippincott Williams & Wilkins. 1531
17. Fanci R, Paci C, Anichini P, Pecile P, Marra G, et al. (2003) Incidence and molecular epidemiology of Pseudomonas aeruginosa bacteremias in patients with acute leukemia: analysis by pulsed-field gel electrophoresis. New Microbiol 26: 353–361. 14596346
18. Tancrede CH, Andremont AO (1985) Bacterial translocation and gram-negative bacteremia in patients with hematological malignancies. J Infect Dis 152: 99–103. 3925032
19. Miranda LN, van der Heijden IM, Costa SF, Sousa AP, Sienra RA, et al. (2009) Candida colonisation as a source for candidaemia. J Hosp Infect 72: 9–16. doi: 10.1016/j.jhin.2009.02.009 19303662
20. Nucci M, Anaissie E (2001) Revisiting the source of candidemia: skin or gut? Clin Infect Dis 33: 1959–1967. 11702290
21. Berg RD (1999) Bacterial translocation from the gastrointestinal tract. Adv Exp Med Biol 473: 11–30. 10659341
22. Pasqualotto AC, Nedel WL, Machado TS, Severo LC (2006) Risk factors and outcome for nosocomial breakthrough candidaemia. J Infect 52: 216–222. 15936825
23. Rosen GP, Nielsen K, Glenn S, Abelson J, Deville J, et al. (2005) Invasive fungal infections in pediatric oncology patients: 11-year experience at a single institution. J Pediatr Hematol Oncol 27: 135–140. 15750444
24. Fan D, Coughlin LA, Neubauer MM, Kim J, Kim MS, et al. (2015) Activation of HIF-1alpha and LL-37 by commensal bacteria inhibits Candida albicans colonization. Nat Med.
25. Koh AY, Kohler JR, Coggshall KT, Van Rooijen N, Pier GB (2008) Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog 4: e35. doi: 10.1371/journal.ppat.0040035 18282097
26. White SJ, Rosenbach A, Lephart P, Nguyen D, Benjamin A, et al. (2007) Self-regulation of Candida albicans population size during GI colonization. PLoS Pathog 3: e184. 18069889
27. Noverr MC, Huffnagle GB (2004) Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect Immun 72: 6206–6210. 15501745
28. Mason KL, Erb Downward JR, Mason KD, Falkowski NR, Eaton KA, et al. (2012) Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infect Immun 80: 3371–3380. doi: 10.1128/IAI.00449-12 22778094
29. Taur Y, Xavier JB, Lipuma L, Ubeda C, Goldberg J, et al. (2012) Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Infect Dis 55: 905–914. doi: 10.1093/cid/cis580 22718773
30. Koh AY, Mikkelsen PJ, Smith RS, Coggshall KT, Kamei A, et al. (2010) Utility of in vivo transcription profiling for identifying Pseudomonas aeruginosa genes needed for gastrointestinal colonization and dissemination. PLoS One 5: e15131. doi: 10.1371/journal.pone.0015131 21170272
31. Koh AY, Priebe GP, Pier GB (2005) Virulence of Pseudomonas aeruginosa in a murine model of gastrointestinal colonization and dissemination in neutropenia. Infect Immun 73: 2262–2272. 15784570
32. Sawa T, Ohara M, Kurahashi K, Twining SS, Frank DW, et al. (1998) In vitro cellular toxicity predicts Pseudomonas aeruginosa virulence in lung infections. Infect Immun 66: 3242–3249. 9632591
33. Falgier C, Kegley S, Podgorski H, Heisel T, Storey K, et al. (2011) Candida species differ in their interactions with immature human gastrointestinal epithelial cells. Pediatr Res 69: 384–389. doi: 10.1203/PDR.0b013e31821269d5 21283049
34. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, et al. (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939–949. 9298905
35. Kong EF, Kucharikova S, Van Dijck P, Peters BM, Shirtliff ME, et al. (2015) Clinical implications of oral candidiasis: host tissue damage and disseminated bacterial disease. Infect Immun 83: 604–613. doi: 10.1128/IAI.02843-14 25422264
36. Schlecht LM, Peters BM, Krom BP, Freiberg JA, Hansch GM, et al. (2015) Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue. Microbiology 161: 168–181. doi: 10.1099/mic.0.083485-0 25332378
37. Ganz T, Nemeth E (2006) Regulation of iron acquisition and iron distribution in mammals. Biochim Biophys Acta 1763: 690–699. 16790283
38. Skaar EP (2010) The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6: e1000949. doi: 10.1371/journal.ppat.1000949 20711357
39. Takase H, Nitanai H, Hoshino K, Otani T (2000) Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect Immun 68: 1834–1839. 10722571
40. Takase H, Nitanai H, Hoshino K, Otani T (2000) Requirement of the Pseudomonas aeruginosa tonB gene for high-affinity iron acquisition and infection. Infect Immun 68: 4498–4504. 10899848
41. Meyer JM, Neely A, Stintzi A, Georges C, Holder IA (1996) Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infect Immun 64: 518–523. 8550201
42. Imperi F, Massai F, Facchini M, Frangipani E, Visaggio D, et al. (2013) Repurposing the antimycotic drug flucytosine for suppression of Pseudomonas aeruginosa pathogenicity. Proc Natl Acad Sci U S A 110: 7458–7463. doi: 10.1073/pnas.1222706110 23569238
43. Almeida RS, Wilson D, Hube B (2009) Candida albicans iron acquisition within the host. FEMS Yeast Res 9: 1000–1012. doi: 10.1111/j.1567-1364.2009.00570.x 19788558
44. Kronstad JW, Cadieux B, Jung WH (2013) Pathogenic yeasts deploy cell surface receptors to acquire iron in vertebrate hosts. PLoS Pathog 9: e1003498. doi: 10.1371/journal.ppat.1003498 24009498
45. Murciano C, Villamon E, O'Connor JE, Gozalbo D, Gil ML (2006) Killed Candida albicans yeasts and hyphae inhibit gamma interferon release by murine natural killer cells. Infect Immun 74: 1403–1406. 16428793
46. Paulus SC, van Saene HK, Hemsworth S, Hughes J, Ng A, et al. (2005) A prospective study of septicaemia on a paediatric oncology unit: a three-year experience at The Royal Liverpool Children's Hospital, Alder Hey, UK. Eur J Cancer 41: 2132–2140. 16129600
47. Navarathna DH, Hornby JM, Krishnan N, Parkhurst A, Duhamel GE, et al. (2007) Effect of farnesol on a mouse model of systemic candidiasis, determined by use of a DPP3 knockout mutant of Candida albicans. Infect Immun 75: 1609–1618. 17283095
48. Stookey LL (1970) Ferrozine—a new spectrophotometric reagent for iron. Anal Chem 42: 779–781.
49. Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102: 11076–11081. 16043697
50. Rogan MP, Taggart CC, Greene CM, Murphy PG, O'Neill SJ, et al. (2004) Loss of microbicidal activity and increased formation of biofilm due to decreased lactoferrin activity in patients with cystic fibrosis. J Infect Dis 190: 1245–1253. 15346334
51. Singh PK, Parsek MR, Greenberg EP, Welsh MJ (2002) A component of innate immunity prevents bacterial biofilm development. Nature 417: 552–555. 12037568
52. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK (2007) The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 117: 877–888. 17364024
53. Genco CA, Chen CY, Arko RJ, Kapczynski DR, Morse SA (1991) Isolation and characterization of a mutant of Neisseria gonorrhoeae that is defective in the uptake of iron from transferrin and haemoglobin and is avirulent in mouse subcutaneous chambers. J Gen Microbiol 137: 1313–1321. 1919507
54. Litwin CM, Calderwood SB (1993) Role of iron in regulation of virulence genes. Clin Microbiol Rev 6: 137–149. 8472246
55. Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML (2002) Siderophore-mediated signaling regulates virulence factor production in Pseudomonasaeruginosa. Proc Natl Acad Sci U S A 99: 7072–7077. 11997446
56. Nicas TI, Bradley J, Lochner JE, Iglewski BH (1985) The role of exoenzyme S in infections with Pseudomonas aeruginosa. J Infect Dis 152: 716–721. 2995500
57. Tang H, Kays M, Prince A (1995) Role of Pseudomonas aeruginosa pili in acute pulmonary infection. Infect Immun 63: 1278–1285. 7890385
58. Tang HB, DiMango E, Bryan R, Gambello M, Iglewski BH, et al. (1996) Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection. Infect Immun 64: 37–43. 8557368
59. Amidon GL, Lee HJ (1994) Absorption of peptide and peptidomimetic drugs. Annu Rev Pharmacol Toxicol 34: 321–341. 8042854
60. Lee YH, Sinko PJ (2000) Oral delivery of salmon calcitonin. Adv Drug Deliv Rev 42: 225–238.
61. Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG (2002) Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet 32: 435–443. 12467341
62. Padmanabhan P, Grosse J, Asad AB, Radda GK, Golay X (2013) Gastrointestinal transit measurements in mice with 99mTc-DTPA-labeled activated charcoal using NanoSPECT-CT. EJNMMI Res 3: 60. doi: 10.1186/2191-219X-3-60 23915679
63. Andrews SC, Robinson AK, Rodriguez-Quinones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215–237. 12829269
64. Hunter RC, Asfour F, Dingemans J, Osuna BL, Samad T, et al. (2013) Ferrous iron is a significant component of bioavailable iron in cystic fibrosis airways. MBio 4.
65. Konings AF, Martin LW, Sharples KJ, Roddam LF, Latham R, et al. (2013) Pseudomonas aeruginosa uses multiple pathways to acquire iron during chronic infection in cystic fibrosis lungs. Infect Immun 81: 2697–2704. doi: 10.1128/IAI.00418-13 23690396
66. Evans DF, Pye G, Bramley R, Clark AG, Dyson TJ, et al. (1988) Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut 29: 1035–1041. 3410329
67. Moura E, Verheul AF, Marx JJ (1998) A functional defect in hereditary haemochromatosis monocytes and monocyte-derived macrophages. Eur J Clin Invest 28: 164–173. 9541131
68. van Asbeck BS, Marx JJ, Struyvenberg A, Verhoef J (1984) Functional defects in phagocytic cells from patients with iron overload. J Infect 8: 232–240. 6736664
69. Patel RM, Myers LS, Kurundkar AR, Maheshwari A, Nusrat A, et al. (2012) Probiotic bacteria induce maturation of intestinal claudin 3 expression and barrier function. Am J Pathol 180: 626–635. doi: 10.1016/j.ajpath.2011.10.025 22155109
70. Grillot R, Portmann-Coffin V, Ambroise-Thomas P (1994) Growth inhibition of pathogenic yeasts by Pseudomonas aeruginosa in vitro: clinical implications in blood cultures. Mycoses 37: 343–347. 7746293
71. Kerr JR (1994) Suppression of fungal growth exhibited by Pseudomonas aeruginosa. J Clin Microbiol 32: 525–527. 8150966
72. Kerr JR, Taylor GW, Rutman A, Hoiby N, Cole PJ, et al. (1999) Pseudomonas aeruginosa pyocyanin and 1-hydroxyphenazine inhibit fungal growth. J Clin Pathol 52: 385–387. 10560362
73. Ray TL, Payne CD (1988) Scanning electron microscopy of epidermal adherence and cavitation in murine candidiasis: a role for Candida acid proteinase. Infect Immun 56: 1942–1949. 3294180
74. Scherwitz C (1982) Ultrastructure of human cutaneous candidosis. J Invest Dermatol 78: 200–205. 7035576
75. Purschke FG, Hiller E, Trick I, Rupp S (2012) Flexible survival strategies of Pseudomonas aeruginosa in biofilms result in increased fitness compared with Candida albicans. Mol Cell Proteomics 11: 1652–1669. doi: 10.1074/mcp.M112.017673 22942357
76. Peleg AY, Tampakakis E, Fuchs BB, Eliopoulos GM, Moellering RC Jr., et al. (2008) Prokaryote-eukaryote interactions identified by using Caenorhabditis elegans. Proc Natl Acad Sci U S A 105: 14585–14590. doi: 10.1073/pnas.0805048105 18794525
77. Akagawa G, Abe S, Yamaguchi H (1995) Mortality of Candida albicans-infected mice is facilitated by superinfection of Escherichia coli or administration of its lipopolysaccharide. J Infect Dis 171: 1539–1544. 7769289
78. Burd RS, Raymond CS, Dunn DL (1992) Endotoxin promotes synergistic lethality during concurrent Escherichia coli and Candida albicans infection. J Surg Res 52: 537–542. 1528027
79. Neely AN, Law EJ, Holder IA (1986) Increased susceptibility to lethal Candida infections in burned mice preinfected with Pseudomonas aeruginosa or pretreated with proteolytic enzymes. Infect Immun 52: 200–204. 2420722
80. Peters BM, Noverr MC (2013) Candida albicans-Staphylococcus aureus polymicrobial peritonitis modulates host innate immunity. Infect Immun 81: 2178–2189. doi: 10.1128/IAI.00265-13 23545303
81. Bodey GP (2001) Pseudomonas aeruginosa infections in cancer patients: have they gone away? Curr Opin Infect Dis 14: 403–407. 11964856
82. Angebault C, Djossou F, Abelanet S, Permal E, Ben Soltana M, et al. (2013) Candida albicans is not always the preferential yeast colonizing humans: a study in Wayampi Amerindians. J Infect Dis 208: 1705–1716. doi: 10.1093/infdis/jit389 23904289
83. Reichart PA, Khongkhunthian P, Samaranayake LP, Yau J, Patanaporn V, et al. (2005) Oral Candida species and betel quid-associated oral lesions in Padaung women of Northern Thailand. Mycoses 48: 132–136. 15743432
84. Xu J, Mitchell TG (2003) Geographical differences in human oral yeast flora. Clin Infect Dis 36: 221–224. 12522756
85. Bougnoux ME, Diogo D, Francois N, Sendid B, Veirmeire S, et al. (2006) Multilocus sequence typing reveals intrafamilial transmission and microevolutions of Candida albicans isolates from the human digestive tract. J Clin Microbiol 44: 1810–1820. 16672411
86. Kam AP, Xu J (2002) Diversity of commensal yeasts within and among healthy hosts. Diagn Microbiol Infect Dis 43: 19–28. 12052625
87. Xu J, Boyd CM, Livingston E, Meyer W, Madden JF, et al. (1999) Species and genotypic diversities and similarities of pathogenic yeasts colonizing women. J Clin Microbiol 37: 3835–3843. 10565893
88. Almeida RS, Brunke S, Albrecht A, Thewes S, Laue M, et al. (2008) the hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog 4: e1000217. doi: 10.1371/journal.ppat.1000217 19023418
89. Cornelis P, Bodilis J (2009) A survey of TonB-dependent receptors in fluorescent pseudomonads. Environ Microbiol Rep 1: 256–262. doi: 10.1111/j.1758-2229.2009.00041.x 23765855
90. Cuiv PO, Keogh D, Clarke P, O'Connell M (2007) FoxB of Pseudomonas aeruginosa functions in the utilization of the xenosiderophores ferrichrome, ferrioxamine B, and schizokinen: evidence for transport redundancy at the inner membrane. J Bacteriol 189: 284–287. 17056746
91. Llamas MA, Mooij MJ, Sparrius M, Vandenbroucke-Grauls CM, Ratledge C, et al. (2008) Characterization of five novel Pseudomonas aeruginosa cell-surface signalling systems. Mol Microbiol 67: 458–472. 18086184
92. Ochsner UA, Johnson Z, Vasil ML (2000) Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiology 146 (Pt 1): 185–198. 10658665
93. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC (2006) Feo—transport of ferrous iron into bacteria. Biometals 19: 143–157. 16718600
94. Wang Y, Newman DK (2008) Redox reactions of phenazine antibiotics with ferric (hydr)oxides and molecular oxygen. Environ Sci Technol 42: 2380–2386. 18504969
95. Chatzinikolaou I, Abi-Said D, Bodey GP, Rolston KV, Tarrand JJ, et al. (2000) Recent experience with Pseudomonas aeruginosa bacteremia in patients with cancer: Retrospective analysis of 245 episodes. Arch Intern Med 160: 501–509. 10695690
96. Micol JB, de Botton S, Guieze R, Coiteux V, Darre S, et al. (2006) An 18-case outbreak of drug-resistant Pseudomonas aeruginosa bacteriemia in hematology patients. Haematologica 91: 1134–1138. 16885056
97. Brandl K, Plitas G, Mihu CN, Ubeda C, Jia T, et al. (2008) Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455: 804–807. doi: 10.1038/nature07250 18724361
98. Brandtzaeg P (2010) Food allergy: separating the science from the mythology. Nat Rev Gastroenterol Hepatol 7: 380–400. doi: 10.1038/nrgastro.2010.80 20606633
99. Beach RC, Menzies IS, Clayden GS, Scopes JW (1982) Gastrointestinal permeability changes in the preterm neonate. Arch Dis Child 57: 141–145. 7065710
100. Rouwet EV, Heineman E, Buurman WA, ter Riet G, Ramsay G, et al. (2002) Intestinal permeability and carrier-mediated monosaccharide absorption in preterm neonates during the early postnatal period. Pediatr Res 51: 64–70. 11756641
101. Finck-Barbancon V, Goranson J, Zhu L, Sawa T, Wiener-Kronish JP, et al. (1997) ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol Microbiol 25: 547–557. 9302017
102. Kudoh I, Wiener-Kronish JP, Hashimoto S, Pittet JF, Frank D (1994) Exoproduct secretions of Pseudomonas aeruginosa strains influence severity of alveolar epithelial injury. Am J Physiol 267: L551–556. 7977765
103. Vallis AJ, Finck-Barbancon V, Yahr TL, Frank DW (1999) Biological effects of Pseudomonas aeruginosa type III-secreted proteins on CHO cells. Infect Immun 67: 2040–2044. 10085057
104. Allewelt M, Coleman FT, Grout M, Priebe GP, Pier GB (2000) Acquisition of expression of the Pseudomonas aeruginosa ExoU cytotoxin leads to increased bacterial virulence in a murine model of acute pneumonia and systemic spread. Infect Immun 68: 3998–4004. 10858214
105. Chang W, Small DA, Toghrol F, Bentley WE (2005) Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide. BMC Genomics 6: 115. 16150148
106. Swanson BL, Colmer JA, Hamood AN (1999) The Pseudomonas aeruginosa exotoxin A regulatory gene, ptxS: evidence for negative autoregulation. J Bacteriol 181: 4890–4895. 10438759
107. Swanson BL, Hamood AN (2000) Autoregulation of the Pseudomonas aeruginosa protein PtxS occurs through a specific operator site within the ptxS upstream region. J Bacteriol 182: 4366–4371. 10894751
108. Goodman AL, Kallstrom G, Faith JJ, Reyes A, Moore A, et al. (2011) Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc Natl Acad Sci U S A 108: 6252–6257. doi: 10.1073/pnas.1102938108 21436049
109. Lopez-Medina E, Neubauer MM, Pier GB, Koh AY (2011) RNA isolation of Pseudomonas aeruginosa colonizing the murine gastrointestinal tract. J Vis Exp.
110. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628. doi: 10.1038/nmeth.1226 18516045
111. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106. doi: 10.1186/gb-2010-11-10-r106 20979621
112. Samuel BS, Gordon JI (2006) A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci U S A 103: 10011–10016. 16782812
113. Savli H, Karadenizli A, Kolayli F, Gundes S, Ozbek U, et al. (2003) Expression stability of six housekeeping genes: A proposal for resistance gene quantification studies of Pseudomonas aeruginosa by real-time quantitative RT-PCR. J Med Microbiol 52: 403–408. 12721316
114. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP (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. 9661666
115. Mettrick KA, Lamont IL (2009) Different roles for anti-sigma factors in siderophore signalling pathways of Pseudomonas aeruginosa. Mol Microbiol 74: 1257–1271. doi: 10.1111/j.1365-2958.2009.06932.x 19889096
116. Morgan AF (1979) Transduction of Pseudomonas aeruginosa with a mutant of bacteriophage E79. J Bacteriol 139: 137–140. 110777
117. Chuanchuen R, Narasaki CT, Schweizer HP (2002) Benchtop and microcentrifuge preparation of Pseudomonas aeruginosa competent cells. Biotechniques 33: 760, 762–763. 12398182
118. Riemer J, Hoepken HH, Czerwinska H, Robinson SR, Dringen R (2004) Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal Biochem 331: 370–375. 15265744
119. Stookey LL (1970) Ferrozine—a new spectrophotometric reagent for iron. Anal Chem 42: 779–781.
120. Carmi R, Carmeli S, Levy E, Gough FJ (1994) (+)-(S)-dihydroaeruginoic acid, an inhibitor of Septoria tritici and other phytopathogenic fungi and bacteria, produced by Pseudomonas fluorescens. J Nat Prod 57: 1200–1205. 7798954
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 8
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Human Non-neutralizing HIV-1 Envelope Monoclonal Antibodies Limit the Number of Founder Viruses during SHIV Mucosal Infection in Rhesus Macaques
- Type VI Secretion System Toxins Horizontally Shared between Marine Bacteria
- Are Human Intestinal Eukaryotes Beneficial or Commensals?
- Illuminating Targets of Bacterial Secretion