The protein BpsB is a poly-β-1,6-N-acetyl-D-glucosamine deacetylase required for biofilm formation in Bordetella bronchiseptica

Journal of Biological Chemistry

Volumn 290, Issue 37, 2015, Pages 22827-22840

  Little, Dustin J ^a,b,e   Milek, Sonja ^c   Bamford, Natalie C ^a,b   Ganguly, Tridib ^c   Difrancesco, Benjamin R ^d   Nitz, Mark ^d   Deora, Rajendar ^c   Howell, P Lynne ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; BIOCHEMISTRY; ESCHERICHIA COLI; PROTEINS;

ACTIVE SITE RESIDUES; BORDETELLA SPECIES; CARBOHYDRATE ESTERASE; COMPLEX ARCHITECTURES; DEACETYLASE ACTIVITY; DIVALENT METAL CATIONS; EXOPOLYSACCHARIDES; STRUCTURAL DIFFERENCES;

BIOFILMS;

ACYLTRANSFERASE; COBALT; NICKEL; PROTEIN BPSB; PROTEIN ICAB; PROTEIN PGAB; UNCLASSIFIED DRUG; AMIDASE; BACTERIAL PROTEIN; BETA GLUCAN; DEACETYLATED POLY-N-ACETYL-1-6-GLUCOSAMINE; POLY-N-ACETYL-1-6-GLUCOSAMINE;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOFILM; BIOSYNTHESIS; BORDETELLA BRONCHISEPTICA; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEACETYLATION; ENZYME ACTIVE SITE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; STRUCTURE ACTIVITY RELATION; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

AMIDOHYDROLASES; AMINO ACID MOTIFS; BACTERIAL PROTEINS; BETA-GLUCANS; BIOFILMS; BORDETELLA BRONCHISEPTICA; COBALT; NICKEL; PROTEIN STRUCTURE, TERTIARY;

EID: 84941591667     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.672469     Document Type: Article

References (68)

1. Goodnow, R. A. (1980) Biology of Bordetella bronchiseptica. Microbiol. Rev. 44, 722-738
2. Mattoo, S., and Cherry, J. D. (2005) Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin. Microbiol. Rev. 18, 326-382
3. Sukumar, N., Nicholson, T. L., Conover, M. S., Ganguly, T., and Deora, R. (2014) Comparative analyses of a cystic fibrosis isolate of Bordetella bronchiseptica reveal differences in important pathogenic phenotypes. Infect. Immun. 82, 1627-1637
4. Centers for Disease Control and Prevention (2012) Pertussis epidemic-Washington, 2012. MMWR Morb. Mortal Wkly Rep. 61, 517-522
5. Cherry, J. D. (2012) Epidemic pertussis in 2012-the resurgence of a vaccinepreventable disease. N. Engl. J. Med. 367, 785-787
6. Jakinovich, A., and Sood, S. K. (2014) Pertussis: still a cause of death, seven decades into vaccination. Curr. Opin. Pediatr. 26, 597-604
7. Sugisaki, K., Hanawa, T., Yonezawa, H., Osaki, T., Fukutomi, T., Kawakami, H., Yamamoto, T., and Kamiya, S. (2013) Role of (p) ppGpp in biofilm formation and expression of filamentous structures in Bordetella pertussis. Microbiology 159, 1379-1389
8. Parise, G., Mishra, M., Itoh, Y., Romeo, T., and Deora, R. (2007) Role of a putative polysaccharide locus in Bordetella biofilm development. J. Bacteriol. 189, 750-760
9. Mishra, M., Parise, G., Jackson, K. D., Wozniak, D. J., and Deora, R. (2005) The BvgAS signal transduction system regulates biofilm development in Bordetella. J. Bacteriol. 187, 1474-1484
10. Serra, D. O., Lücking, G., Weiland, F., Schulz, S., Görg, A., Yantorno, O. M., and Ehling-Schulz, M. (2008) Proteome approaches combined with Fourier transform infrared spectroscopy revealed a distinctive biofilm physiology in Bordetella pertussis. Proteomics 8, 4995-5010
11. Irie, Y., Mattoo, S., and Yuk, M. H. (2004) The Bvg virulence control system regulates biofilm formation in Bordetella bronchiseptica. J. Bacteriol. 186, 5692-5698
12. Sisti, F., Ha, D. G., O'Toole, G. A., Hozbor, D., and Fernández, J. (2013) Cyclic-di-GMP signalling regulates motility and biofilm formation in Bordetella bronchiseptica. Microbiology 159, 869-879
13. Serra, D. O., Conover, M. S., Arnal, L., Sloan, G. P., Rodriguez, M. E., Yantorno, O. M., and Deora, R. (2011) FHA-mediated cell-substrate and cell-cell adhesions are critical for Bordetella pertussis biofilm formation on abiotic surfaces and in the mouse nose and the trachea. PLoS ONE 6, e28811
14. Conover, M. S., Mishra, M., and Deora, R. (2011) Extracellular DNA is essential for maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS ONE 6, e16861
15. Conover, M. S., Sloan, G. P., Love, C. F., Sukumar, N., and Deora, R. (2010) The Bps polysaccharide of Bordetella pertussis promotes colonization and biofilm formation in the nose by functioning as an adhesin. Mol. Microbiol. 77, 1439-1455
16. Sloan, G. P., Love, C. F., Sukumar, N., Mishra, M., and Deora, R. (2007) The Bordetella Bps polysaccharide is critical for biofilm development in the mouse respiratory tract. J. Bacteriol. 189, 8270-8276
17. Irie, Y., and Yuk, M. H. (2007) In vivo colonization profile study of Bordetella bronchiseptica in the nasal cavity. FEMS Microbiol. Lett. 275, 191-198
18. Hall-Stoodley, L., Costerton, J. W., and Stoodley, P. (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95-108
19. López, D., Vlamakis, H., and Kolter, R. (2010) Biofilms. Cold Spring Harb. Perspect. Biol. 2, a000398
20. Vu, B., Chen, M., Crawford, R. J., and Ivanova, E. P. (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14, 2535-2554
21. Sutherland, I. (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147, 3-9
22. Branda, S. S., Vik, S., Friedman, L., and Kolter, R. (2005) Biofilms: the matrix revisited. Trends Microbiol. 13, 20-26
23. Ganguly, T., Johnson, J. B., Kock, N. D., Parks, G. D., and Deora, R. (2014) The Bordetella pertussis Bps polysaccharide enhances lung colonization by conferring protection from complement-mediated killing. Cell. Microbiol. 16, 1105-1118
24. Mack, D., Fischer, W., Krokotsch, A., Leopold, K., Hartmann, R., Egge, H., and Laufs, R. (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear β-1, 6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178, 175-183
25. McKenney, D., Pouliot, K. L., Wang, Y., Murthy, V., Ulrich, M., Döring, G., Lee, J. C., Goldmann, D. A., and Pier, G. B. (1999) Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284, 1523-1527
26. Wang, X., Preston, J. F., 3rd, and Romeo, T. (2004) The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol. 186, 2724-2734
27. Whitney, J. C., and Howell, P. L. (2013) Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria. Trends Microbiol. 21, 63-72
28. Steiner, S., Lori, C., Boehm, A., and Jenal, U. (2013) Allosteric activation of exopolysaccharide synthesis through cyclic di-GMP-stimulated proteinprotein interaction. EMBO J. 32, 354-368
29. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The carbohydrate-active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
30. Little, D. J., Poloczek, J., Whitney, J. C., Robinson, H., Nitz, M., and Howell, P. L. (2012) The structure- and metal-dependent activity of Escherichia coli PgaB provides insight into the partial de-N-acetylation of poly-β-1, 6-N-acetyl-D-glucosamine. J. Biol. Chem. 287, 31126-31137
31. Little, D. J., Bamford, N. C., Nitz, M., and Howell, P. L. (2014) in Encyclopedia of Inorganic and Bioinorganic Chemistry (Scott, R. A., ed) pp. 1-11, John Wiley & Sons Ltd., Chichester, UK
32. Little, D. J., Li, G., Ing, C., DiFrancesco, B. R., Bamford, N. C., Robinson, H., Nitz, M., Pomès, R., and Howell, P. L. (2014) Modification and periplasmic translocation of the biofilm exopolysaccharide poly-β-1, 6-N-acetyl-Dglucosamine. Proc. Natl. Acad. Sci. U. S. A. 111, 11013-11018
33. Itoh, Y., Rice, J. D., Goller, C., Pannuri, A., Taylor, J., Meisner, J., Beveridge, T. J., Preston, J. F., 3rd, and Romeo, T. (2008) Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin, poly-β-1, 6-N-acetyl-D-glucosamine (PGA). J. Bacteriol. 190, 3670-3680
34. Nishiyama, T., Noguchi, H., Yoshida, H., Park, S. Y., and Tame, J. R. (2013) The structure of the deacetylase domain of Escherichia coli PgaB, an enzyme required for biofilm formation: a circularly permuted member of the carbohydrate esterase 4 family. Acta Crystallogr. D Biol. Crystallogr. 69, 44-51
35. Little, D. J., Bamford, N. C., Pokrovskaya, V., Robinson, H., Nitz, M., and Howell, P. L. (2014) Structural basis for the de-N-acetylation of poly-β-1, 6-N-acetyl-D-glucosamine in Gram-positive bacteria. J. Biol. Chem. 289, 35907-35917
36. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collection in oscillation mode. Methods Enzymol. 276, 307-326
37. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
38. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
39. Painter, J., and Merritt, E. A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 62, 439-450
40. Painter, J., and Merritt, E. A. (2006) TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr. 39, 109-111
41. Dolinsky, T. J., Czodrowski, P., Li, H., Nielsen, J. E., Jensen, J. H., Klebe, G., and Baker, N. A. (2007) PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res. 35, W522-W525
42. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32, W665-W667
43. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U. S. A. 98, 10037-10041
44. Morin, A., Eisenbraun, B., Key, J., Sanschagrin, P. C., Timony, M. A., Ottaviano, M., and Sliz, P. (2013) Collaboration gets the most out of software. eLife 2, e01456
45. Leung, C., Chibba, A., Gómez-Biagi, R. F., and Nitz, M. (2009) Efficient synthesis and protein conjugation of β-(136)-D-N-acetylglucosamine oligosaccharides from the polysaccharide intercellular adhesin. Carbohydr. Res. 344, 570-575
46. Udenfriend, S., Stein, S., Böhlen, P., Dairman, W., Leimgruber, W., and Weigele, M. (1972) Fluorescamine: a reagent for assay of amino acids, peptides, proteins, and primary amines in the picomole range. Science 178, 871-872
47. Pokrovskaya, V., Poloczek, J., Little, D. J., Griffiths, H., Howell, P. L., and Nitz, M. (2013) Functional characterization of Staphylococcus epidermidis IcaB, a de-N-acetylase important for biofilm formation. Biochemistry 52, 5463-5471
48. Maira-Litrán, T., Kropec, A., Goldmann, D. A., and Pier, G. B. (2005) Comparative opsonic and protective activities of Staphylococcus aureus conjugate vaccines containing native or deacetylated staphylococcal poly-N-acetyl-β-(1-6)-glucosamine. Infect. Immun. 73, 6752-6762
49. 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
50. Conover, M. S., Redfern, C. J., Ganguly, T., Sukumar, N., Sloan, G., Mishra, M., and Deora, R. (2012) BpsR modulates Bordetella biofilm formation by negatively regulating the expression of the Bps polysaccharide. J. Bacteriol. 194, 233-242
51. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948
52. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
53. Janeček, Š., Svensson, B., and MacGregor, E. A. (2014) α-Amylase: an enzyme specificity found in various families of glycoside hydrolases. Cell. Mol. Life Sci. 71, 1149-1170
54. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
55. Little, D. J., Whitney, J. C., Robinson, H., Yip, P., Nitz, M., and Howell, P. L. (2012) Combining in situ proteolysis and mass spectrometry to crystallize Escherichia coli PgaB. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68, 842-845
56. Sukumar, N., Mishra, M., Sloan, G. P., Ogi, T., and Deora, R. (2007) Differential Bvg phase-dependent regulation and combinatorial role in pathogenesis of two Bordetella paralogs, BipA and BcfA. J. Bacteriol. 189, 3695-3704
57. Laganowsky, A., Zhao, M., Soriaga, A. B., Sawaya, M. R., Cascio, D., and Yeates, T. O. (2011) An approach to crystallizing proteins by metal-mediated synthetic symmetrization. Protein Sci. 20, 1876-1890
58. Blair, D. E., and van Aalten, D. M. (2004) Structures of Bacillus subtilis PdaA, a family 4 carbohydrate esterase, and a complex with N-acetylglucosamine. FEBS Lett. 570, 13-19
59. Andrés, E., Albesa-Jové, D., Biarnés, X., Moerschbacher, B. M., Guerin, M. E., and Planas, A. (2014) Structural basis of chitin oligosaccharide deacetylation. Angew. Chem. Int. Ed. Engl. 53, 6882-6887
60. Blair, D. E., Schüttelkopf, A. W., MacRae, J. I., and van Aalten, D. M. (2005) Structure and metal-dependent mechanism of peptidoglycan deacetylase, a streptococcal virulence factor. Proc. Natl. Acad. Sci. U. S. A. 102, 15429-15434
61. Abu Khweek, A., Fetherston, J. D., and Perry, R. D. (2010) Analysis of HmsH and its role in plague biofilm formation. Microbiology 156, 1424-1438
62. Vuong, C., Kocianova, S., Voyich, J. M., Yao, Y., Fischer, E. R., DeLeo, F. R., and Otto, M. (2004) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J. Biol. Chem. 279, 54881-54886
63. Deora, R. (2002) Differential regulation of the Bordetella bipA gene: distinct roles for different BvgA binding sites. J. Bacteriol. 184, 6942-6951
64. Cotter, P. A., and Miller, J. F. (1994) BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect. Immun. 62, 3381-3390
65. Miller, V. L., and Mekalanos, J. J. (1988) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170, 2575-2583
66. Edwards, R. A., Keller, L. H., and Schifferli, D. M. (1998) Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207, 149-157
67. Kovach, M. E., Phillips, R. W., Elzer, P. H., Roop, R. M., 2nd, and Peterson, K. M. (1994) pBBR1MCS: a broad-host-range cloning vector. BioTechniques 16, 800-802
68. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21