Phosphorylation-independent activity of the response regulators AlgB and AlgR in promoting alginate biosynthesis in mucoid Pseudomonas aeruginosa

Journal of Bacteriology

Volumn 180, Issue 4, 1998, Pages 956-968

  Ma, Sheng ^a   Selvaraj, Uma ^b   Ohman, Dennis E ^a   Quarless, Ryan ^b   Hassett, Daniel J ^c   Wozniak, Daniel J ^b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; ASPARTIC ACID; HEXAHISTIDINE; NICKEL; PROTEIN HISTIDINE KINASE; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; CARBOHYDRATE METABOLISM; CYSTIC FIBROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PSEUDOMONAS AERUGINOSA; REGULATOR GENE; SIGNAL TRANSDUCTION;

NEGIBACTERIA; PROKARYOTA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 0031931507     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.4.956-968.1998     Document Type: Article

References (68)

1. Ausubel, F. M., R. Brent, E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1987. Current protocols in molecular biology. Green Publishing Associates and John Wiley-Interscience, New York, N.Y.
2. Baldus, J. M., B. D. Green, P. Youngman, and C. P. Moran, Jr. 1994. Phosphorylation of Bacillus subtilis transcription factor Spo0A stimulates transcription from the spoIIG promoter by enhancing binding to weak 0A boxes. J. Bacteriol. 176:296-306.
3. Baynham, P. J., and D. J. Wozniak. 1996. Identification and characterization of AIgZ, an AlgT-dependent DNA binding protein required for Pseudomonas aeruginosa algD transcription. Mol. Microbiol. 22:97-108.
4. Becker, A., M. Schmidt, W. Jager, and A. Puhler. 1995. New gentamicin-resistance and lacZ promoter-probe cassettes suitable for insertion mutagenesis and generation of transcriptional fusions. Gene 162:37-39.
5. Bourret, R. B., J. F. Hess, and M. I. Simon. 1990. Conserved aspartate residues and phosphorylation in signal transduction by the chemotaxis protein CheY. Proc. Natl. Acad. Sci. USA 87:41-45.
6. Boyd, J., and S. Lory. 1996. Dual function of PilS during transcriptional activation of the Pseudomonas aeruginosa pilin subunit gene. J. Bacteriol. 178:831-839.
7. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
8. Chitnis, C. E., and D. E. Ohman. 1993. Genetic analysis of the alginate biosynthetic gene cluster of Pseudomonas aeruginosa shows evidence for an operonic structure. Mol. Microbiol. 8:583-590.
9. Delgado, J., S. Forst, S. Harlocker, and M. Inouye. 1993. Identification of a phosphorylation site and functional analysis of conserved aspartic acid residues of OmpR, a transcriptional activator for ompF and ompC in Escherichia coli. Mol. Microbiol. 10:1037-1047.
10. Deretic, V., R. Dikshit, M. Konyecsni, A. M. Chakrabarty, and T. K. Misra. 1989. The algR gene, which regulates mucoidy in Pseudomonas aeruginosa, belongs to a class of environmentally responsive genes. J. Bacteriol. 171: 1278-1283.
11. Deretic, V., J. F. Gill, and A. M. Chakrabarty. 1987. Gene algD coding for GDPmannose dehydrogenase is transcriptionally activated in mucoid Pseudomonas aeruginosa. J. Bacteriol. 169:351-358.
12. Deretic, V., H. J. Leveau, C. D. Mohr, and N. S. Hibler. 1992. In vitro phosphorylation of AlgR, a regulator of mucoidy in Pseudomonas aeruginosa, by a histidine protein kinase and effects of small phospho-donor molecules. Mol. Microbiol. 6:2761-2767.
13. Devries, C. A., and D. E. Ohman. 1994. Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternative sigma factor, and shows evidence for autoregulation. J. Bacteriol. 176:6677-6687.
14. Dubnau, D., J. Hahn, M. Roggiani, F. Piazza, and Y. Weinrauch. 1994. Two-component regulators and genetic competence in Bacillus subtilis. Res. Microbiol. 145:403-411.
15. Fick, R. B. J., F. Sonoda, and D. B. Hornick. 1992. Emergence and persistence of Pseudomonas aeruginosa in the cystic fibrosis airway. Semin. Respir. Infect. 7:168-178.
16. Fiedler, U., and V. Weiss. 1995. A common switch in activation of the response regulators NtrC and PhoB: phosphorylation induces dimerization of the receiver modules. EMBO J. 14:3696-3705.
17. Figurski, D., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
18. Flynn, J. L., and D. E. Ohman. 1988. Cloning of genes from mucoid Pseudomonas aeruginosa which control spontaneous conversion to the alginate production phenotype. J. Bacteriol. 170:1452-1460.
19. Frankin, M. J., C. E. Chitnis, P. Gacesa, A. Sonesson, D. C. White, and D. E. Ohman. 1994. Pseudomonas aeruginosa AIgG is a polymer level alginate C5-mannuronan epimerase. J. Bacteriol. 176:1821-1830.
20. Goldberg, J. B., W. L. German, J. L. Flynn, and D. E. Ohman. 1993. A mutation in algN permits trans activation of alginate production by algT in Pseudomonas species. J. Bacteriol. 175:1303-1308.
21. Goldberg, J. B., and D. E. Ohman. 1984. Cloning and expression in Pseudomonas aeruginosa of a gene involved in the production of alginate. J. Bacteriol. 158:1115-1121.
22. Goldberg, J. B., and D. E. Ohman. 1987. Construction and characterization of Pseudomonas aeruginosa algB mutants: role of algB in high-level production of alginate. J. Bacteriol. 169:1593-1602.
23. Govan, J. R. W., and V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60:539-574.
24. Jin, S., R. K. Prusti, T. Roitsch, R. G. Ankenbauer, and E. W. Nester. 1990. Phosphorylation of the VirG protein of Agrobacterium tumefaciens by the autophosphorylated VirA protein: essential role in biological activity of VirG. J. Bacteriol. 172:4945-4950.
25. Kato, J., and A. M. Chakrabarty. 1991. Purification of the regulatory protein AIgR1 and its binding in the far upstream region of the algD promoter in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 88:1760-1764.
26. Knutson, C. A., and A. Jeanes. 1968. A new modification of the carbazole analysis: application to heteropolysaccharides. Anal. Biochem. 24:470-481.
27. Lion, T., and O. A. Haas. 1990. Nonradioactive labeling of probe with digoxigenin by polymerase chain reaction. Anal. Biochem. 188:335-337.
28. Lukat, G. S., W. R. McCleary, A. M. Stock, and J. B. Stock. 1992. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc. Natl. Acad. Sci. USA 89:718-722.
29. Ma, S., D. J. Wozniak, and D. E. Ohman. 1997. Identification of the histidine protein kinase KinB in Pseudomonas aeruginosa and its phosphorylation of the alginate regulator AIgB. J. Biol. Chem. 272:17952-17960.
30. Martin, D. W., B. W. Holloway, and V. Deretic. 1993. Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AIgU shows sequence similarities with a Bacillus sigma factor. J. Bacteriol. 175: 1153-1164.
31. Martin, D. W., M. J. Schurr, M. H. Mudd, and V. Deretic. 1993. Differentiation of Pseudomonas aeruginosa into the alginate-producing form: inactivation of mucB causes conversion to mucoidy. Mol. Microbiol. 9:497-506.
32. Martin, D. W., M. J. Schurr, M. H. Mudd, J. R. W. Govan, B. W. Holloway, and V. Deretic. 1993. Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 90: 8377-8381.
33. e and stress response. J. Bacteriol. 176:6688-6696.
34. 22 for expression of the alginate regulon in Pseudomonas aeruginosa and localization of its antagonist proteins MucA and MucB (AlgN). J. Bacteriol. 179:3711-3720.
35. McCleary, W. R., and J. B. Stock. 1994. Acetyl phosphate and the activation of two-component response regulators. J. Biol. Chem. 269:31567-31572.
36. McIver, K. S., E. Kessler, J. C. Olson, and D. E. Ohman. 1995. The elastase propeptide functions as an intramolecular chaperone required for elastase activity and secretion in Pseudomonas aeruginosa. Mol. Microbiol. 18:877-889.
37. Mohr, C. D., J. H. J. Leveau, D. P. Krieg, N. S. Hibler, and V. Deretic. 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.
38. 54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains. J. Bacteriol. 175:6067-6074.
39. Msadek, T., F. Kunst, and G. Rapoport. 1995. A signal transduction network in Bacillus subtilis includes the DegS/DegU and ComP/ComA two-component systems, p. 447-471. In J. A. Hoch and T. J. Silhavy (ed.). Two-component signal transduction. ASM Press, Washington, D.C.
40. Ohman, D. E., and A. M. Chakrabarty. 1981. Genetic mapping of chromosomal determinants for the production of the exopolysaccharide alginate in a Pseudomonas aeruginosa cystic fibrosis isolate. Infect. Immun. 33:142-148.
41. Ohman, D. E., K. Mathee, C. J. McPherson, C. A. DeVries, S. Ma, D. J. Wozniak, and M. J. Franklin. 1996. Regulation of the alginate (algD) operon in Pseudomonas aeruginosa, p. 472-483. In T. Nakazawa, K. Furukawa, D. Haas, and S. Silver (ed.), Molecular biology of pseudomonads. ASM Press, Washington, D.C.
42. Ohman, D. E., M. A. West, J. L. Flynn, and J. B. Goldberg. 1985. Method for gene replacement in Pseudomonas aeroginosa used in construction of recA mutants: recA-independent instability of alginate production. J. Bacteriol. 162:1068-1074.
43. Parkinson, J. S. 1993. Signal transduction schemes of bacteria. Cell 73:857-871.
44. Parkinson, J. S., and E. C. Kofoid. 1992. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26:71-112.
45. Reyrat, J. M., M. David, J. Batut, and P. Boistard. 1994. FixL of Rhizobium meliloti enhances the transcriptional activity of a mutant FixJD54N protein by phosphorylation of an alternate residue. J. Bacteriol. 176:1969-1976.
46. Roychoudhury, S., N. A. Zielinski, A. J. Ninfa, N. E. Allen, L. N. Jungheim, T. I. Nicas, and A. M. Chakrabarty. 1993. Inhibitors of two-component signal transduction systems: inhibition of alginate gene activation in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 90:965-969.
47. Sanders, D. A., B. L. Gillece-Castro, A. L. Burlingame, and D. E. Koshland. 1992. Phosphorylation site of NtrC, a protein phosphatase whose covalent intermediate activates transcription. J. Bacteriol. 174:5117-5122.
48. Sanders, D. A., B. L. Gillece-Castro, and A. M. Stock. 1989. Identification of the site of phosphorylation of the chemotaxis response regulator protein CheY. J. Biol. Chem. 264:21770-21778.
49. Schurr, M. J., and V. Deretic. 1997. Microbial pathogenesis in cystic fibrosis: coordinate regulation of heat-shock response and conversion to mucoidy in Pseudomonas aeruginosa. Mol. Microbiol. 24:411-420.
50. E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruinosa conversion to mucoidy in cystic fibrosis. J. Bacteriol. 178:4997-5004.
51. Schweizer, H. P. 1992. Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker. Mol. Microbiol. 6:1195-1204.
52. Schweizer, H. P. 1993. Small broad-host-range gentamycin resistance cassettes for site-specific insertion and deletion mutagenesis. BioTechniques 15:831-833.
53. Schweizer, H. P., and T. T. Hoang. 1995. An improved system for gene replacement and xy/E fusion analysis in Pseudomonas aeruginosa. Gene 158: 15-22.
54. Staskawicz, B., D. Dahlbeck, N. Keen, and C. Napoli. 1987. Molecular characterization of cloned avirulence genes from race-0 and race-1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
55. Stock, J. B., A. J. Ninfa, and A. M. Stock. 1989. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53:450-490.
56. Stock, J. B., M. G. Surette, M. Levit, and P. Park. 1995. Two-component signal transduction systems: structure-function relationships and mechanisms of catalysis, p. 25-51. In J. A. Hoch and T. J. Silhavy (ed.), Two-component signal transduction. ASM Press, Washington, D.C.
57. Vieira, J., and J. Messing. 1982. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259-268.
58. VoIz, K., and P. Matsumura. 1991. Crystal structure of Escherichia coli CheY refined at 1.7 Å resolution. J. Biol. Chem. 266:15511-15519.
59. Wanner, B. L. 1992. Is cross regulation by phosphorylation of two-component response regulator proteins important in bacteria? J. Bacteriol. 174: 2053-2058.
60. Webber, C. A., and R. J. Kadner. 1995. Action of receiver and activator modules of UhpA in transcriptional control of the Escherichia coli sugar phosphate transport system. Mol. Microbiol. 15:883-893.
61. Webber, C. A., and R. J. Kadner. 1997. Involvement of the amino-terminal phosphorylation module of UhpA in activation of uhpT transcription in Escherichia coli. Mol. Microbiol. 24:1039-1048.
62. Whitchurch, C. B., R. A. Alm, and J. S. Mattick. 1996. The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 93:9839-9843.
63. Wozniak, D. J., and D. E. Ohman. 1991. Pseudomonas aeruginosa AlgB, a two-component response regulator of the NtrC-family, is required for algD transcription. J. Bacteriol. 173:1406-1413.
64. Wozniak, D. J., and D. E. Ohman. 1993. Involvement of the alginate algT gene and integration host factor in the regulation of the Pseudomonas aeruginosa algB Gene. J. Bacteriol. 175:4145-4153.
65. Wozniak, D. J., and D. E. Ohman. 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.
66. Xie, Z., D. Hershberger, S. Shankar, R. W. Ye, and A. M. Chakrabarty. 1996. Sigma factor-anti-sigma factor interaction in alginate synthesis: inhibition of AlgT by MucA. J. Bacteriol. 178:4990-4996.
67. Yu, H., J. C. Boucher, N. S. Hibler, and V. Deretic. 1996. Virulence properties of Pseudomonas aeruginosa lacking the extreme-stress sigma factor AIgU (sigma E). Infect. Immun. 64:2774-2781.
68. Yu, H., M. Mudd, J. C. Boucher, M. J. Schurr, and V. Deretic. 1997. Identification of the algZ gene upstream of the response regulator algR and its participation in control of alginate production in Pseudomonas aeruginosa. J. Bacteriol. 179:187-193.