Absence of membrane phosphatidylcholine does not affect virulence and stress tolerance phenotypes in the opportunistic pathogen Pseudomonas aeruginosa

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Malek, Adel A ^a   Wargo, Matthew J ^b   Hogan, Deborah A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLCHOLINE; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CONTROLLED STUDY; CULTURE MEDIUM; MALE; MEMBRANE FORMATION; MICROARRAY ANALYSIS; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; PHENOTYPE; PSEUDOMONAS AERUGINOSA; STRAIN DIFFERENCE; TWITCHING MOTILITY; WILD TYPE; ADAPTATION; ANIMAL; BACTERIAL COUNT; BIOFILM; CELL MEMBRANE; CYTOLOGY; DNA MICROARRAY; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MUTATION; PATHOGENICITY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SURFACE PROPERTY; VIRULENCE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BIOFILMS; CELL MEMBRANE; COLONY COUNT, MICROBIAL; HUMANS; MICE; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PHOSPHATIDYLCHOLINES; PSEUDOMONAS AERUGINOSA; STRESS, PHYSIOLOGICAL; SURFACE PROPERTIES; VIRULENCE;

EID: 84857178125     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030829     Document Type: Article

References (56)

1. Henry SA, Patton-Vogt JL, (1998) Genetic regulation of phospholipid metabolism: Yeast as a model eukaryote. Prog Nucleic Acid Res Mol Biol 61: 133-179.
2. Exton JH, (1997) Phospholipase D: Enzymology, mechanisms of regulation, and function. Physiol Rev 77: 303-320.
3. Exton JH, (1994) Phosphatidylcholine Breakdown and Signal-Transduction. Biochim Biophys Acta 1212: 26-42.
4. Aktas M, Wessel M, Hacker S, Klusener S, Gleichenhagen J, et al. (2010) Phosphatidylcholine biosynthesis and its significance in bacteria interacting with eukaryotic cells. Eur J Cell Biol 89: 888-894.
5. Martinez-Morales F, Schobert M, Lopez-Lara IM, Geiger O, (2003) Pathways for phosphatidylcholine biosynthesis in bacteria. Microbiology 149: 3461-3471.
6. Vance DE, Ridgway ND, (1988) The methylation of phosphatidylethanolamine. Prog Lipid Res 27: 61-79.
7. de Rudder KE, Sohlenkamp C, Geiger O, (1999) Plant-exuded choline is used for rhizobial membrane lipid biosynthesis by phosphatidylcholine synthase. J Biol Chem 274: 20011-20016.
8. Minder AC, de Rudder KE, Narberhaus F, Fischer HM, Hennecke H, et al. (2001) Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. Mol Microbiol 39: 1186-1198.
9. de Rudder KE, Lopez-Lara IM, Geiger O, (2000) Inactivation of the gene for phospholipid N-methyltransferase in Sinorhizobium meliloti: phosphatidylcholine is required for normal growth. Mol Microbiol 37: 763-772.
10. Wessel M, Klusener S, Godeke J, Fritz C, Hacker S, et al. (2006) Virulence of Agrobacterium tumefaciens requires phosphatidylcholine in the bacterial membrane. Mol Microbiol 62: 906-915.
11. Klusener S, Aktas M, Thormann KM, Wessel M, Narberhaus F, (2009) Expression and physiological relevance of Agrobacterium tumefaciens phosphatidylcholine biosynthesis genes. J Bacteriol 191: 365-374.
12. Conover GM, Martinez-Morales F, Heidtman MI, Luo ZQ, Tang M, et al. (2008) Phosphatidylcholine synthesis is required for optimal function of Legionella pneumophila virulence determinants. Cell Microbiol 10: 514-528.
13. Comerci DJ, Altabe S, de Mendoza D, Ugalde RA, (2006) Brucella abortus synthesizes phosphatidylcholine from choline provided by the host. J Bacteriol 188: 1929-1934.
14. Conde-Alvarez R, Grillo MJ, Salcedo SP, de Miguel MJ, Fugier E, et al. (2006) Synthesis of phosphatidylcholine, a typical eukaryotic phospholipid, is necessary for full virulence of the intracellular bacterial parasite Brucella abortus. Cell Microbiol 8: 1322-1335.
15. Wilderman PJ, Vasil AI, Martin WE, Murphy RC, Vasil ML, (2002) Pseudomonas aeruginosa synthesizes phosphatidylcholine by use of the phosphatidylcholine synthase pathway. J Bacteriol 184: 4792-4799.
16. Baysse C, Cullinane M, Denervaud V, Burrowes E, Dow JM, et al. (2005) Modulation of quorum sensing in Pseudomonas aeruginosa through alteration of membrane properties. Microbiology 151: 2529-2542.
17. 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.
18. 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.
19. D'Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Déziel D, et al. (2007) Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol Microbiol 64: 512-533.
20. 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.
21. Willumeit R, Kumpugdee M, Funari SS, Lohner K, Navas BP, et al. (2005) Structural rearrangement of model membranes by the peptide antibiotic NK-2. Biochim Biophys Acta 1669: 125-134.
22. Lysenko ES, Gould J, Bals R, Wilson JM, Weiser JN, (2000) Bacterial phosphorylcholine decreases susceptibility to the antimicrobial peptide LL-37/hCAP18 expressed in the upper respiratory tract. Infect Immun 68: 1664-1671.
23. Hamilton A, Popham DL, Carl DJ, Lauth X, Nizet V, et al. (2006) Penicillin-binding protein 1a promotes resistance of group B streptococcus to antimicrobial peptides. Infect Immun 74: 6179-6187.
24. Harshey RM, (2003) Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57: 249-273.
25. O'Toole G, Kaplan HB, Kolter R, (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54: 49-79.
26. Costerton JW, Stewart PS, Greenberg EP, (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
27. Friedman L, Kolter R, (2004) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186: 4457-4465.
28. O'Toole GA, Kolter R, (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
29. Anderson GG, Moreau-Marquis S, Stanton BA, O'Toole GA, (2008) In vitro analysis of tobramycin-treated Pseudomonas aeruginosa biofilms on cystic fibrosis-derived airway epithelial cells. Infect Immun 76: 1423-1433.
30. Moreau-Marquis S, Redelman CV, Stanton BA, Anderson GG, (2010) Co-culture models of Pseudomonas aeruginosa biofilms grown on live human airway cells. J Vis Exp.
31. Hogan DA, Kolter R, (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296: 2229-2232.
32. Kida Y, Shimizu T, Kuwano K, (2011) Cooperation between LepA and PlcH Contributes to the in vivo virulence and growth of Pseudomonas aeruginosa in mice. Infect Immun 79: 211-219.
33. Wargo MJ, Ho TC, Gross MJ, Whittaker LA, Hogan DA, (2009) GbdR Regulates Pseudomonas aeruginosa plcH and pchP transcription in response to choline catabolites. Infection and Immunity 77: 1103-1111.
34. Miyata S, Casey M, Frank DW, Ausubel FM, Drenkard E, (2003) Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect Immun 71: 2404-2413.
35. Hauser AR, Cobb E, Bodi M, Mariscal D, Valles J, et al. (2002) Type III protein secretion is associated with poor clinical outcomes in patients with ventilator-associated pneumonia caused by Pseudomonas aeruginosa. Crit Care Med 30: 521-528.
36. Lyczak JB, Cannon CL, Pier GB, (2000) Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2: 1051-1060.
37. Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, et al. (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci U S A 97: 8815-8821.
38. Kang PJ, Hauser AR, Apodaca G, Fleiszig SMJ, Wiener J, et al. (1997) Identification of Pseudomonas aeruginosa genes required for epithelial cell injury. Mol Microbiol 24: 1249-1262.
39. Hollsing AE, Granstrom M, Vasil ML, Wretlind B, Strandvik B, (1987) Prospective study of serum antibodies to Pseudomonas-Aeruginosa exoproteins in Cystic Fibrosis. J Clin Microbiol 25: 1868-1874.
40. Kurioka S, Matsuda M, (1976) Phospholipase C assay using p-nitrophenylphosphoryl-choline together with sorbitol and its application to studying the metal and detergent requirement of the enzyme. Anal Biochem 75: 281-289.
41. Wargo MJ, Gross MJ, Rajamani S, Allard JL, Lundblad LK, et al. (2011) Hemolytic phospholipase C inhibition protects lung function during Pseudomonas aeruginosa infection. Am J Respir Crit Care Med 184: 345-354.
42. Klein S, Lorenzo C, Hoffmann S, Walther JM, Storbeck S, et al. (2009) Adaptation of Pseudomonas aeruginosa to various conditions includes tRNA-dependent formation of alanyl-phosphatidylglycerol. Mol Microbiol 71: 551-565.
43. Bogdanov M, Mileykovskaya E, Dowhan W, (2008) Lipids in the assembly of membrane proteins and organization of protein supercomplexes: implications for lipid-linked disorders. Subcell Biochem 49: 197-239.
44. Zhang W, Campbell HA, King SC, Dowhan W, (2005) Phospholipids as determinants of membrane protein topology. Phosphatidylethanolamine is required for the proper topological organization of the gamma-aminobutyric acid permease (GabP) of Escherichia coli. J Biol Chem 280: 26032-26038.
45. Neidhardt FC, Bloch PL, Smith DF, (1974) Culture medium for enterobacteria. J Bacteriol 119: 736-747.
46. Schweizer HD, (1993) Small broad-host-range gentamycin resistance gene cassettes for site-specific insertion and deletion mutagenesis. Biotechniques 15: 831-834.
47. Choi KH, Schweizer HP, (2006) mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc 1: 153-161.
48. Folch J, Lees M, Stanley GHS, (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497-509.
49. Stewart JC, (1980) Colorimetric determination of phospholipids with ammonium ferrothiocyanate. Anal Biochem 104: 10-14.
50. O'Toole GA, Gibbs KA, Hager PW, Phibbs PV Jr, Kolter R, (2000) The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J Bacteriol 182: 425-431.
51. Murad AM, Leng P, Straffon M, Wishart J, Macaskill S, et al. (2001) NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. Embo J 20: 4742-4752.
52. Bochner BR, (2009) Global phenotypic characterization of bacteria. FEMS Microbiol Rev 33: 191-205.
53. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG, et al. (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
54. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
55. Shortridge VD, Lazdunski A, Vasil ML, (1992) Osmoprotectants and phosphate regulate expression of phospholipase C in Pseudomonas aeruginosa. Mol Microbiol 6: 863-871.
56. Schweizer HP, (1991) Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene 97: 109-121.