The biosynthesis of Pseudomonas aeruginosa alginate: Regulation of a virulence factor;La biosynthese des alginates chez Pseudomonas aeruginosa: Regulation de l'expression d'un facteur de virulence

Bulletin de l'Institut Pasteur

Volumn 94, Issue 2, 1996, Pages 139-149

  Pasquier, C ^a   Dournes, J L ^a   Chabanon, G ^a   Marty, N ^a  

^a CHU RANGUEIL   (France)

Author keywords

algD gene; alginate; alternative sigma factors; biosynthesis; cystic fibrosis; muc gene; Pseudomonas aeruginosa; regulation; review; virulence

Indexed keywords

ALGINIC ACID; SIGMA FACTOR;

BACTERIAL VIRULENCE; BIOSYNTHESIS; GENE EXPRESSION REGULATION; NONHUMAN; PSEUDOMONAS AERUGINOSA; REVIEW;

BACTERIA (MICROORGANISMS); PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 0029815871     PISSN: 00202452     EISSN: None     Source Type: Journal    
DOI: 10.1016/0020-2452(96)81740-4     Document Type: Review

References (71)

1. [1] Marty, N. & Chabanon, G. (1992), Pseudomonas aeruginosa dans la mucoviscidose. Revue française des laboratoires, 249, 103-107.
2. [2] Pedersen, S.S. (1992), Lung infection with alginate-producing, mucoid Pseudomonas aeruginosa in cystic fibrosis. Acta Pathol. Microbiol. Immunol. Scand., 100, 1-79.
3. [3] Buret, A. & Cripps, A.W. (1993), The immunoevasive activities of Pseudomonas aeruginosa. Relevance for cystic fibrosis. Am. Rev. Respir. Dis., 148, 793-805.
4. [4] Gordon, C.A., Hodges, N.A. & Mariott, C. (1988), Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. J. Antimicrob. Chemother., 22, 667-674.
5. [5] Marcus, H., Austria, A. & Baker, N.R. (1989), Adherence of Pseudomonas aeruginosa to tracheal epithelium. Infect. Immun., 57, 1050-1053.
6. [6] Marty, N., Dournes, J.-L., Chabanon, G. & Montrozier, H. (1992), Influence of nutrient media on the chemical composition of the exopolysaccharide from mucoid and non-mucoid Pseudomonas aeruginosa. FEMS Microbiol. Lett., 98, 35-44.
7. [7] Gacesa, P. & Russell, N.J. (1990), The structure and properties of alginate, in "Pseudomonas infection and alginates". Biochemistry, genetics and pathology (Gacesa, P. & Russell, N.J.) (pp. 29-49). Chapman and Hall, London.
8. [8] Woods, D.E., Sokol, P.A., Bryan, L.E., Storey, D.G., Mattingly, S.J., Vogel, H.J. & Ceri, H. (1991), In vivo regulation of virulence in Pseudomonas aeruginosa associated with genetic rearrangement. J. Infect. Dis., 163, 143-149.
9. [9] Fett, W.F., Wijey, C. & Lifson, E.R. (1992), Occurrence of alginate gene sequences among members of the pseudomonad rRNA homology groups I-IV. FEMS Microbiol. Lett., 99, 151-158.
10. [10] Narbad, A., Hewlins, M.J., Gacesa, P. & Russell, N.J. (1990), The use of 13C-n.m.r. spectroscopy to monitor alginate biosynthesis in mucoid Pseudomonas aeruginosa. Biochem. J., 267, 579-584.
11. [11] May, T.B., Shinabarger, D., Maharaj, R., Kato, J., Chu, L., DeVault, J.D., Roychoudhury, S., Zielinski, N.A., Berry, A., Rothmel, R.K., Misra, T.K. & Chakrabarty, A.M. (1991), Alginate synthesis by Pseudomonas aeruginosa: a key pathogenic factor in chronic pulmonary infections of cystic fibrosis patients. Clin. Microbiol. Rev., 4, 191-206.
12. [12] Tatnell, P.J., Russell, N.J. & Gacesa, P. (1994), GDP-mannose dehydrogenase is the key regulatory enzyme in alginate biosynthesis in Pseudomonas aeruginosa: evidence from metabolite studies. Microbiology, 140, 1745-1754.
13. [13] Darzins, A., Wang, S.-K., Vanags, R.I. & Chakrabarty, A.M. (1985), Clustering of mutations affecting alginic acid biosynthesis in mucoid Pseudomonas aeruginosa. J. Bacteriol., 164, 516-524.
14. [14] Tatnell, P.J., Russell, N.J. & Gacesa, P. (1993), A metabolic study of the activity of GDP-mannose dehydrogenase and concentrations of activated intermediates of alginate biosynthesis in Pseudomonas aeruginosa. J. Gen. Microbiol., 139, 119-127.
15. [15] May, T.B. & Chakrabarty, A.M. (1994), Pseudomonas aeruginosa: genes and enzymes of alginate synthesis. Trends Microbiol., 2, 151-157.
16. [16] Rehm, B.H.A., Boheim, G., Tommassen, J. & Winkler, U.K. (1994), Overexpression of algE in Escherichia coli: subcellular localization, purification, and ion channel properties. J. Bacteriol., 176, 5639-5647.
17. [17] Franklin, M.J., Chitnis, C.E., Gacesa, P., Sonesson, A., White, D.C. & Ohman, D.E. (1994), Pseudomonas aeruginosa AlgG is a polymer level alginate C5-mannuronan epimerase. J. Bacteriol., 176, 1821-1830.
18. [18] Monday, S.R. & Schiller, N.L. (1996), Alginate synthesis in Pseudomonas aeruginosa - the role of algL (alginate lyase) and algX. J. Bacteriol., 178, 625-632.
19. [19] Schiller, N.L., Monday, S.R., Boyd, C.M., Keen, N.T. & Ohman, D.E. (1993), Characterization of the Pseudomonas aeruginosa alginate lyase gene (algL): cloning, sequencing, and expression in Escherichia coli. J. Bacteriol., 175, 4780-4789.
20. [20] Franklin, M.J. & Ohman, D.E. (1993), Identification of algF in the alginate biosynthetic gene cluster of Pseudomonas aeruginosa which is required for alginate acetylation. J. Bacteriol., 175, 5057-5065.
21. [21] May, T.B., Shinabarger, D., Boyd, A. & Chakrabarty, A.M. (1994), Identification of amino acid residues involved in the activity of phosphomannose isomerase-guanosine 5'-diphospho-D-mannose pyrophosphorylase. J. Biol. Chem., 269, 4872-4877.
22. [22] Lightfoot, J. & Lam, J.S. (1993), Chromosomal mapping, expression and synthesis of lipopolysaccharide in Pseudomonas aeruginosa: a role for guanosine diphospho (GDP)-D-mannose. Mol. Microbiol., 8, 771-782.
23. [23] Coyne, M.J., Russell, K.S., Coyle, C.L. & Goldberg, J.B. (1994), The Pseudomonas aeruginosa algC gene encodes phosphoglucomutase, required for synthesis of a complete lipopolysaccharide core. J. Bacteriol., 176, 3500-3507.
24. [24] Kato, J., Chu, L., Kitano, K., DeVault, J.D., Kimbara, K., Chakrabarty, A.M. & Misra, T.K. (1989), Nucleotide sequence of a regulatory region controlling alginate synthesis in Pseudomonas aeruginosa: characterization of the algR2 gene. Gene, 84, 31-38.
25. [25] Konyecsni, W.M. & Deretic, V. (1990), DNA sequence and expression analysis of algP and algQ, components of the multigene system transcriptionally regulating mucoidy in Pseudomonas aeruginosa: algP contains multiple direct repeats. J. Bacteriol., 172, 2511-2520.
26. [26] Goldberg, J.B. & Dahnke, T. (1992), Pseudomonas aeruginosa algB, which modulates the expression of alginate, is a member of the NtrC subclass of prokaryotic regulators. Mol. Microbiol., 6, 59-66.
27. [27] Chitnis, C.E. & Ohman, D.E. (1993), Genetic analysis of the alginate biosynthetic gene cluster of Pseudomonas aeruginosa shows evidence of an operonic structure. Mol. Microbiol., 8, 583-590.
28. [28] Deretic, V., Dikshit, R., Konyecsni, W.N., Chakrabarty, A.M. & Misra, T.K. (1989), The algR gene, which regulates mucoidy in Pseudomonas aeruginosa, belongs to a class of environmentally responsive genes. J. Bacteriol., 171, 1278-1283.
29. [29] Hellingwerf, K.J., Postma, P.W., Tommassen, J. & Westerhoff, H.V. (1995), Signal transduction in bacteria: phospho-neural network(s) in Escherichia coli? FEMS Microbiol. Rev., 16, 309-321.
30. [30] Deretic, V., Schurr, M.J., Boucher, J.C. & Martin, D.W. (1994), Conversion of Pseudomonas aeruginosa to mucoidy in cystic fibrosis: environmental stress and regulation of bacterial virulence by alternative sigma factor. J. Bacteriol., 176, 2773-2780.
31. [31] Roychoudhury, S., Sakai, K., Schlictman, D. & Chakrabarty, A.M. (1992), Signal transduction in exopolysaccharide alginate synthesis: phosphorylation of the response regulator AlgR1 in Pseudomonas aeruginosa and Escherichia coli. Gene, 112, 45-51.
32. [32] Shankar, S., Schlictman, D. & Chakrabarty, A.M. (1995), Regulation of nucleoside diphosphate kinase and an alternative kinase in Escherichia coli - role of the sspa and rnk genes in nucleoside triphosphate formation. Mol. Microbiol., 17, 935-943.
33. [33] Roychoudhury, S., Zielinski, N.A., Ninfa, A.J., Allen, N.E., Jungheim, L.N., Nicas, T.I. & Chakrabarty, A.M. (1993), Inhibitors of two-component signal transduction systems: inhibition of alginate gene activation in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA, 90, 965-969.
34. [34] Deretic, V., Leveau, J.H.J., Mohr, C.D. & Hibler, N.S. (1992), In vitro phosphorylation of AlgR, a regulator of mucoidy in Pseudomonas aeruginosa, by a histidine protein kinase and effects of small phosphodonor molecules. Mol. Microbiol., 6, 2761-2767.
35. [35] Schlictman, D., Shankar, S. & Chakrabarty, A.M. (1995), The Escherichia coli genes sspA and rnk can functionally replace the Pseudomonas aeruginosa alginate regulatory gene algR2. Mol. Microbiol., 16, 309-320.
36. [36] Mohr, C.D., Leveau, J.H.J., Krieg, D.P., Hibler, N.S. & Deretic, V. (1992), AlgR-binding sites within the algD promoter make up a set of inverted repeats separated by a large intervening segment of DNA. J. Bacteriol., 174, 6624-6633.
37. [37] Zielinski, N.A., Maharaj, R., Roychoudhury, S., Danganan, C.E., Hendrickson, W. & Chakrabarty, A.M. (1992), Alginate synthesis in Pseudomonas aeruginosa: environmental regulation of the algC promoter. J. Bacteriol., 174, 7680-7688.
38. [38] Fujiwara, S., Zielinski, N.A. & Chakrabarty, A.M. (1993), Enhancer-like activity of AlgR1-binding site in alginate gene activation: positional, orientational, and sequence specificity. J. Bacteriol., 175, 5452-5459.
39. [39] Perez-Martin, J., Rojo, F. & DeLorenzo, V. (1994), Promoters responsive to DNA bending: a common theme in prokaryotic gene expression. Microbiol. Rev., 58, 268-290.
40. p1), a histone-like element participating in control of mucoidy in Pseudomonas aeruginosa. J. Bacteriol., 174, 824-831.
41. [41] Mohr, C.D. & Deretic, V. (1992), In vitro interactions of the histone-like protein IHF with the algD promoter, a critical site for control of mucoidy in Pseudomonas aeruginosa. Biochem. Biophys. Res. Commun., 189, 837-844.
42. [42] DeVault, J.D., Hendrickson, W., Kato, J. & Chakrabarty, A.M. (1991), Environmentally regulated algD promoter is responsive to cAMP receptor protein in Escherichia coli. Mol Microbiol., 5, 2503-2509.
43. [43] Wozniak, D.J. & Ohman, D.E. (1991), Pseudomonas aeruginosa algB, a two-component response regulator of the NtrC family, is required for algD transcription. J. Bacteriol., 173, 1406-1413.
44. [44] Goldberg, J.B. & Ohman, D.E. (1987), Construction and characterization of Pseudomonas aeruginosa algB mutants: role of algB in high-level production of alginate. J. Bacteriol., 169, 1593-1602.
45. [45] DeVault, J.D., Kimbara, K. & Chakrabarty, A.M. (1990), Pulmonary dehydration and infection in cystic fibrosis: evidence that ethanol activates alginate gene expression and induction of mucoidy in Pseudomonas aeruginosa. Mol. Microbiol., 4, 737-745.
46. [46] Terry, J.M., Piña, S.E. & Mattingly, S.J. (1991), Environmental conditions which influence mucoid conversion in Pseudomonas aeruginosa PAO1. Infect. Immun., 59, 471-477.
47. [47] Bayer, A.S., Eftekhar, F., Tu, J., Nast, C.C. & Speert, D.P. (1990), Oxygen-dependent up-regulation of mucoid exopolysaccharide (alginate) production in Pseudomonas aeruginosa. Infect. Immun., 58, 1344-1349.
48. [48] Leitão, J.H. & Sá-Correia, I. (1993), Oxygen-dependent alginate synthesis and enzymes in Pseudomonas aeruginosa. J. Gen. Microbiol., 139, 441-445.
49. [49] Leitão, J.H., Fialho, A.M. & Sá-Correia, I. (1992), Effects of growth temperature on alginate synthesis and enzymes in Pseudomonas aeruginosa variants. J. Gen. Microbiol., 138, 605-610.
50. [50] Mohr, C.D., Sonsteby, S.K. & Deretic, V. (1994), The Pseudomonas aeruginosa homologs of hemC and hemD are linked to the gene encoding the regulator of mucoidy AlgR. Mol. Gen. Genet., 242, 177-184.
51. [51] Deretic, V., Martin, D.W., Shurr, M.J., Mudd, M.H., Hibler, N.S., Curcic, R. & Boucher, J.C. (1993), Conversion to mucoidy in Pseudomonas aeruginosa. Bio/Technology, 11, 1133-1136.
52. [52] Boucher, J.C., Martinezsalazar, J., Schurr, M.J., Mudd, M.H., Yu, H. & Deretic, V. (1996), Two distinct loci affecting conversion to mucoidy in Pseudomonas aeruginosa in cystic fibrosis encode homologs of the serine protease htra. J. Bacteriol., 178, 511-523.
53. [53] Yu, H., Schurr, M.J. & Deretic, V. (1995), Functional equivalence of Escherichia coli sigma E and Pseudomonas aeruginosa AlgU : E. coli rpoE restores mucoidy and reduces sensitivity to reactive oxygen intermediates in algU mutants of P. aeruginosa. J. Bacteriol., 177, 3259-3268.
54. [54] Schurr, M.J., Martin, D.W., Mudd, M.H. & Deretic, V. (1994), Gene cluster controlling conversion to alginate-overproducing phenotype in Pseudomonas aeruginosa: functional analysis in a heterologous host and role in the instability of mucoidy. J. Bacteriol., 176, 3375-3382.
55. [55] Martin, D.W., Schurr, M.J., Mudd, M.H., Govan, J.R.W., Holloway, B.W. & Deretic, V. (1993), Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc. Natl. Acad. Sci. USA, 90, 8377-8381.
56. [56] Martin, D.W., Schurr, M.J., Mudd, M.H. & Deretic, V. (1993), Differentiation of Pseudomonas aeruginosa into the alginate-producing form: inactivation of mucB causes conversion to mucoidy. Mol. Microbiol., 9, 497-506.
57. [57] DeVries, C.A. & Ohman, D.E. (1994), Mucoid-to-non-mucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation. J. Bacteriol., 176, 6677-6687.
58. [58] Schurr, M.J., Yu, H., Boucher, J.C., Hibler, N.S. & Deretic, V. (1995), Multiple promoters and induction by heat shock of the gene encoding the alternative sigma factor algU (sigma E) which controls mucoidy in cystic fibrosis isolates of Pseudomonas aeruginosa. J. Bacteriol., 177, 5670-5679.
59. [59] Sokol, P.A., Luan, M.-Z., Storey, D.G. & Thirukkumaran, P. (1994), Genetic rearrangement associated with in vivo mucoid conversion of Pseudomonas aeruginosa PAO1 is due to insertion elements. J. Bacteriol., 176, 553-562.
60. [60] Martin, D.W., Holloway, B.W. & Deretic, V. (1993), Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: algU shows sequence similarities with a Bacillus sigma-factor. J. Bacteriol., 175, 1153-1164.
61. [61] Allan, B., Linseman, M., MacDonald, L.A., Lam, J.S. & Kropinski, A.M. (1988), Heat shock response of Pseudomonas aeruginosa. J. Bacteriol., 170, 3668-3674.
62. [62] Tanaka, K. & Takahashi, H. (1991), Cloning and analysis of the gene (rpoDA) for the principal a factor of Pseudomonas aeruginosa. Biochim. Biophys. Acta., 1089, 113-119.
63. 32-like RNA polymerase in rpoDA gene expression. J. Bacteriol., 175, 1069-1074.
64. [64] Fujita, M., Tanaka, K., Takahashi, H. & Amemura, A. (1994), Transcription of the principal sigma-factor genes, rpoD and rpoS, in Pseudomonas aeruginosa is controlled according to the growth phase. Mol. Microbiol., 13, 1071-1077.
65. [65] Starnbach, M.N. & Lory, S. (1992), The fliA (rpoF) gene of Pseudomonas aeruginosa encodes an alternative sigma factor required for flagellin synthesis. Mol. Microbiol., 6, 459-469.
66. [66] Jin, S., Ishimoto, K. & Lory, S. (1994), Nucleotide sequence of the rpoN gene and characterization of two downstream open reading frames in Pseudomonas aeruginosa. J. Bacteriol., 176, 1316-1322.
67. [67] Benvenisti, L., Koby, S., Rutman, A., Giladi, H., Yura, T. & Oppenheim, A.B. (1995), Cloning and primary sequence of the rpoH gene from Pseudomonas aeruginosa. Gene, 155, 73-76.
68. [68] Deretic, V., Schurr, M.J. & Yu, H. (1995), Pseudomonas aeruginosa, mucoidy and the chronic infection phenotype in cystic fibrosis. Trends Microbiol., 3, 351-356.
69. [69] Wozniak, D.J. & Ohman, D.E. (1994), Transcriptional analysis of the Pseudomonas aeruginosa genes algR, algB, and algD reveals a hierarchy of alginate gene expression which is modulated by algT. J. Bacteriol., 176, 6007-6014.
70. [70] Davies, D.G., Chakrabarty, A.M. & Geesey, G.G. (1993), Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl. Environ. Microbiol., 59, 1181-1186.
71. [71] Boyd, A. & Chakrabarty, A.M. (1994), Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl. Environ. Microbiol., 60, 2355-2359.