Structural insights into substrate specificity and the anti β-elimination mechanism of pectate lyase

Biochemistry

Volumn 49, Issue 3, 2010, Pages 539-546

  Seyedarabi, Arefeh ^a   To, Teng Teng ^a   Ali, Salyha ^a,c   Hussain, Syeed ^a,e   Fries, Markus ^a,f   Madsen, Robert ^b   Clausen, Mads H ^b   Teixteira, Susana ^c,d   Brocklehurst, Keith ^a   Pickersgill, Richard W ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c INSTITUT LAUE LANGEVIN   (France)

^d KEELE UNIVERSITY   (United Kingdom)

^e ASTRAZENECA   (United Kingdom)

^f BAXTER BIOSCIENCE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS SUBTILIS; CALCIUM IONS; CATALYTIC BASE; HELICAL CONFORMATION; HOMOGALACTURONAN; INACTIVE ENZYMES; MICHAELIS COMPLEX; PECTATE LYASE; PLANT CELL WALL; SCISSILE BOND; STRUCTURAL INSIGHTS; SUBSITES; SUBSTRATE BINDS; SUBSTRATE SPECIFICITY;

ABSTRACTING; AMINO ACIDS; BACTERIOLOGY; CALCIUM; CALCIUM ALLOYS; CARBOXYLATION; ENZYMES; GENE TRANSFER; OLIGOSACCHARIDES; ORGANIC POLYMERS; PLANT CELL CULTURE; PROTONS; SUBSTRATES;

IONS;

ALANINE; CALCIUM; CARBOXYLIC ACID; GALACTURONIC ACID; LYSINE; OLIGOSACCHARIDE; PECTATE LYASE; PECTIN;

ACIDIFICATION; AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS SUBTILIS; CHEMICAL BOND; COMPLEX FORMATION; ELIMINATION REACTION; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; METHYLATION; MICHAELIS CONSTANT; PRIORITY JOURNAL;

BACILLUS SUBTILIS; BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; OLIGOSACCHARIDES; PECTINS; POLYSACCHARIDE-LYASES; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

BACILLUS SUBTILIS; HARNESS;

EID: 74949100466     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901503g     Document Type: Article

References (48)

1. Collmer, A., and Keen, N. T. (1986) The Role of Pectic Enzymes in Plant Pathogenesis. Annu. Rev. Phytopathol. 24, 383-409.
2. Wolfenden, R., and Snider, M. J. (2001) The depth of chemical time and the power of enzymes as catalysts. Acc. Chem. Res. 34, 938-945.
3. 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.
4. Yoder, M. D., Keen, N. T., and Jurank, F. (1993) New domain motif: The structure of pectate lyase C, a secreted plant virulence factor. Science 260, 1503-1507.
5. Pickersgill, R. W., Jenkins, J.,Harris,G.,Nasser,W., andRobert-Baudouy, J. (1994) The structure of Bacillus subtilis pectate lyase in complex with calcium. Nat. Struct. Biol. 1, 717-723.
6. Akita, M., Suzuki, A., Kobayashi, T., Ito, S., and Yamane, T. (2001) The first structure of pectate lyase belonging to polysaccharide lyase family 3. Acta Crystallogr. D57, 1786-1792.
7. Jenkins, J., Shevchik, V. E., Hugouvieux-Cotte-Pattat, N., and Pickersgill, R. W. (2004) The crystal structure of pectate lyase Pel9A from Erwinia chrysanthemi. J. Biol. Chem. 279, 9139-9145.
8. Mayans, O., Scott, M., Connerton, I., Gravesen, T., Benen, J., Visser, J., Pickersgill, R., and Jenkins, J. (1997) Two crystal structures of pectin lyase A from Aspergillus reveal a pH driven conformational change and striking divergence in the substrate-binding clefts of pectin and pectate lyases. Structure 5, 677-689.
9. Vitali, J., Schick, B., Kester, H. C. M., Visser, J., and Jurnak, F. (1998) The three-dimensional structure of Aspergillus niger pectin lyase B at 1.7-angstrom resolution. Plant Physiol. 116, 69-80.
10. Petersen, T. N., Kauppinen, S., and Larsen, S. (1997) The crystal structure of rhamnogalacturonase A from Aspergillus aculeatus: A right-handed parallel β helix. Structure 5, 533-544.
11. Pickersgill, R., Smith, D., Worboys, K., and Jenkins, J. (1998) Crystal structure of polygalacturonase from Erwinia carotovora ssp. carotovora. J. Biol. Chem. 273, 24660-24664.
12. Jenkins, J., Mayans, O., Smith, D., Worboys, K., and Pickersgill, R. W. (2001) Three-dimensional structure of Erwinia chrysanthemi pectin methylesterase reveals a novel esterase active site. J. Mol. Biol. 305, 951-960.
13. Johansson, K., El-Ahmad, M., Friemann, R., Jornvall, H., Markovic, O., and Eklund, H. (2002) Crystal structure of plant pectin methylesterase. FEBS Lett. 514, 243-249.
14. Fries, M., Ihrig, J., Brocklehurst, K., Shevchik, V. E., and Pickersgill, R. W. (2007) Molecular basis of the activity of the phytopathogen pectin methylesterase. EMBO J. 26, 3879-3887.
15. Jenkins, J., and Pickersgill, R. (2001) The architecture of parallel β-helices and related folds. Prog. Biophys. Mol. Biol. 77, 111-175.
16. Abbott, D. W., and Boraston, A. B. (2007) A family 2 pectate lyase displays a rare fold and transition metal-assisted β-elimination. J. Biol. Chem. 282, 35328-35336.
17. Charnock, S. J., Brown, I. E., Turkenburg, J. P., Black, G. W., and Davies, G. J. (2001) Characterization of a novel pectate lyase, Pel10A, from Pseudomonas cellulosa. Proc. Natl. Acad. Sci. U.S.A. 99, 12067-12072.
18. Scavetta, R. D., Herron, S. R., Hotchkiss, A. T., Kita, N., Keen, N. T., Benen, J. A., Kester, H. C., Visser, J., and Jurank, F. (1999) Structure of a plant cell wall fragment complexed to pectate lyase C. Plant Cell 11, 1081-1092.
19. Herron, S., Benen, J. A., Scavetta, R. D., Visser, J., and Jurank, F. (2000) Structure and function of pectic enzymes: Virulence factors of plant pathogens. Proc. Natl. Acad. Sci. U.S.A. 97, 8762-8769.
20. Leslie, A. G. (1999) Integration of macromolecular diffraction data. Acta Crystallogr. D55, 240-255.
21. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D62, 72-82.
22. Vagin, A. A., and Teplyakov, A. (1997) MOLREP: An automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025.
23. 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.
24. Perrakis, A., Morris, R., and Lamzin, V. S. (1999) Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6, 458-463.
25. Jones, T. A., Zou, J.-Y., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A47, 110-119.
26. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D60, 2126-2132.
27. Rigby, N. M., MacDougall, A. J., Ring, S. G., Cairns, P., Morris, R., and Gunning, P. A. (2000) Observations on the crystallization of oligogalacturonates. Carbohydr. Res. 328, 235-239.
28. Clausen, M. H., Jorgensen, M. R., Thorsen, J., and Madsen, R. (2001) A strategy for chemical synthesis of selectively methylesterified oligomers of galacturonic acid. J. Chem. Soc., Perkin Trans. 1, 543-551.
29. Clausen, M., and Madsen, R. (2004) Synthesis of oligogalacturonates conjugated to BSA. Carbohydr. Res. 339, 2159-2169.
30. Clausen, M. H., and Madsen, R. (2003) Synthesis of hexasaccharide fragments of pectin. Chem. - Eur. J. 9, 3821-3832.
31. Petersen, B. O., Meier, S., Duus, J. O., and Clausen, M. H. (2008) Structural characterization of homogalacturonan by NMR spectroscopy-assignment of reference compounds. Carbohydr. Res. 343, 2830-2833.
32. 2+ binding to pectate lyase C. J. Biol. Chem. 278, 12271-12277.
33. Morris, E. R., Powell, D. A., Gidley, M. J., and Rees, D. A. (1982) Conformations and interactions of pectins 1. Polymorphism between gel and solid states of calcium polygalacturonate. J. Mol. Biol. 155, 507-516.
34. Powell, D. A., Morris, E. R., Gidley, M. J., and Rees, D. A. (1982) Conformations and interactions of pectins 2. Influence of residue sequence on chain association in calcium pectate gels. J. Mol. Biol. 155, 517-531.
35. Walkinshaw, M. D., and Arnott, S. (1981) Conformations and interactions of pectins. 1. X-ray-diffraction analyses of sodium pectate in neutral and acidified forms. J. Mol. Biol. 153, 1055-1073.
36. Walkinshaw, M. D., and Arnott, S. (1981) Conformations and interactions of pectins. 2. Models for junction zones in pectinic acid and calcium pectate gels. J. Mol. Biol. 153, 1075-1085.
37. Jarvis, M. C., and Apperley, D. C. (1995) Chain conformation in concentrated pectic gels: Evidence from C-13 NMR. Carbohydr. Res. 275, 131-145.
38. Hricovini, M., Bystricky, S., and Malovikova, A. (1991) Conformations of (1-4)-linked α-D-galacturono-di-saccharides and α-D-galacturono-tri-saccharides in solution analyzed by NMR measurements and theoretical calculations. Carbohydr. Res. 220, 23-31.
39. Gouvion, C., Mazeau, K., Heyraud, A., Taravel, F. R., and Tvaroska, I. (1994) Conformational study of digalacturonic acid and sodium digalacturonate in solution. Carbohydr. Res. 261, 187-202.
40. 1H-NMR and molecular dynamics. Biopolymers 34, 457-462.
41. Gerlt, J. A., and Gassman, P. G. (1992) Understanding enzyme-catalyzed proton abstraction from carbon acids: Details of step-wise mechanisms for β-elimination reactions. J. Am. Chem. Soc. 114, 5928-5934.
42. Gerlt, J. A., and Gassman, P. G. (1993) Understanding the rates of certain enzyme-catalyzed reactions: Proton abstraction from carbon acids, acyl-transfer reactions, and displacement reactions of phosphodiesters. J. Am. Chem. Soc. 115, 11552-11568.
43. Jenkins, J., Shevchik, V. E., Hugouvieux-Cotte-Pattat, N., and Pickersgill, R. W. (2004) The crystal structure of pectate lyase Pel9A from Erwinia chrysanthemi. J. Biol. Chem. 279, 9139-9145.
44. Atkins, E. D. T., Nieduszy.Ia, Parker, K. D., and Smolko, E. E. (1973) Structural components of alginic acid. 2. Crystalline-structure of poly-α-L-guluronic acid: Results of X-ray-diffraction and polarized infrared studies. Biopolymers 12, 1879-1887.
45. Perez, S., Mazeau, K., and du Penhoat, C. H. (2000) The three-dimensional structures of the pectic polysaccharides. Plant Physiol. Biochem. 38, 37-55.
46. Braccini, I., Grasso, R. P., and Perez, S. (1999) Conformational and configurational features of acidic polysaccharides and their interactions with calcium ions: A molecular modeling investigation. Carbohydr. Res. 317, 119-130.
47. DeLano, W. L., Ed. (2002) The PyMOL molecular graphics system. 0.80 version. The PyMOL User's Manual, DeLano Scientific, San Carlos, CA
48. Wallace, A. C., Laskowski, R. A., and Thornton, J. M. (1995) LIGPLOT: A program to generate schematic diagrams of protein ligand interactions. Protein Eng. 8, 127-134.