Recognition of heteropolysaccharide alginate by periplasmic solute-binding proteins of a bacterial ABC transporter

Biochemistry

Volumn 51, Issue 17, 2012, Pages 3622-3633

  Nishitani, Yu ^a   Maruyama, Yukie ^a   Itoh, Takafumi ^a   Mikami, Bunzo ^a   Hashimoto, Wataru ^a   Murata, Kousaku ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ALGINATE OLIGOSACCHARIDE; BINDING PROTEINS; CARBOXYL GROUPS; GRAM-NEGATIVE BACTERIA; HETEROPOLYSACCHARIDE; HYDROXYL GROUPS; NON-REDUCING TERMINAL RESIDUE; SPHINGOMONAS SP; STRUCTURAL DETERMINANTS; SUBSITES; SUBSTRATE RECOGNITION;

CYTOLOGY; HYDROGEN BONDS; OLIGOSACCHARIDES; PROTEINS; SUBSTRATES; X RAY CRYSTALLOGRAPHY;

ALGINATE;

ABC TRANSPORTER; ALGINIC ACID; BINDING PROTEIN; CARBOXYL GROUP; HYDROXYL GROUP; OLIGOSACCHARIDE; PERIPLASMIC SOLUTE BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM CULTURE; CHEMICAL INTERACTION; CRYSTAL STRUCTURE; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SPHINGOMONAS; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATASES; ALDEHYDES; ALGINATES; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; GLUCURONIC ACID; HEXURONIC ACIDS; PERIPLASMIC PROTEINS; POLYSACCHARIDES; PROTEIN BINDING; SPHINGOMONAS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; SPHINGOMONAS SP.;

EID: 84860463104     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300194f     Document Type: Article

References (42)

1. Gacesa, P. (1988) Alginates Carbohydr. Polym. 8, 161-182
2. Remminghorst, U. and Rehm, B. H. (2006) Bacterial alginates: From biosynthesis to applications Biotechnol. Lett. 28, 1701-1712
3. Akiyama, H., Endo, T., Nakakita, R., Murata, K., Yonemoto, Y., and Okayama, K. (1992) Effect of depolymerized alginates on the growth of bifidobacteria Biosci., Biotechnol., Biochem. 56, 355-356
4. May, T. B. and Chakrabarty, A. M. (1994) Pseudomonas aeruginosa: Genes and enzymes of alginate synthesis Trends Microbiol. 2, 151-157
5. Wong, T. Y., Preston, L. A., and Schiller, N. L. (2000) Alginate lyase: Review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications Annu. Rev. Microbiol. 54, 289-340
6. Singh, A., Nigam, P. S., and Murphy, J. D. (2011) Renewable fuels from algae: An answer to debatable land based fuels Bioresour. Technol. 102, 10-16
7. Nyvall, P., Corre, E., Boisset, C., Barbeyron, T., Rousvoal, S., Scornet, D., Kloareg, B., and Boyen, C. (2003) Characterization of mannuronan C-5-epimerase genes from the brown alga Laminaria digitata Plant Physiol. 133, 726-735
8. Garron, M. L. and Cygler, M. (2010) Structural and mechanistic classification of uronic acid-containing polysaccharide lyases Glycobiology 20, 1547-1573
9. Murata, K., Kawai, S., Mikami, B., and Hashimoto, W. (2008) Superchannel of bacteria: Biological significance and new horizons Biosci., Biotechnol., Biochem. 72, 265-277
10. Hisano, T., Kimura, N., Hashimoto, W., and Murata, K. (1996) Pit structure on bacterial cell surface Biochem. Biophys. Res. Commun. 220, 979-982
11. Momma, K., Mikami, B., Mishima, Y., Hashimoto, W., and Murata, K. (2002) Crystal structure of AlgQ2, a macromolecule (alginate)-binding protein of Sphingomonas sp. A1 at 2.0 Å resolution J. Mol. Biol. 316, 1061-1069
12. Momma, K., Okamoto, M., Mishima, Y., Mori, S., Hashimoto, W., and Murata, K. (2000) A novel bacterial ATP-binding cassette (ABC) transporter system that allows uptake of macromolecules J. Bacteriol. 182, 3998-4004
13. Yoon, H.-J., Hashimoto, W., Miyake, O., Okamoto, M., Mikami, B., and Murata, K. (2000) Overexpression in Escherichia coli, purification, and characterization of Sphingomonas sp. A1 alginate lyases Protein Expression Purif. 19, 84-90
14. Hashimoto, W., Miyake, O., Momma, K., Kawai, S., and Murata, K. (2000) Molecular identification of oligoalginate lyase of Sphingomonas sp. strain A1 as one of the enzymes required for complete depolymerization of alginate J. Bacteriol. 182, 4572-4577
15. Eitinger, T., Rodionov, D. A., Grote, M., and Schneider, E. (2011) Canonical and ECF-type ATP-binding cassette importers in prokaryotes: Diversity in modular organization and cellular functions FEMS Microbiol. Rev. 35, 3-67
16. Hugouvieux-Cotte-Pattat, N. and Reverchon, S. (2001) Two transporters, TogT and TogMNAB, are responsible for oligogalacturonide uptake in Erwinia chrysanthemi 3937 Mol. Microbiol. 41, 1125-1132
17. Momma, K., Mishima, Y., Hashimoto, W., Mikami, B., and Murata, K. (2005) Direct evidence for Sphingomonas sp. A1 periplasmic proteins as macromolecule-binding proteins associated with ABC transporter: Molecular insights into alginate transport in the periplasm Biochemistry 44, 5053-5064
18. Mishima, Y., Momma, K., Hashimoto, W., Mikami, B., and Murata, K. (2003) Crystal structure of AlgQ2, a macromolecule (alginate)-binding protein of Sphingomonas sp. A1, complexed with an alginate tetrasaccharide at 1.6-Å resolution J. Biol. Chem. 278, 6552-6559
19. Takeda, H., Yoneyama, F., Kawai, S., Hashimoto, W., and Murata, K. (2011) Bioethanol production from marine biomass alginate by metabolically engineered bacteria Energy Environ. Sci. 4, 2575-2581
20. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular cloning: A laboratory manual, Cold Spring Harbor Laboratory Press, Plainview, NY.
21. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227, 680-685
22. Haug, A., Larsen, B., and Smidsrod, O. (1966) A study of the constitution of alginic acid by partial acid hydrolysis Acta Chem. Scand. 20, 183-190
23. Miyake, O., Ochiai, A., Hashimoto, W., and Murata, K. (2004) Origin and diversity of alginate lyases of families PL-5 and -7 in Sphingomonas sp. strain A1 J. Bacteriol. 186, 2891-2896
24. Miller, G. L. (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar Anal. Chem. 31, 426-428
25. Niesen, F. H., Berglund, H., and Vedadi, M. (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability Nat. Protoc. 2, 2212-2221
26. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
27. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system (CNS): A new software system for macromolecular structure determination Acta Crystallogr. D54, 905-921
28. Sheldrick, G. M. (2008) A short history of SHELX Acta Crystallogr. D64, 112-122
29. Vagin, A. and Teplyakov, A. (1997) MOLREP: An automated program for molecular replacement J. Appl. Crystallogr. 30, 1022-1025
30. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
31. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255
32. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
33. Schuettelkopf, A. W. and Van Aalten, D. M. F. (2004) PRODRG: A tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. D60, 1355-1363
34. Kabsch, W. (1976) A solution for the best rotation to relate two sets of vectors Acta Crystallogr. A32, 922-923
35. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
36. DeLano, W. L. (2004) The PyMOL Molecular Graphics System, DeLano Scientific LLC, San Carlos, CA.
37. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The protein data bank Nucleic Acids Res. 28, 235-242
38. Giuliani, S. E., Frank, A. M., and Collart, F. R. (2008) Functional assignment of solute-binding proteins of ABC transporters using a fluorescence-based thermal shift assay Biochemistry 47, 13974-13984
39. Ramachandran, G. N. and Sasisekharan, V. (1968) Conformations of polypeptides and proteins Adv. Protein Chem. 23, 283-438
40. Llanes, F., Ryan, D. H., and Marchessault, R. H. (2000) Magnetic nanostructured composites using alginates of different M/G ratios as polymeric matrix Int. J. Biol. Macromol. 27, 35-40
41. Holtan, S., Bruheim, P., and Skjǎk-Bræk, G. (2006) Mode of action and subsite studies of guluronan block-forming mannuronan C-5 epimerases AlgE1 and AlgE6 Biochem. J. 395, 319-329
42. Campa, C., Holtan, S., Nilsen, N., Bjerkan, T. M., Stokke, B. T., and Skjǎk-Bræk, G. (2004) Biochemical analysis of the processive mechanism for epimerization of alginate by mannuronan C-5 epimerase AlgE4 Biochem. J. 381, 155-164