Membrane topology of outer membrane protein AlgE, which is required for alginate production in Pseudomonas aeruginosa

Applied and Environmental Microbiology

Volumn 76, Issue 6, 2010, Pages 1806-1812

  Hay, Iain D ^a   Rehman, Zahid U ^a   Rehm, Bernd H A ^a  

^a MASSEY UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

CHRONIC INFECTION; CYSTIC FIBROSIS; DEGRADATION PRODUCTS; DELETION MUTANTS; EXTRACELLULAR LOOPS; EXTRACELLULAR POLYSACCHARIDES; HUMAN PATHOGENS; MEMBRANE TOPOLOGY; OUTER MEMBRANE PROTEIN; P.AERUGINOSA; PERIPLASM; PSEUDOMONAS AERUGINOSA; SITE-SPECIFIC; VIRULENCE FACTORS;

BIOLOGICAL MEMBRANES; DEGRADATION; PROTEINS; TOPOLOGY;

ALGINATE;

ALGINIC ACID; GLUCURONIC ACID; HEXURONIC ACID; OUTER MEMBRANE PROTEIN;

ALGINATE; BACTERIUM; GENE EXPRESSION; MEMBRANE; MUTATION; POLYMERIZATION; PROTEIN; PUBLIC HEALTH; TOPOLOGY; VIRULENCE;

AMINO ACID SEQUENCE; ARTICLE; BIOLOGICAL MODEL; CELL MEMBRANE; CHEMISTRY; GENE DELETION; GENETIC COMPLEMENTATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; PSEUDOMONAS AERUGINOSA; SITE DIRECTED MUTAGENESIS;

ALGINATES; AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; CELL MEMBRANE; GENE DELETION; GENETIC COMPLEMENTATION TEST; GLUCURONIC ACID; HEXURONIC ACIDS; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

EID: 77749304001     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02945-09     Document Type: Article

References (49)

1. Albrecht, M. T., and N. L. Schiller. 2005. Alginate lyase (AlgL) activity is required for alginate biosynthesis in Pseudomonas aeruginosa. J. Bacteriol. 187:3869-3872.
2. Bagos, P. G., T. D. Liakopoulos, I. C. Spyropoulos, and S. J. Hamodrakas. 2004. PRED-TMBB: a web server for predicting the topology of beta-barrel outer membrane proteins. Nucleic Acids Res. 32:W400-W404.
3. Blatch, G. L., and M. Lassle. 1999. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21:932-939.
4. Blumenkrantz, N., and G. Asboe-Hansen. 1973. New method for quantitative determination of uronic acids. Anal. Biochem. 54:484-489.
5. Bornet, C., N. Saint, L. Fetnaci, M. Dupont, A. Davin-Regli, C. Bollet, and J. M. Pages. 2004. Omp35, a new Enterobacter aerogenes porin involved in selective susceptibility to cephalosporins. Antimicrob. Agents Chemother. 48:2153-2158.
6. Chiu, J., D. Tillett, I. W. Dawes, and P. E. March. 2008. Site-directed, ligase-independent mutagenesis (SLIM) for highly efficient mutagenesis of plasmids greater than 8kb. J. Microbiol. Methods 73:195-198.
7. Choi, K. H., A. Kumar, and H. P. Schweizer. 2006. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J. Microbiol. Methods 64:391-397.
8. Chu, L., T. B. May, A. M. Chakrabarty, and T. K. Misra. 1991. Nucleotide sequence and expression of the algE gene involved in alginate biosynthesis by Pseudomonas aeruginosa. Gene 107:1-10.
9. Costerton, J. W. 2001. Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol. 9:50-52.
10. D'Andrea, L. D., and L. Regan. 2003. TPR proteins: the versatile helix. Trends Biochem. Sci. 28:655-662.
11. Elkins, C. A., and H. Nikaido. 2003. Chimeric analysis of AcrA function reveals the importance of its C-terminal domain in its interaction with the AcrB multidrug efflux pump. J. Bacteriol. 185:5349-5356.
12. Franklin, M. J., and D. E. Ohman. 2002. Mutant analysis and cellular localization of the AlgI, AlgJ, and AlgF proteins required for O acetylation of alginate in Pseudomonas aeruginosa. J. Bacteriol. 184:3000-3007.
13. Grabert, E., J. Wingender, and U. K. Winkler. 1990. An outer membrane protein characteristic of mucoid strains of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 56:83-87.
14. Gutsche, J., U. Remminghorst, and B. H. A. Rehm. 2005. Biochemical analysis of alginate biosynthesis protein AlgX from Pseudomonas aeruginosa: purification of an AlgX-MucD (AlgY) protein complex. Biochimie 88:245-251.
15. Hancock, R. E. W., and A. M. Carey. 1979. Outer membrane of Pseudomonas aeruginosa: heat- 2-mercaptoethanol-modifiable proteins. J. Bacteriol. 140: 902-910.
16. Hay, I. D., U. Remminghorst, and B. H. A. Rehm. 2009. MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 75:1110-1120.
17. Hoang, T. T., R. R. Karkhoff-Schweizer, A. J. Kutchma, and H. P. Schweizer. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
18. Holloway, B. W., H. Matsumoto, and P. V. Phibbs, Jr. 1986. The chromosome map of Pseudomonas aeruginosa PAO. Acta Microbiol. Pol. 35:161-164.
19. Jain, S., M. J. Franklin, H. Ertesvag, S. Valla, and D. E. Ohman. 2003. The dual roles of AlgG in C-5-epimerization and secretion of alginate polymers in Pseudomonas aeruginosa. Mol. Microbiol. 47:1123-1133.
20. Jain, S., and D. E. Ohman. 1998. Deletion of algK in mucoid Pseudomonas aeruginosa blocks alginate polymer formation and results in uronic acid secretion. J. Bacteriol. 180:634-641.
21. Jain, S., and D. E. Ohman. 2005. Role of an alginate lyase for alginate transport in mucoid Pseudomonas aeruginosa. Infect. Immun. 73:6429-6436.
22. Jap, B. K., P. J. Walian, and K. Gehring. 1991. Structural architecture of an outer membrane channel as determined by electron crystallography. Nature 350:167-170.
23. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop II, and K. M. Peterson. 1995. Four new derivatives of the broad-hostrange cloning vector pBBR1MCS, carrying different antibiotic- resistance cassettes. Gene 166:175-176.
24. Martin, D. W., M. J. Schurr, M. H. Mudd, J. R. Govan, B. W. Holloway, and V. Deretic. 1993. Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc. Natl. Acad. Sci. U. S. A. 90:8377-8381.
25. Merighi, M., V. T. Lee, M. Hyodo, Y. Hayakawa, and S. Lory. 2007. The second messenger bis-(3-5)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 65:876-895.
26. Monday, S. R., and N. L. Schiller. 1996. Alginate synthesis in Pseudomonas aeruginosa: the role of AlgL (alginate lyase) and AlgX. J. Bacteriol. 178:625-632.
27. Nguyen, K. A., J. Zylicz, P. Szczesny, A. Sroka, N. Hunter, and J. Potempa. 2009. Verification of a topology model of PorT as an integral outer-membrane protein in Porphyromonas gingivalis. Microbiology 155:328-337.
28. Oglesby, L. L., S. Jain, and D. E. Ohman. 2008. Membrane topology and roles of Pseudomonas aeruginosa Alg8 and Alg44 in alginate polymerization. Microbiology 154:1605-1615.
29. Rehm, B. H. A. 1996. The Azotobacter vinelandii gene algJ encodes an outer-membrane protein presumably involved in export of alginate. Microbiology 142(Pt 4):873-880.
30. Rehm, B. H. A., G. Boheim, J. Tommassen, and U. K. Winkler. 1994. Overexpression of algE in Escherichia coli: subcellular localization, purification, and ion channel properties. J. Bacteriol. 176:5639-5647.
31. Rehm, B. H. A., E. Grabert, J. Hein, and U. K. Winkler. 1994. Antibody response of rabbits and cystic fibrosis patients to an alginate-specific outer membrane protein of a mucoid strain of Pseudomonas aeruginosa. Microb. Pathog. 16:43-51.
32. Rehm, B. H. A., and R. E. W. Hancock. 1996. Membrane topology of the outer membrane protein OprH from Pseudomonas aeruginosa: PCR-mediated site-directed insertion and deletion mutagenesis. J. Bacteriol. 178:3346-3349.
33. Remminghorst, U., and B. H. A. Rehm. 2006. Alg44, a unique protein required for alginate biosynthesis in Pseudomonas aeruginosa. FEBS Lett. 580:3883-3888.
34. Remminghorst, U., and B. H. A. Rehm. 2006. Bacterial alginates: from biosynthesis to applications. Biotechnol. Lett. 28:1701-1712.
35. Remminghorst, U., and B. H. A. Rehm. 2006. In vitro alginate polymerization and the functional role of Alg8 in alginate production by Pseudomonas aeruginosa. Appl. Environ. Microbiol. 72:298-305.
36. Robles-Price, A., T. Y. Wong, H. Sletta, S. Valla, and N. L. Schiller. 2004. AlgX is a periplasmic protein required for alginate biosynthesis in Pseudomonas aeruginosa. J. Bacteriol. 186:7369-7377.
37. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
38. Schlegel, H. G., H. Kaltwasser, and G. Gottschalk. 1961. A submersion method for culture of hydrogen-oxidizing bacteria: growth physiological studies. Arch. Mikrobiol. 38:209-222. (In German.)
39. Simon, R., U. Priefer, and A. Puhler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gramnegative bacteria. Biotechnology (NY) 1:784-791.
40. Soding, J., A. Biegert, and A. N. Lupas. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33:W244-W248.
41. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. L. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. S. Wong, Z. Wu, I. T. Paulsen, J. Reizer, M. H. Saier, R. E. W. Hancock, S. Lory, and M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959-964.
42. Struyve, M., J. Visser, H. Adriaanse, R. Benz, and J. Tommassen. 1993. Topology of PhoE porin: the 'eyelet' region. Mol. Microbiol. 7:131-140.
43. Tikhonova, E. B., Q. Wang, and H. I. Zgurskaya. 2002. Chimeric analysis of the multicomponent multidrug efflux transporters from gram-negative bacteria. J. Bacteriol. 184:6499-6507.
44. Van Gelder, P., N. Saint, P. Phale, E. F. Eppens, A. Prilipov, R. van Boxtel, J. P. Rosenbusch, and J. Tommassen. 1997. Voltage sensing in the PhoE and OmpF outer membrane porins of Escherichia coli: role of charged residues. J. Mol. Biol. 269:468-472.
45. Van Gelder, P., N. Saint, R. van Boxtel, J. P. Rosenbusch, and J. Tommassen. 1997. Pore functioning of outer membrane protein PhoE of Escherichia coli: mutagenesis of the constriction loop L3. Protein Eng. 10:699-706.
46. Visudtiphole, V., D. A. Chalton, Q. Hong, and J. H. Lakey. 2006. Determining OMP topology by computation, surface plasmon resonance and cysteine labelling: the test case of OMPG. Biochem. Biophys. Res. Commun. 351: 113-117.
47. Wang, S. K., I. Sa'-Correia, A. Darzins, and A. M. Chakrabarty. 1987. Characterization of the Pseudomonas aeruginosa alginate (alg) gene region II. J. Gen. Microbiol. 133:2303-2314.
48. Whitney, J. C., A. M. Neculai, D. E. Ohman, and P. L. Howell. 2009. Expression, refolding, crystallization and preliminary X-ray analysis of Pseudomonas aeruginosa AlgE. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65:463-466.
49. Winsor, G. L., T. Van Rossum, R. Lo, B. Khaira, M. D. Whiteside, R. E. Hancock, and F. S. Brinkman. 2009. Pseudomonas genome database: facilitating user-friendly, comprehensive comparisons of microbial genomes. Nucleic Acids Res. 37:D483-D488.