Transglycosylation by Chitinase D from Serratia proteamaculans improved through altered substrate interactions

Journal of Biological Chemistry

Volumn 287, Issue 53, 2012, Pages 44619-44627

  Madhuprakash, Jogi ^a   Tanneeru, Karunakar ^a   Purushotham, Pallinti ^a   Guruprasad, Lalitha ^a   Podile, Appa Rao ^a  

^a UNIVERSITY OF HYDERABAD   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SUBSTITUTION; CATALYTIC CENTER; CHITINASES; DOUBLE MUTANTS; HYDROLYTIC ACTIVITIES; HYDROLYTIC PRODUCT; SERRATIA PROTEAMACULANS; SUBSTRATE INTERACTION; TRANSGLYCOSYLATION;

AMINO ACIDS; GLYCOSYLATION;

CATALYST ACTIVITY;

ALANINE; BACTERIAL ENZYME; CHITINASE D; GLYCINE; PHENYLALANINE; SERINE; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL STRAIN; CONCENTRATION (PARAMETERS); ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; HYDROLYSIS KINETICS; MOLECULAR WEIGHT; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SEQUENCE HOMOLOGY; SERRATIA; SERRATIA PROTEAMACULANS; STRUCTURAL HOMOLOGY;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CHITINASE; GLYCOSYLATION; HYDROLYSIS; KINETICS; MODELS, MOLECULAR; OLIGOSACCHARIDES; PROTEIN BINDING; SERRATIA; SUBSTRATE SPECIFICITY;

SERRATIA PROTEAMACULANS;

EID: 84871737296     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.400879     Document Type: Article

References (41)

1. Minke, R., and Blackwell, J. (1978) The structure of α-chitin. J. Mol. Biol. 120, 167-181
2. Gardner, K. H., and Blackwell, J. (1975) Refinement of structure of β-chitin. Biopolymers 14, 1581-1595
3. Kim, S. K., and Rajapakse, N. (2005) Enzymatic production and biological activities of chitosan oligosaccharides (COS).Areview. Carbohydr. Polym. 62, 357-368
4. Vander, P., V rum, K. M., Domard, A., Eddine El Gueddari, N., and Moerschbacher, B. M. (1998) Comparison of the ability of partially N-acetylated chitosans and chitooligosaccharides to elicit resistance reactions in wheat leaves. Plant Physiol. 118, 1353-1359
5. Cabrera, J. C., Messiaen, J., Cambier, P., and Van Cutsem, P. (2006) Size, acetylation, and concentration of chitooligosaccharide elicitors determine the switch from defence involving PAL activation to cell death and water peroxide production in Arabidopsis cell suspensions. Physiol. Plant 127, 44-56
6. Kendra, D. F., and Hadwiger, L. A. (1984) Characterization of the smallest chitosan oligomer that is maximally antifungal to Fusariumsolani and elicits pisatin formation in Pisum sativum. Exp. Mycol. 8, 276-281 (Pubitemid 14012217)
7. Barber, M. S., Bertram, R. E., and Ride, J. P. (1989) Chitin oligosaccharides elicit lignification in wounded wheat leaves. Physiol. Mol. Plant Pathol. 34, 3-12
8. Moerschbacher, B., Kogel, K. H., Noll, U., and Reisener, H. J. (1986) An elicitor of the hypersensitive lignification response in wheat leaves isolated from the rust fungus Pucciniagraminis f. sp. tritici. I. Partial purification and characterization. Z. Naturforsch. 41, 830-838
9. Gotthardt, U., and Grambow, H. J. (1992) Near-isogenic wheat suspension cultures. Establishment, elicitor induced peroxidase activity, and potential use in the study of host/pathogen interactions. J. Plant Physiol. 139, 659-665
10. Liu, T., Liu, Z., Song, C., Hu, Y., Han, Z., She, J., Fan, F., Wang, J., Jin, C., Chang, J., Zhou, J. M., and Chai, J. (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336, 1160-1164
11. Sakai, K., Nanjo, F., and Usui, T. (1990) Production and utilization of oligosaccharides from chitin and chitosan. Denpun. Kagaku. 37, 79-86
12. Williams, S. J., and Withers, S. G. (2000) Glycosyl fluorides in enzymatic reactions. Carbohydr. Res. 327, 27-46 (Pubitemid 30624997)
13. Ly, H. D., and Withers, S. G. (1999) Mutagenesis of glycosidases. Annu. Rev. Biochem. 68, 487-522 (Pubitemid 29449201)
14. Zakariassen, H., Hansen, M. C., Jøranli, M., Eijsink, V. G., and Sørlie, M. (2011) Mutational effects on transglycosylating activity of family 18 chitinases and construction of a hyper transglycosylating mutant. Biochemistry 50, 5693-5703
15. Aronson, N. N., Jr., Halloran, B. A., Alexeyev, M. F., Zhou, X. E., Wang, Y., Meehan, E. J., and Chen, L. (2006) Mutation of a conserved tryptophan in the chitin-binding cleft of Serratia marcescens chitinase A enhances transglycosylation. Biosci. Biotechnol. Biochem. 70, 243-251 (Pubitemid 43150983)
16. Fukamizo, T., Goto, S., Torikata, T., and Araki, T. (1989) Enhancement of transglycosylation activity of lysozyme by chemical modification. Agric. Biol. Chem. 53, 2641-2651 (Pubitemid 20077530)
17. Taira, T., Fujiwara, M., Dennhart, N., Hayashi, H., Onaga, S., Ohnuma, T., Letzel, T., Sakuda, S., and Fukamizo, T. (2010) Transglycosylation reaction catalyzed by a class V chitinase from cycad, Cycas revolut., A study involving site-directed mutagenesis, HPLC, and real time ESI-MS. Biochim. Biophys. Acta 1804, 668-675
18. Li, C., Huang, W., and Wang, L. X. (2008) Chemo-enzymatic synthesis of N-linked neoglycoproteins through a chitinase-catalyzed transglycosylation. Bioorg. Med. Chem. 16, 8366-8372
19. Fan, S. Q., Huang, W., and Wang, L. X. (2012) Remarkable transglycosylation activity of glycosynthase mutants of endo-D, an endo-β-N-acetyl-glucosaminidase from Streptococcus pneumoniae. J. Biol. Chem. 287, 11272-11281
20. Purushotham, P., and Podile, A. R. (2012) Synthesis of long chain chitooligosaccharides by a hypertransglycosylating processive endochitinase of Serratia proteamaculans 568. J. Bacteriol. 194, 4260-4271
21. Shi, J., Blundell, T. L., and Mizuguchi, K. (2001) FUGUE. Sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310, 243-257 (Pubitemid 32619966)
22. Sashidhar, B., Inampudi, K. K., Guruprasad, L., Kondreddy, A., Gopinath, K., and Podile, A. R. (2010) Highly conserved Asp-204 and Gly-776 are important for activity of the quinoprotein glucose dehydrogenase of Escherichia coli and for mineral phosphate solubilization. J. Mol. Microbiol. Biotechnol. 18, 109-119
23. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (Pubitemid 24007801)
24. Bowie, J. U., Lüthy, R., and Eisenberg, D. (1991) A method to identify protein sequences that fold into a known three-dimensional structure. Science 253, 164-170 (Pubitemid 21917131)
25. Lüthy, R., Bowie, J. U., and Eisenberg, D. (1992) Assessment of protein models with three-dimensional profiles. Nature 356, 83-85
26. Ramachandran, G. N., Ramakrishnan, C., and Sasisekharan, V. (1963) Stereochemistry of polypeptide chain configurations. Mol. Biol. 7, 95-99
27. Ke, S. H., and Madison, E. L. (1997) Rapid and efficient site-directed mutagenesis by single-tube "megaprimer" PCR method. Nucleic Acids Res. 25, 3371-3372
28. Neeraja, C., Moerschbacher, B., and Podile, A. R. (2010) Fusion of cellulose binding domain to the catalytic domain improves the activity and conformational stability of chitinase in Bacillus licheniformis DSM13. Bioresour. Technol. 101, 3635-3641
29. Purushotham, P., Sarma, P. V., and Podile, A. R. (2012) Multiple chitinases of an endophytic Serratia proteamaculans 568 generate chitin oligomers. Bioresour. Technol. 112, 261-269
30. Taghavi, S., Garafola, C., Monchy, S., Newman, L., Hoffman, A., Weyens, N., Barac, T., Vangronsveld, J., and van der Lelie, D. (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl. Environ. Microbiol. 75, 748-757
31. Henrissat, B., and Davies, G. (1997) Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7, 637-644 (Pubitemid 27472582)
32. Zakariassen, H., Eijsink, V. G., and Sørlie, M. (2010) Signatures of activation parameters reveal substrate-dependent rate determining steps in polysaccharide turnover by a family 18 chitinase. Carbohydr. Polym. 81, 14-20
33. Lü, Y., Yang, H., Hu, H., Wang, Y., Rao, Z., and Jin, C. (2009) Mutation of Trp137 to glutamate completely removes transglycosyl activity associated with the Aspergillus fumigatus AfChiB1. Glycoconj. J. 26, 525-534
34. Makino, A., Kurosaki, K., Ohmae, M., and Kobayashi, S. (2006) Chitinase-catalyzed synthesis of alternatingly N-deacetylated chitin. A chitin-chitosan hybrid polysaccharide. Biomacromolecules 7, 950-957
35. Synstad, B., Gåseidnes, S., Van Aalten, D. M., Vriend, G., Nielsen, J. E., and Eijsink, V. G. (2004) Mutational and computational analysis of the role of conserved residues in the active site of a family 18 chitinase. Eur. J. Biochem. 271, 253-262 (Pubitemid 38130453)
36. Watanabe, T., Kobori, K., Miyashita, K., Fujii, T., Sakai, H., Uchida, M., and Tanaka, H. (1993) Identification of glutamic acid 204 and aspartic acid 200 in chitinase A1 of Bacillus circulans WL-12 as essential residues for chitinase activity. J. Biol. Chem. 268, 18567-18572 (Pubitemid 23273791)
37. Norberg, A. L., Dybvik, A. I., Zakariassen, H., Mormann, M., Peter-Katalinić, J., Eijsink, V. G., and Sørlie, M. (2011) Substrate positioning in chitinase A, a processive chito-biohydrolase from Serratia marcescens. FEBS Lett. 585, 2339-2344
38. Krokeide, I. M., Synstad, B., Gåseidnes, S., Horn, S. J., Eijsink, V. G., and Sørlie, M. (2007) Natural substrate assay for chitinases using high-performance liquid chromatography. A comparison with existing assays. Anal. Biochem. 363, 128-134 (Pubitemid 46348973)
39. van Aalten, D. M., Komander, D., Synstad, B., Gåseidnes, S., Peter, M. G., and Eijsink, V. G. (2001) Structural insights into the catalytic mechanism of a family 18 exo-chitinase. Proc. Natl. Acad. Sci. U.S.A. 98, 8979-8984 (Pubitemid 32743855)
40. Jitonnom, J., Lee, V. S., Nimmanpipug, P., Rowlands, H. A., and Mulholland, A. J. (2011) Quantum mechanics/molecular mechanics modeling of substrate-assisted catalysis in family 18 chitinases. Conformational changes and the role of Asp142 in catalysis in ChiB. Biochemistry 50, 4697-4711
41. Watanabe, T., Ariga, Y., Sato, U., Toratani, T., Hashimoto, M., Nikaidou, N., Kezuka, Y., Nonaka, T., and Sugiyama, J. (2003) Aromatic residues within the substrate-binding cleft of Bacillus circulans chitinase A1 are essential for hydrolysis of crystalline chitin. Biochem. J. 376, 237-244 (Pubitemid 37487219)