Interkingdom adenosine signal reduces Pseudomonas aeruginosa pathogenicity

Microbial Biotechnology

Volumn 5, Issue 4, 2012, Pages 560-572

  Sheng, Lili ^a,b   Pu, Mingming ^a   Hegde, Manjunath ^a   Zhang, Yuanxing ^b   Jayaraman, Arul ^a   Wood, Thomas K ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; ELASTASE; FERRIC UPTAKE REGULATOR; PYOCYANINE; RHAMNOLIPID; SIDEROPHORE; VIRULENCE FACTOR;

ARTICLE; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BIOFILM; BIOSYNTHESIS; CAENORHABDITIS ELEGANS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE CONTROL; HYDROLYSIS; IRON TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION;

ADENOSINE; ANIMALS; BIOFILMS; CAENORHABDITIS ELEGANS; GENE EXPRESSION PROFILING; GLYCOLIPIDS; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; VIRULENCE; VIRULENCE FACTORS;

EID: 84862028018     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/j.1751-7915.2012.00338.x     Document Type: Article

References (63)

1. Alverdy, J., Holbrook, C., Rocha, F., Seiden, L., Wu, R.L., Musch, M., etal. (2000) Gut-derived sepsis occurs when the right pathogen with the right virulence genes meets the right host: evidence for in vivo virulence expression in Pseudomonas aeruginosa. Ann Surg 232: 480-489.
2. Andrews, S.C., Robinson, A.K., and Rodríguez-Quiñones, F. (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215-237.
3. Attila, C., Ueda, A., and Wood, T.K. (2008) PA2663 (PpyR) increases biofilm formation in Pseudomonas aeruginosa PAO1 through the psl operon and stimulates virulence and quorum-sensing phenotypes. Appl Microbiol Biotechnol 78: 293-307.
4. Bansal, T., Englert, D., Lee, J., Hegde, M., Wood, T.K., and Jayaraman, A. (2007) Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun 75: 4597-4607.
5. Bansal, T., Alaniz, R.C., Wood, T.K., and Jayaraman, A. (2010) The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc Natl Acad Sci USA 107: 228-233.
6. Bjorn, M.J., Sokol, P.A., and Iglewski, B.H. (1979) Influence of iron on yields of extracellular products in Pseudomonas aeruginosa cultures. J Bacteriol 138: 193-200.
7. Bodey, G.P., Bolivar, R., Fainstein, V., and Jadeja, L. (1983) Infections caused by Pseudomonas aeruginosa. Rev Infect Dis 5: 279-313.
8. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
9. Caiazza, N.C., Shanks, R.M., and O'Toole, G.A. (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187: 7351-7361.
10. Calderwood, S.B., and Mekalanos, J.J. (1987) Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J Bacteriol 169: 4759-4764.
11. Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., Bassler, B.L., and Hughson, F.M. (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545-549.
12. Cornelis, P., Matthijs, S., and Van Oeffelen, L. (2009) Iron uptake regulation in Pseudomonas aeruginosa. Biometals 22: 15-22.
13. Costerton, J.W., Stewart, P.S., and Greenberg, E.P. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
14. Crane, J.K., and Shulgina, I. (2009) Feedback effects of host-derived adenosine on enteropathogenic Escherichia coli. FEMS Immunol Med Microbiol 57: 214-228.
15. Crane, J.K., Olson, R.A., Jones, H.M., and Duffey, M.E. (2002) Release of ATP during host cell killing by enteropathogenic E.coli and its role as a secretory mediator. Am J Physiol Gastrointest Liver Physiol 283: G74-G86.
16. Daniels, R., Vanderleyden, J., and Michiels, J. (2004) Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 28: 261-289.
17. Diggle, S.P., Cornelis, P., Williams, P., and Cámara, M. (2006) 4-Quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int J Med Microbiol 296: 83-91.
18. Egan, L.J., Sandborn, W.J., Mays, D.C., Tremaine, W.J., and Lipsky, J.J. (1999) Plasma and rectal adenosine in inflammatory bowel disease: effect of methotrexate. Inflamm Bowel Dis 5: 167-173.
19. Essar, D.W., Eberly, L., Hadero, A., and Crawford, I.P. (1990) Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J Bacteriol 172: 884-900.
20. Farrow, J.M., 3rd, and Pesci, E.C. (2007) Two distinct pathways supply anthranilate as a precursor of the Pseudomonas quinolone signal. J Bacteriol 189: 3425-3433.
21. Feldman, M., Bryan, R., Rajan, S., Scheffler, L., Brunnert, S., Tang, H., and Prince, A. (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43-51.
22. Freestone, P.P., Haigh, R.D., Williams, P.H., and Lyte, M. (1999) Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers. FEMS Microbiol Lett 172: 53-60.
23. Fuqua, W.C., Winans, S.C., and Greenberg, E.P. (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176: 269-275.
24. González Barrios, A.F., Zuo, R., Hashimoto, Y., Yang, L., Bentley, W.E., and Wood, T.K. (2006) Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 188: 305-316.
25. Haskó, G., and Cronstein, B.N. (2004) Adenosine: an endogenous regulator of innate immunity. Trends Immunol 25: 33-39.
26. Hassett, D.J., Howell, M.L., Ochsner, U.A., Vasil, M.L., Johnson, Z., and Dean, G.E. (1997) An operon containing fumC and sodA encoding fumarase C and manganese superoxide dismutase is controlled by the ferric uptake regulator in Pseudomonas aeruginosa: fur mutants produce elevated alginate levels. J Bacteriol 179: 1452-1459.
27. Hegde, M., Wood, T.K., and Jayaraman, A. (2009) The neuroendocrine hormone norepinephrine increases Pseudomonas aeruginosa PA14 virulence through the las quorum-sensing pathway. Appl Microbiol Biotechnol 84: 763-776.
28. Heurlier, K., Dénervaud, V., and Haas, D. (2006) Impact of quorum sensing on fitness of Pseudomonas aeruginosa. Int J Med Microbiol 296: 93-102.
29. Heydorn, A., Nielsen, A.T., Hentzer, M., Sternberg, C., Givskov, M., Ersbøll, B.K., and Molin, S. (2000) Quantification of biofilm structures by the novel computer program comstat. Microbiology 146: 2395-2407.
30. Jahoor, A., Patel, R., Bryan, A., Do, C., Krier, J., Watters, C., etal. (2008) Peroxisome proliferator-activated receptors mediate host cell proinflammatory responses to Pseudomonas aeruginosa autoinducer. J Bacteriol 190: 4408-4415.
31. Kimura, Y., Turner, J.R., Braasch, D.A., and Buddington, R.K. (2005) Lumenal adenosine and AMP rapidly increase glucose transport by intact small intestine. Am J Physiol Gastrointest Liver Physiol 289: G1007-G1014.
32. Kohler, J.E., Zaborina, O., Wu, L., Wang, Y., Bethel, C., Chen, Y., etal. (2005) Components of intestinal epithelial hypoxia activate the virulence circuitry of Pseudomonas. Am J Physiol Gastrointest Liver Physiol 288: G1048-G1054.
33. Kuchma, S.L., Brothers, K.M., Merritt, J.H., Liberati, N.T., Ausubel, F.M., and O'Toole, G.A. (2007) BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189: 8165-8178.
34. Laughlin, R.S., Musch, M.W., Hollbrook, C.J., Rocha, F.M., Chang, E.B., and Alverdy, J.C. (2000) The key role of Pseudomonas aeruginosa PA-I lectin on experimental gut-derived sepsis. Ann Surg 232: 133-142.
35. Lee, J., Attila, C., Cirillo, S.L., Cirillo, J.D., and Wood, T.K. (2009) Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol 2: 75-90.
36. Lee, V.T., Matewish, J.M., Kessler, J.L., Hyodo, M., Hayakawa, Y., and Lory, S. (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65: 1474-1484.
37. Liberati, N.T., Urbach, J.M., Miyata, S., Lee, D.G., Drenkard, E., Wu, G., etal. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci USA 103: 2833-2838.
38. Marshall, J.C., Christou, N.V., and Meakins, J.L. (1993) The gastrointestinal tract. The 'undrained abscess' of multiple organ failure. Ann Surg 218: 111-119.
39. Martínez-Granero, F., Capdevila, S., Sánchez-Contreras, M., Martín, M., and Rivilla, R. (2005) Two site-specific recombinases are implicated in phenotypic variation and competitive rhizosphere colonization in Pseudomonas fluorescens. Microbiology 151: 975-983.
40. Mey, A.R., Wyckoff, E.E., Kanukurthy, V., Fisher, C.R., and Payne, S.M. (2005) Iron and Fur regulation in Vibrio cholerae and the role of Fur in virulence. Infect Immun 73: 8167-8178.
41. O'Toole, G.A., and Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
42. Ochsner, U.A., Vasil, A.I., and Vasil, M.L. (1995) Role of the ferric uptake regulator of Pseudomonas aeruginosa in the regulation of siderophores and exotoxin A expression: purification and activity on iron-regulated promoters. J Bacteriol 177: 7194-7201.
43. Ochsner, U.A., Wilderman, P.J., Vasil, A.I., and Vasil, M.L. (2002) GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45: 1277-1287.
44. Ohman, D.E., Cryz, S.J., and Iglewski, B.H. (1980) Isolation and characterization of Pseudomonas aeruginosa PAO mutant that produces altered elastase. J Bacteriol 142: 836-842.
45. Overhage, J., Bains, M., Brazas, M.D., and Hancock, R.E. (2008) Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190: 2671-2679.
46. Patel, N.J., Zaborina, O., Wu, L., Wang, Y., Wolfgeher, D.J., Valuckaite, V., etal. (2007) Recognition of intestinal epithelial HIF-1alpha activation by Pseudomonas aeruginosa. Am J Physiol Gastrointest Liver Physiol 292: G134-G142.
47. Rasko, D.A., and Sperandio, V. (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9: 117-128.
48. Ren, D., Bedzyk, L.A., Thomas, S.M., Ye, R.W., and Wood, T.K. (2004) Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64: 515-524.
49. Roman, R.M., and Fitz, J.G. (1999) Emerging roles of purinergic signaling in gastrointestinal epithelial secretion and hepatobiliary function. Gastroenterology 116: 964-979.
50. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.
51. Schook, L.B., Carrick, L., and Berk, R.S. (1976) Murine gastrointestinal tract as a portal of entry in experimental Pseudomonas aeruginosa infections. Infect Immun 14: 564-570.
52. Schwyn, B., and Neilands, J.B. (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160: 47-56.
53. Sheikh, M.A., and Taylor, G.L. (2009) Crystal structure of the Vibrio cholerae ferric uptake regulator (Fur) reveals insights into metal co-ordination. Mol Microbiol 72: 1208-1220.
54. Shimizu, K., Ogura, H., Goto, M., Asahara, T., Nomoto, K., Morotomi, M., etal. (2006) Altered gut flora and environment in patients with severe SIRS. J Trauma 60: 126-133.
55. Sritharan, M. (2006) Iron and bacterial virulence. Indian J Med Microbiol 24: 163-164.
56. Tan, M.W., Mahajan-Miklos, S., and Ausubel, F.M. (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci USA 96: 715-720.
57. Thammavongsa, V., Kern, J.W., Missiakas, D.M., and Schneewind, O. (2009) Staphylococcus aureus synthesizes adenosine to escape host immune responses. J Exp Med 206: 2417-2427.
58. Ueda, A., and Wood, T.K. (2010) Tyrosine phosphatase TpbA of Pseudomonas aeruginosa controls extracellular DNA via cyclic diguanylic acid concentrations. Environ Microbiol 2: 449-455.
59. Venturi, V., Weisbeek, P., and Koster, M. (1995) Gene regulation of siderophore-mediated iron acquisition in Pseudomonas: not only the Fur repressor. Mol Microbiol 17: 603-610.
60. Wolkow, C.A., Kimura, K.D., Lee, M.S., and Ruvkun, G. (2000) Regulation of C.elegans life-span by insulinlike signaling in the nervous system. Science 290: 147-150.
61. Xu, J., and Gordon, J.I. (2003) Honor thy symbionts. Proc Natl Acad Sci USA 100: 10452-10459.
62. Zhang, X.S., García-Contreras, R., and Wood, T.K. (2008) Escherichia coli transcription factor YncC (McbR) regulates colanic acid and biofilm formation by repressing expression of periplasmic protein YbiM (McbA). ISME J 2: 615-631.
63. Zheng, P., Sun, J., Geffers, R., and Zeng, A.P. (2007) Functional characterization of the gene PA2384 in large-scale gene regulation in response to iron starvation in Pseudomonas aeruginosa. J Biotechnol 132: 342-352.