Positive signature-tagged mutagenesis in Pseudomonas aeruginosa: Tracking patho-adaptive mutations promoting airways chronic infection

PLoS Pathogens

Volumn 7, Issue 2, 2011, Pages

  Bianconi, Irene ^a   Milani, Andrea ^b   Cigana, Cristina ^a   Paroni, Moira ^a   Levesque, Roger C ^c   Bertoni, Giovanni ^b   Bragonzi, Alessandra ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; CYSTIC FIBROSIS; DISEASE COURSE; EPITHELIUM CELL; EVOLUTIONARY ADAPTATION; GENE IDENTIFICATION; GENE INACTIVATION; GENE MUTATION; GENE SEQUENCE; GENETIC SCREENING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VIVO STUDY; MALE; MOLECULAR EVOLUTION; MOUSE; MUTAGENESIS; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT INFECTION; SEQUENCE ANALYSIS; ADAPTATION; ALGORITHM; ANIMAL; C57BL MOUSE; CELL CULTURE; CHRONIC DISEASE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MUTATION; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; VIRULENCE;

BACTERIA (MICROORGANISMS); MURINAE; PSEUDOMONAS AERUGINOSA;

VIRULENCE FACTOR;

ADAPTATION, BIOLOGICAL; ALGORITHMS; ANIMALS; CELLS, CULTURED; CHRONIC DISEASE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MALE; MICE; MICE, INBRED C57BL; MUTAGENESIS; MUTATION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY TRACT INFECTIONS; VIRULENCE; VIRULENCE FACTORS;

EID: 79952222757     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001270     Document Type: Article

References (48)

1. Bragonzi A, Paroni M, Nonis A, Cramer N, Montanari S, et al. (2009) Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. AJRCCM 180: 138-145.
2. Cigana C, Curcurù L, Leone MR, Ieranò T, Lorè NI, et al. (2009) Pseudomonas aeruginosa exploits lipid A and muropeptides modification as a strategy to lower innate immunity during cystic fibrosis lung infection. PLoS One 4: e8439.
3. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, et al. (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 30: 8487-8492.
4. Tümmler B, (2006) Clonal variations in Pseudomonas aeruginosa. In: Ramos J-L, Levesque RC, editors. Pseudomonas: molecular biology of emerging issues, vol. 4 New York Springer pp. 35-68.
5. Bragonzi A, Wiehlmann L, Klockgether J, Cramer N, Worlitzsch D, et al. (2006) Sequence diversity of the mucABD locus in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 152: 3261-3269.
6. Mahenthiralingam E, Campbell ME, Speert DP, (1994) Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. Infect Immun 62: 596-605.
7. D'Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Déziel E, et al. (2007) Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol Microbiol 64: 512-533.
8. Hoffman L, Kulasekara HD, Emerson J, Houston LS, Burns JL, et al. (2009) Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J Cyst Fibros 8: 66-70.
9. Jain M, Ramirez D, Seshadri R, Cullina JF, Powers CA, et al. (2004) Type III secretion phenotypes of Pseudomonas aeruginosa strains change during infection of individuals with cystic fibrosis. J Clin Microbiol 42: 5229-5237.
10. Oliver A, Cantón R, Campo P, Baquero F, Blázquez J, (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251-1254.
11. Rakhimova E, Munder A, Wiehlmann L, Bredenbruch F, Tümmler B, (2008) Fitness of isogenic colony morphology variants of Pseudomonas aeruginosa in murine airway infection. PLoS One 3: e1685.
12. Young D, Hussell T, Dougan G, (2002) Chronic bacterial infections: living with unwanted guests. Nat Immunol 3: 1026-1032.
13. Nguyen D, Singh PK, (2006) Evolving stealth: genetic adaptation of Pseudomonas aeruginosa during cystic fibrosis infections. Proc Natl Acad Sci U S A 30: 8305-8306.
14. Sokurenko E, Chesnokova V, Dykhuizen DE, Ofek I, Wu XR, et al. (1998) Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci U S A 95: 8922-8926.
15. Moxon E, Murphy PA, (1978) Haemophilus influenzae bacteremia and meningitis resulting from survival of a single organism. Proc Natl Acad Sci U S A 75: 1534-1536.
16. Akopyants N, Eaton KA, Berg DE, (1995) Adaptive mutation and cocolonization during Helicobacter pylori infection of gnotobiotic piglets. Infect Immun 63: 116-121.
17. Galperin M, Koonin EV, (2010) From complete genome sequence to 'complete' understanding? Trends Biotechnol 28: 398-406.
18. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, et al. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400-403.
19. Coulter SN, Schwan WR, Ng EY, Langhorne MH, Ritchie HD, et al. (1998) Staphylococcus aureus genetic loci impacting growth and survival in multiple infection environments. Mol Microbiol 30: 393-404.
20. Herbert MA, Hayes S, Deadman ME, Tang CM, Hood DW, et al. (2002) Signature Tagged Mutagenesis of Haemophilus influenzae identifies genes required for in vivo survival. Microb Pathog 33: 211-23.
21. Bragonzi A, (2010) Murine models of acute and chronic lung infection with cystic fibrosis pathogens. IJMM 300: 584-93.
22. Potvin E, Lehoux DE, Kukavica-Ibrulj I, Richard KL, Sanschagrin F, et al. (2003) In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ Microbiol 5: 1294-1308.
23. Bragonzi A, Worlitzsch D, Pier GB, Timpert P, Ulrich M, et al. (2005) Nonmucoid Pseudomonas aeruginosa expresses alginate in the lungs of patients with cystic fibrosis and in a mouse model. J Infect Dis 192: 410-419.
24. Read AF, Taylor LH, (2001) The ecology of genetically diverse infections. Science 292: 1099-1102.
25. Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S, et al. (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43-51.
26. 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.
27. Bohn YS, Brandes G, Rakhimova E, Horatzek S, Salunkhe P, et al. (2009) Multiple roles of Pseudomonas aeruginosa TBCF10839 PilY1 in motility, transport and infection. Mol Microbiol 71: 730-747.
28. O'Toole GA, Kolter R, (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
29. Ochsner UA, Fiechter A, Reiser J, (1994) Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J Biol Chem 269: 19787-19795.
30. Abdel-Mawgoud AM, Lépine F, Déziel E, (2010) Rhamnolipids: diversity of structures, microbial origins and roles. Appl Microbiol Biotechnol 86: 1323-1336.
31. Lu CD, Yang Z, Li W, (2004) Transcriptome analysis of the ArgR regulon in Pseudomonas aeruginosa. J Bacteriol 186: 3855-3861.
32. Haas D, Galimands M, Gamper M, Zimmermann A, (1990) Arginine network of Pseudomonas aeruginosa: specific and global controls. In: Silver S, Chakrabarty A-M, Iglewski B, Kaplan S, editors. Pseudomonas: biotransformations, pathogenesis, and evolving biotechnology Washington, DC American Society for Microbiology pp. 303-316.
33. Itoh Y, (1997) Cloning and characterization of the aru genes encoding enzymes of the catabolic arginine succinyltransferase pathway in Pseudomonas aeruginosa. J Bacteriol 179: 7280-7729.
34. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, et al. (2002) Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109: 317-325.
35. Alvarez-Ortega C, Harwood CS, (2007) Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol Microbiol 65: 153-165.
36. Martin DW, Mohr CD, (2000) Invasion and intracellular survival of Burkholderia cepacia. Infection and Immunity 68: 24-29.
37. Philpott DJ, Belaid D, Troubadour P, Thiberge JM, Tankovic J, et al. (2002) Reduced activation of inflammatory responses in host cells by mouse-adapted Helicobacter pylory isolates. Cell Microbiol 4: 285-296.
38. Monack D, Mueller A, Falkow S, (2004) Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol 2: 747-765.
39. Finlay B, Falkow S, (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61: 136-169.
40. Kaufmann SHE, (1993) Immunity to intracellular bacteria. Annu Rev Immunol 11: 129-163.
41. Lamothe J, Huynh KK, Grinstein S, Valvano MA, (2007) Intracellular survival of Burkholderia cenocepacia in macrophages is associated with a delay in the maturation of bacter. Cell Microbiol 9: 40-53.
42. Pier G, Grout M, Zaidi TS, Olsen JC, Johnson LG, et al. (1996) Role of mutant CFTR in hypersusceptibility of cystic fibrosis patients to lung infections. Science 271: 64-67.
43. Pier G, Grout M, Zaidi TS, (1997) Cystic fibrosis transmembrane conductance regulator is an epithelial cell receptor for clearance of Pseudomonas aeruginosa from the lung. Proc Natl Acad Sci U S A 94: 12088-12093.
44. Kumar P, Henikoff S, Ng PC, (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4: 1073-1081.
45. Holloway B, Krishnapillai V, Morgan AF, (1979) Chromosomal genetics of Pseudomonas. Microbiol Rev 43: 73-102.
46. Kwon Y, Ricke SC, (2000) Efficient amplification of multiple transposon-flanking sequences. J Microbiol Methods 41: 195-199.
47. Montanari S, Oliver A, Salerno P, Mena A, Bertoni G, et al. (2007) Biological cost of hypermutation in Pseudomonas aeruginosa strains from patients with cystic fibrosis. Microbiology 153: 1445-1454.
48. Pirone L, Bragonzi A, Farcomeni A, Paroni M, Auriche C, et al. (2008) Burkholderia cenocepacia strains isolated from cystic fibrosis patients are apparently more invasive and more virulent than rhizosphere strains. Environ Microbiol 10: 2773-2784.