Structure and function of enzymes acting on chitin and chitosan

Biotechnology and Genetic Engineering Reviews

Volumn 27, Issue 1, 2010, Pages 331-366

  Hoell, Ingunn A ^a   Vaaje Kolstad, Gustav ^b   Eijsink, Vincent G H ^b  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b WESTERN NORWAY UNIVERSITY OF APPLIED SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROLASES; SUGARS;

'CURRENT; BIOACTIVES; CARBOHYDRATE ESTERASE; CHITIN METABOLISM; CHITINASES; CHITOOLIGOSACCHARIDES; ENZYMATIC CONVERSIONS; GLYCOSIDE HYDROLASES; HYDROLASE FAMILY; POLYMERIC SUBSTRATE;

CHITOSAN;

CHITIN; CHITINASE; CHITOSAN; CHITOSANASE; GLYCOSIDASE;

BIOMASS; CARBOHYDRATE METABOLISM; CRUSTACEA; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; FUNGUS; INSECT; NONHUMAN; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW;

CRUSTACEA; FUNGI; HEXAPODA;

EID: 79551583731     PISSN: 02648725     EISSN: 20465556     Source Type: Journal    
DOI: 10.1080/02648725.2010.10648156     Document Type: Article

References (189)

1. Adachi, W., Sakihama, Y., Shimizu, S., Sunami, T., Fukazawa, T. Suzuki, M., Yatsunami, R., Nakamura, S. and Takenaka, A. (2004). Crystal structure of family GH-8 chitosanase with subclass II specificity from Bacillus sp K17. Journal of Molecular Biology343, 785–95.
2. Adams, D.J. (2004). Fungal cell wall chitinases and glucanases. Microbiology150, 2029–2035.
3. Aiba, S. (1991). Studies on chitosan:Evidence for the presence of random and block copolymer structures in partially N-acetylated chitosans. International Journal of Biological Macromolecules13, 40–44.
4. Alzari, P.M., Souchon, H. and Dominguez, R. (1996). The crystal structure of endoglucanase CelA, a family 8 glycosyl hydrolase from Clostridium thermocellum. Structure4, 265–75.
5. Andersen, M.D., Jensen, A., Robertus, J.D., Leah, R. and Skriver, K. (1997). Heterologous expression and characterization of wild-type and mutant forms of a 26 kDa endochitinase from barley (Hordeum vulgare L.). Biochemical Journal322, 815–22.
6. Anthonsen, M.W., Varum, K.M. and Smidsrod, O. (1993). Solution properties of chitosans - conformation and chain stiffness of chitosans with different degrees of N-acetylation. Carbohydrate Polymers22, 193–201.
7. Araki, Y. and Ito, E. (1975). Pathway of chitosan formation in Mucor rouxii - enzymatic deacetylation of chitin. European Journal of Biochemistry55, 71–78.
8. Bentley, S.D., Chater, K.F., CerdeÑo-TÁrraga, A.M., Challis, G.L., etal. (2002). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature417, 141–47.
9. Biely, P., Kratky, Z. and Vrsanska, M. (1981) Substrate-binding site of endo-b-1,4-xylanase of the yeast Cryptococcus albidus. European Journal of Biochemistry119, 559–64.
10. Blackwell, J. (1988). Physical methods for determinination of chitin structure and conformation. Methods in enzymology. J. N. Abelson and M. I. Simon. San Diego, Academic Press, Inc. 161, 435–42.
11. Blair, D. E., Hekmat, O., Schüttelkopf, A.W., Shrestha, B., Tokuyasu, K., Withers, S.G. and Van Aalten, D.M. (2006). Structure and mechanism of chitin deacetylase from the fungal pathogen Colletotrichum lindemuthianum. Biochemistry45, 9416–26.
12. Blair, D.E., Schüttelkopf, A.W., Macrae, J.I. and Van Aalten, D.M.F. (2005). Structure and metal-dependent mechanism of peptidoglycan deacetylase, a streptococcal virulence factor. Proceedings of the National Academy of Sciences of the United States of America102, 15429–34.
13. Blair, D. E. and Van Aalten, D.M.F. (2004). Structures of Bacillus subtilis PdaA, a family 4 carbohydrate esterase, and a complex with N-acetyl-glucosamine. FEBS Letters570, 13–19.
14. Boot, R.G., Blommaart, E.F., Swart, E., Ghauharali-Van Der Vlugt, K., Bijl, N., Moe, C., Place, A. and Aerts, J.M. (2001). Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. Journal of Biological Chemistry276, 6770–8.
15. Boot, R.G., Renkema, G.H., Strijland, A., Van Zonneveld, A.J. and Aerts, J.M. (1995). Cloning of a cDNA encoding chitotriosidase, a human chitinase produced by macrophages. Journal of Biological Chemistry270, 26252–6.
16. Boraston, A.B., Bolam, D.N., Gilbert, H.J. and Davies, G.J. (2004). Carbohydratebinding modules:fine-tuning polysaccharide recognition. Biochemical Journal382, 769–81.
17. Boucher, I., Fukamizo, T., Honda, Y., Willick, G.E., Neugebauer, W.A. and Brzezinski, R. (1995). Site-directed mutagenesis of evolutionary conserved carboxylic amino acids in the chitosanase from Streptomyces sp. N174 reveals two residues essential for catalysis. Journal of Biological Chemistry270, 31077–82.
18. Brurberg, M. B., Nes, I.F. and Eijsink, V.G.H. (1996). Comparative studies of chitinases A and B from Serratia marcescens. Microbiology-Uk142, 1581–9.
19. Bussink, A. P., Speijer, D., Aerts, J.M. and Boot, R.G. (2007). Evolution of mammalian chitinase (-like) members of family 18 glycosyl hydrolases. Genetics177, 959–70.
20. 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 Research37, D233-D238.
21. Carsolio, C., Gutiérrez, A., Jiménez, B., Van Montagu, M. and Herrera-Estrella, A. (1994). Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism. Proceedings of the National Academy of Sciences of the United States of America91, 10903–7.
22. Caufrier, F., Martinou, A., Dupont, C. and Bouritis, V. (2003). Carbohydrate esterase family 4 enzymes:substrate specificity. Carbohydrate Research338, 687–92.
23. Cheng, C. Y., Chang, C.H., Wu, Y.J. and Li, Y.K. (2006). Exploration of glycosyl hydrolase family 75, a chitosanase from Aspergillus fumigatus. Journal of Biological Chemistry281, 3137–44.
24. Cheng, C.Y. and Li, Y.K. (2000). An Aspergillus chitosanase with potential for large-scale preparation of chitosan oligosaccharides. Biotechnologi and Applied Biochemistry32, 197–203.
25. Choi, Y.J., Kim, E.J., Piao, Z., Yun, Y.C. and Shin, Y.C. (2004). Purification and characterization of chitosanase from Bacillus sp strain KCTC 0377BP and Its application for the production of chitosan oligosaccharides. Applied and environmental microbiology70, 4522–31.
26. Cohen-Kupiec, R. and Chet, I. (1998). The molecular biology of chitin digestion. Current Opinion in Biotechnology9, 270–7.
27. Davies, G. and Henrissat, B. (1995). Structures and mechanisms of glycosyl hydrolases. Structure3, 853–59.
28. Davies, G. J., Gloster, T.M. and Henrissat, B. (2005). Recent structural insights into the expanding world of carbohydrate-active enzymes. Current Opinion in Structural Biology15, 637–45.
29. Davies, G. J., Wilson, K.S. and Henrissat, B. (1997). Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochemical Journal321, 557–9.
30. De La Cruz, J., Hidalgo-Gallego, A., Lora, J.M., Benitez, T., Pintor-Toro, J.A. and Llobell, A. (1992). Isolation and characterization of three chitinases from Trichoderma harzianum. European Journal of Biochemistry206, 859–67.
31. Divne, C., StÅhlberg, J., Reinikainen, T., Ruohonen, L., Pettersson, G., Knowles, J.K., Teeri, T.T. and Jones, T.A. (1994) The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei. Science265, 524–528.
32. Dutta, P. K., Ravikumar, M.N. and Dutta, J. (2002). Chitin and chitosan for versatile applications. Journal of Macromolecular ScienceC42, 307–54.
33. Eijsink, V. G. H., Vaaje-Kolstad, G., VÅrum, K.M. and Horn, S.J. (2008). Towards new enzymes for biofuels:lessons from chitinase research. Trends in Biotechnology26, 228–35.
34. Felse, P. A. and Panda, T. (1999). Studies on applications of chitin and its derivatives. Bioprocess Engineering20, 505–12.
35. Felt, O., Buri, P. and Gurny, R. (1998). Chitosan:A unique polysaccharide for drug delivery. Drug Development and Industrial Pharmacy24, 979–93.
36. Fernandes, J. C., Tavaria, F.K., Soares, J., Ramos, O.S., Monteiro, M.J, Pintado, M.E. and Malcata, F.X. (2008). Antimicrobial effects of chitosans and chitooligosaccharides, upon Staphylococcus aureus and Escherichia coli, in food model systems. Food Microbiology25, 922–28.
37. Fukamizo, T. and Brzezinski, R. (1997). Chitosanase from Streptomyces sp. strain N174:a comparative review of its structure and function. Biochemical Cell Biology75, 687–96.
38. Fukamizo, T., Honda, Y., Goto, S., Boucher, I. and Brzezinski, R. (1995). Reaction mechanism of chitosanase from Streptomyces sp. N174. Biochemical Journal311, 377–83.
39. Fukamizo, T, Juffer, A.H, Vogel, H.J., Honda, Y., Tremblay, H., Boucher, I., Neugebauer, W.A. and Brzezinski, R. (2000). Theoretical calculation of pKa reveals an important role of Arg205 in the activity and stability of Streptomyces sp N174 chitosanase. Journal of Biological Chemistry275, 25633–40.
40. Fukamizo, T, Miyake, R., Tamura, A., Ohnuma, T., Skriver, K., Pursiainen, N.V. and Juffer, A.H. (2009). A flexible loop controlling the enzymatic activity and specificity in a glycosyl hydrolase family 19 endochitinase from barley seeds (Hordeum vulgare L.). Biochimica et Biophysica Acta.1794, 1159–67.
41. Fukamizo, T, Ohkawa, T., Ikeda, Y. and Goto, S. (1994). Specificity of chitosanase from Bacillus pumilus. Biochimica et Biophysica Acta1205, 183–8.
42. Gao, X.D., Katsumoto, T. and Onodera, K. (1995). Purification and characterization of chitin deacetylase from Absidia coerulea. Journal of Biochemistry117, 257–63.
43. García, I., Lora, J.M., De La Cruz, J., Benítez, T., Llobell, A. and Pintor-Toro, J.A. (1994) Cloning and characterization of a chitinase (chit42) cDNA from the mycoparasitic fungus Trichoderma harzianum. Current Genetics27, 83–9.
44. Garcia-Casado, G., Collada, C. Allona, I., Casado, R., Pacios, L.F., Aragoncillo, C. and Gomez, L (1998). Site-directed mutagenesis of active site residues in a class I endochitinase from chestnut seeds. Glycobiology8, 1021–28.
45. Gardner, K. H. and Blackwell, J. (1975). Refinement of the structure of beta-chitin. Biopolymers14, 1581–95.
46. Giraud-Guille, M. M. (1986). Chitin-protein molecular organization in arthropods. Chitin in nature and technology. R. Muzarelli, Jeuniaux C. and Gooday G. W. New York, Plenum Press, 29–35.
47. Gooday, G. W. (1990). The ecology of chitin degradation. In Advances in Microbial Ecology ed. K. C. Marshall, pp 387–430. New York:Plenum Press.
48. Guan, B.H., Ni, W.M., Wu, Z.B. and Lai, Y. (2009). Removal of Mn(II) and Zn(II) ions from flue gas desulfurization wastewater with water-soluble chitosan. Separation and Purification Technology65, 269–74.
49. Guan, S.P., Mok, Y.K., Koo, K.N., Chu, K.L. and Wong, W.S. (2009) Chitinases:biomarkers for human diseases. Protein and Peptide Letters16, 490–98.
50. Hahn, M., Hennig, M., Schleiser, B. and Hohne, W. (2000). Structure of jack bean chitinase. Acta Crystallographica. Section D, Biological Crystallography56, 1096–9.
51. Hart, P. J., Monzingo, A.F., Ready, M.P., Ernst, S.R. and Robertus, J.D. (1993). Crystal structure of an endochitinase from Hordeum vulgare L seeds. Journal of Molecular Biology229, 189–93.
52. Hart, P. J., Pfluger, H.D., Monzingo, A.F., Hollis, T. and Robertus, J.D. (1995). The refined crystal-structure of an endochitinase from Hordeum vulgare L seeds at 1.8 Angstrom resolution. Journal of Molecular Biology248, 402–13.
53. Heggset, E. B., Hoell, I.A., Kristoffersen, M., Eijsink, V.G.H. and VÅrum, K.M. (2009). Degradation of chitosans with chitinase G from Streptomyces coelicolor A3(2):production of chito-oligosaccharides and insight into subsite specificities. Biomacromolecules10, 892–9.
54. Hennig, M., Jansonius, J.N., Terwisscha Van Scheltinga, A.C., Dijkstra, B.W. and Schleisier, B. (1995). Crystal structure of concanavalin B at 1.65 A resolution, An “inactivated” chitinase from seeds of Canavalia ensiformis. Journal of Molecular Biology. 254, 237–46.
55. Hennig, M., Schlesier, B., Dauter, Z., Pfeffer, S., Betzel, C., HÖhne, W.E. and Wilson, K.S. (1992) A TIM barrel protein without enzymatic activity? Crystal-structure of narbonin at 1.8 A resolution. FEBS Letters306, 80–4.
56. Henrissat, B. and Davies, G. (1997). Structural and sequence-based classification of glycoside hydrolases. Current Opinion in Structural Biology7, 637–44.
57. Henrissat, B., Teeri, T.T. and Warren, R.A.J. (1998) A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Letters425, 352–4.
58. Hernick, M. and Fierke, C.A. (2005). Zinc hydrolases:the mechanisms of zincdependent deacetylases. Archives of Biochemistry and Biophysics433, 71–84.
59. Hjeljord, L.G., Stensvand, A. and Tronsmo, A. (2001). Antagonism of nutrientactivated conidia of Trichoderma harzianum (atroviride) P1 against Botrytis cinerea. Phytopathology91, 1172–80.
60. Hodgson, D. A. (2000). Primary metabolism and its control in Streptomycetes:a most unusual group of bacteria. Advances in Microbial Physiology42, 47–238.
61. Hoell, I. A., Dalhus, B., Heggset, E.B., Aspmo, S.I. and Eijsink, V.G.H. (2006). Crystal structure and enzymatic properties of a bacterial family 19 chitinase reveal differences from plant enzymes. FEBS Journal273, 4889–900.
62. Hoell, I.A., Klemsdal, S.S., Vaaje-Kolstad, G., Horn, S.J. and Eijsink, V.G.H. (2005). Overexpression and characterization of a novel chitinase from Trichoderma atroviride strain P1. Biochimica et Biophysica Acta1748, 180–90.
63. Holm, L. and Sander, C. (1994). Structural similarity of plant chitinase and lysozymes from animals and phage - an evolutionary connection. FEBS Letters340, 129–32.
64. Hopwood, D. A. (1999). Forty years of genetics with Streptomyces:from in vivo through in vitro to in silico. Microbiology145, 2183–2202.
65. Horn, S. J., Sikorski, P., Cederkvist, J.B., Vaaje-Kolstad, G., Sorlie, M., Synstad, B., Vriend, G., VÅrum, K.M. and Eijsink, V.G.H. (2006a). Costs and benefits of processivity in enzymatic degradation of recalcitrant polysaccharides. Proceedings of the National Academy of Sciences of the United States of America103, 18089–94.
66. Horn, S. J., Sorbotten, A., Synstad, B., Sikorski, P., Sorlie, M., VÅrum, K.M. and Eijsink, V.G.H. (2006b). Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS Journal273, 491–503.
67. Huet, J., Rucktooa, P., Clantin, B., Azarkan, M., Looze, Y., Villeret, V. and Wintjens, R. (2008). X-ray structure of papaya chitinase reveals the substrate binding mode of glycosyl hydrolase family 19 chitinases. Biochemistry47, 8283–91.
68. Hult, E. L., Katouno, F., Clantin, B., Azarkan, M., Looze, Y., Villeret, V. and Wintjens, R. (2005). Molecular directionality in crystalline beta-chitin:hydrolysis by chitinases A and B from Serratia marcescens 2170. Biochemical Journal388,:851–56.
69. Ike, M., Ko, Y., Yokoyama, K., Sumitani, J.I., Kawaquchi, T., Ogasawara, W., Okada, H. and Morikawa, Y. (2007). Cellobiohydrolase I (Cel7A) from Trichoderma reesei has chitosanase activity. Journal of Molecular Catalysis B-Enzymatic47, 159–63.
70. Ikeda, H., Ishikawa, J., Hanamoto, A., Shinose, M., Kikuchi, H., Shiba, T., Sakaki, Y., Hattori, M. and Omura, S. (2003). Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nature Biotechnology21, 526–31.
71. Iseli, B., Armand, S., Boller, T., Neuhaus, J.M. and Henrissat, B. (1996). Plant chitinases use two different hydrolytic mechanisms. FEBS Letters382, 186–8.
72. Isogawa, D., Fukuda, T., Kuroda, K., Kusaoke, H., Kimoto, H., Suye, S. and Ueda, M. (2009). Demonstration of catalytic proton acceptor of chitosanase from Paenibacillus fukuinensis by comprehensive analysis of mutant library. Applied Microbiology and Biotechnology85, 95–104.
73. Itoh, Y., Watanabe, J., Fukada, H., Mizuno, R., Kezuka, Y., Nonaka, T. and Watanabe, T. (2006). Importance of Trp59 and Trp60 in chitin-binding, hydrolytic, and antifungal activities of Streptomyces griseus chitinase C. Applied Microbiology and Biotechnology72, 1176–84.
74. Izume, M., Nagae, S., Kawagishi H., Mitsutomi M. and Ohtakara A. (1992). Action pattern of Bacillus sp no7 M chitosanase on partially N-acetylated chitosan. Bioscience, Biotechnology, and Biochemistry56, 448–53.
75. Jeon, Y. J., Park, P. J. and Kim, S.K. (2001). Antimicrobial effect of chitooligosaccharides produced by bioreactor. Carbohydrate Polymers44, 71–6.
76. Kafetzopoulos, D., Thireos, G., Vournakis, J.N. and Bouriotis, V. (1993). The primary structure of a fungal chitin deacetylase reveals the function for 2 bacterial gene products. Proceedings of the National Academy of Sciences of the United States of America90, 8005–8.
77. Karlsson, M. and Stenlid, J. (2008). Comparative evolutionary histories of the fungal chitinase gene family reveal non-random size expansions and contractions due to adaptive natural selection. Evolutionary Bioinformatics Online4, 47–60.
78. Karlson, M. and Stenlid, J. (2009). Evolution of family 18 glycoside hydrolases:diversity, domain structures and phylogenetic relationships. Journal of Molecular Microbiology and Biotechnology16, 208–23.
79. Kawase, T., Yokokawa, S., Saito, A., Fujii, T., Nikaidou, N., Miyashita, K. and Watanabe, T. (2006). Comparison of enzymatic and antifungal properties between family 18 and 19 chitinases from S. coelicolor A3(2). Bioscience, Biotechnology, and Biochemistry70, 988–98.
80. Kezuka, Y., Ohishi, M., Itoh, Y., Watanabe, J., Mitsutomi, M., Watanabe, T. and Nonaka, T. (2006). Structural studies of a two-domain chitinase from Streptomyces griseus HUT6037. Journal of Molecular Biology358, 472–84.
81. Khor, E. (2002). Chitin:a biomaterial in waiting. Current Opinion in Solid State & Materials Science6, 313–17.
82. Kikkawa, Y., Tokuhisa, H., Shingai, H., Hiraishi, T., Houjou, H., Kanesato, M., Imanaka, T. and Tanaka, T. (2008). Interaction force of chitin-binding domains onto chitin surface. Biomacromolecules9, 2126–31.
83. Kim, D.J., Baek, J.M., Uribe, P., Kenerley, C.M. and Cook, D.R. (2002). Cloning and characterization of multiple glycosyl hydrolase genes from Trichoderma virens. Current Genetics40, 374–84.
84. Kim, S. K. and Rajapakse, N. (2005). Enzymatic production and biological activities of chitosan oligosaccharides (COS):a review. Carbohydrate Polymers62, 357–68.
85. Kimoto, H., Kusaoke, H., Yamamoto, I., Fujii, Y., Onodera, T. and Taketo, A. (2002). Biochemical and genetic properties of Paenibacillus glycosyl hydrolase having chitosanase activity and discoidin domain. Journal of Biological Chemistry277, 14695–702.
86. Knapp, S., Vocadlo, D., Gao, Z.N., Kirk, B., Lou, J.P. and Withers, S.G. (1996). NAGthiazoline, an N-acetyl-beta-hexosaminidase inhibitor that implicates acetamido participation. Journal of the American Chemical Society118, 6804–5.
87. Kobayashi, S., Kiyosada, T. and Shoda, S. (1996). Synthesis of artificial chitin:Irreversible catalytic behavior of a glycosyl hydrolase through a transition state analogue substrate. Journal of the American Chemical Society118, 13113–4.
88. Koshland, D. E. (1953). Stereochemistry and the mechanism of enzymatic reactions. Biological Reviews of the Cambridge Philosophical Society28, 416–36.
89. Krajewska, B. (2004). Application of chitin- and chitosan-based materials for enzyme immobilizations:a review. Enzyme and Microbial Technology35, 126–39.
90. Kubota, N. and Eguchi, Y. (1997). Facile preparation of water-soluble N-acetylated chitosan and molecular weight dependence of its water-solubility. Polymer Journal29, 123–7.
91. Kurita, K. (2001). Controlled functionalization of the polysaccharide chitin. Progress in Polymer Science26, 1921–71.
92. Lacombe-Harvey, M. E., Fukamizo, T., Gagnon, J., Ghinet, M.G., Dennhart, N., Letzel, T. and Brzezinski, R. (2009). Accessory active site residues of Streptomyces sp. N174 chitosanase:variations on a common theme in the lysozyme superfamily. FEBS Journal276, 857–69.
93. Ladet, S., David, L. and Domard, A. (2008). Multi-membrane hydrogels. Nature452, 76–9.
94. Langer, R.C. and Vinetz, J.M. (2001). Plasmodium ookinete-secreted chitinase and parasite penetration of the mosquito peritrophic matrix. Trends in Parasitology17, 269–72.
95. Lima, L.H.C., Ulhoa, C.J., Fernandes, A.P. and Felix, C.R. (1997). Purification of a chitinase from Trichoderma sp. and its action on Sclerotium rolfsii and Rhizoctonia solani cell walls. Journal of Genetics and Applied Microbiology43, 31–7.
96. Liu, H. T., Li, W.M., Xu, G., Li, X.Y., Bai, X.F., Wei, P., Yu, C. and Du, Y.G. (2009). Chitosan oligosaccharides attenuate hydrogen peroxide-induced stress injury in human umbilical vein endothelial cells. Pharmacological Research59, 167–75.
97. Long, S. R. (1989). Rhizobium legume nodulation - life together in the underground. Cell56, 203–14.
98. Lorito, M., Hayes, C.K., Dipietro, A., Woo, S.L. and Harman, G.E. (1994). Purification, characterization, and synergistic activity of a glucan 1,3-beta-glucosidase and an N-acetyl-beta-glucosaminidase from Trichoderma harzianum. Phytopathology84, 398–405.
99. Maenaka, K., Kawai, G., Watanabe, K., Sunada, F. and Kumagai, I. (1994). Functional and structural role of a tryptophan generally observed in protein-carbohydrate interaction - Trp62 of hen egg-white lysozyme. Journal of Biologucal Chemistry269, 7070–5.
100. Marcotte, E. M., Monzingo, A.F., Ernst, S.R., Brzezinski, R. and Robertus, J.D. (1996). X-ray structure of an anti-fungal chitosanase from Streptomyces N174. Nature Structural Biology3, 155–62.
101. Mark, B. L., Vocadlo, D.J., Knapp, S., Triggs-Raine, B.L., Withers, S.G. and James, M.N.G. (2001). Crystallographic evidence for substrate-assisted catalysis in a bacterial beta-hexosaminidase. Journal of Biological Chemistry276, 10330–7.
102. Martinez, D., Berka, R.M., Henrissat, B., Saloheimo, M., etal. (2008). Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina) Nature Biotechnology26, 553–560.
103. Martinou, A., Kafetzopoulos, D. and Bouriotis, V. (1993). Isolation of chitin deacetylase from Mucor rouxii by immunoaffinity chromatography. Journal of Chromatography644, 35–41.
104. Martinou, A., Koutsioulis, D. and Bouriotis, V. (2002). Expression, purification, and characterization of a cobalt-activated chitin deacetylase (Cda2p) from Saccharomyces cerevisiae. Protein Expression and Purification24, 111–6.
105. Merino, S. T. and Cherry, J. (2007). Progress and challenges in enzyme development for biomass utilization. Advances in Biochemical Engineering/Biotechnology108,95–120.
106. Merzendorfer, H. and Zimoch, L. (2003). Chitin metabolism in insects:structure, function and regulation of chitin synthases and chitinases. Journal of Experimental Biology206, 4393–4412.
107. Minke, R. and Blackwell J. (1978). The structure of alpha-chitin. Journal of Molecular Biology120, 167–81.
108. Mitsutomi, M., Kidoh, H. Tomita, H. and Watanabe, T. (1995). The action of Bacillus circulans Wl-12 chitinases on partially N-acetylated chitosan. Bioscience Biotechnology and Biochemistry59, 529–31.
109. Mitsutomi, M., Isono, M., Uchiyama, A., Nikaidou, N., Ikegami, T. and Watanabe, T. (1998). Chitosanase activity of the enzyme previously reported as beta-1,3–1,4-glucanase from Bacillus circulans WL-12. Bioscience Biotechnology and Biochemistry62, 2107–14.
110. Mizuno, R., Fukamizo, T., Sugiyama, S., Nishizawa, Y., Kezuka, Y., Nonaka, T., Suzuki, K. and Watanabe, T. (2008). Role of the loop structure of the catalytic domain in rice class I chitinase. Journal of Biochemistry143, 487–95.
111. Monzingo, A. F., Marcotte, E.M., Hart, P.J. and Robertus, J.D. (1996). Chitinases, chitosanases, and lysozymes can be divided into procaryotic and eucaryotic families sharing a conserved core. Nature Structural Biology3, 133–40.
112. Neuhaus, J.M., Fritig, B., Linthorst, H.J.M., Meins, F., Mikkelsen, J.D. And Ryals, J. (1996). A revised nomenclature for chitinase genes. Plant Molecular Biology Reporter14, 102–4.
113. Ngo, D. N., Kim, M.M. and Kim, S.K. (2008). Chitin oligosaccharides inhibit oxidative stress in live cells. Carbohydrate Polymers74, 228–34.
114. Nishiyama, Y., Langan, P. and Chanzy, H. (2002). Crystal Structure and Hydrogen-Bonding System in Cellulose Iβ from Synchrotron X-ray and Neutron Fiber Diffraction. Journal of American Chemical Society124, 9074–82.
115. No, H. K. and Meyers, S.P. (2000). Application of chitosan for treatment of wastewaters. Reviews of Environmental Contamination and Toxicology163, 1–27.
116. Ohnishi, T., Juffer, A.H., Tamoi, M., Skriver, K. and Fukamizo, T. (2005). 26 kDa endochitinase from barley seeds:an interaction of the ionizable side chains essential for catalysis. Journal of Biochemistry138, 553–62.
117. Ohnishi, Y., Ishikawa, J., Hara, H., Suzuki, H., Ikenoya, M., Ikeda, H., Yamashita, A., Hattori, M. and Horinouchi, S. (2008). Genome sequence of the streptomycinproducing microorganism Streptomyces griseus IFO 13350. Journal of Bacteriology190, 4050–60.
118. Ohno, T., Armand, S., Hata, T., Nikaidou, N., Henrissat, B., Mitsutomi, M. and Watanabe, T. (1996). A modular family 19 chitinase found in the prokaryotic organism Streptomyces griseus HUT 6037. Journal of Bacteriology178, 5065–70.
119. Papanikolau, Y., Prag, G., Tavlas, G., Vorgias, C.E., Oppenheim, A.B. and Petratos, K. (2001). High resolution structural analyses of mutant chitinase A complexes with substrates provide new insight into the mechanism of catalysis. Biochemistry40, 11338–43.
120. Park, J.K., Shimono, K., Ochiai, N., Shigeru, K., Kurita, M., Ohta, Y., Tanaka, K., Matsuda, H. and Kawamukai, M. (1999). Purification, characterization, and gene analysis of a chitosanase (ChoA) from Matsuebacter chitosanotabidus 3001. Journal of Bacteriology181, 6642–9.
121. Paul, W. and Sharma, C.P. (2000). Chitosan, a drug carrier for the 21st century:a review. STP Pharma Sciences10, 5–22.
122. Pedraza-Reyes, M. and Gutierrez-Corona, F. (1997). The bifunctional enzyme chitosanase-cellulase produced by the gram-negative microorganism Myxobacter sp. AL-1 is highly similar to Bacillus subtilis endoglucanases. Archives of Microbiology168, 321–7.
123. Perrakis, A., Tews, I., Dauter, Z., Oppenheim, A.B., Chet, I., Wilson, K.S. and Vorgias, C.E. (1994). Crystal-structure of a bacterial chitinase at 2.3 angstrom resolution. Structure2, 1169–80.
124. Prashanth, K. V. H. and Tharanathan, R.N. (2005). Depolymerized products of chitosan as potent inhibitors of tumor-induced angiogenesis. Biochimica et Biophysica Acta1722,:22–29.
125. Psylinakis, E., Boneca, I.G., Mavromatis, K., Deli, A., Hayhurst, E., Foster, S.J., VÅrum, K.M. and Bouriotis, V. (2005). Peptidoglycan N-acetylglucosamine deacetylases from Bacillus cereus, highly conserved proteins in Bacillus anthracis. Journal of Biological Chemistry280, 30856–63.
126. Raabe, D., Al-Sawalmih, A., Yi, S. B. and Fabritius, H. (2007). Preferred crystallographic texture of alpha-chitin as a microscopic and macroscopic design principle of the exoskeleton of the lobster Homarus americanus. Acta Biomaterialia3, 882–95.
127. Rao, F. V., Houston, D.R., Boot, R.G., Aerts, J.M.F.G., Hodkinson, M., Adams, D.J., Shiomi, K., Omura, S. and van Aalten, D.M.F. (2005). Specificity and affinity of natural product cyclopentapeptide inhibitors against A. fumigatus, human, and bacterial chitinases. Chemistry and Biology12, 65–76.
128. Renkema, G. H., Boot, R.G., Muijsers, A.O., Donkerkoopman, W.E. and Aerts, J.M.F.G. (1995). Purification and characterization of human chitotriosidase, a novel member of the chitinase family of proteins. Journal of Biological Chemistry270, 2198–202.
129. Rinaudo, M. (2006). Chitin and chitosan:Properties and applications. Progress in Polymer Science31, 603–32.
130. Rinaudo M. and Domard A. (1989). Solution properties of chitosan. In Chitin and Chitosan:Sources, Chemistry, Biochemistry, Physical Properties and Applications eds G. Skjak-Braeck, T. Anthonsen and P.A. Sandford, pp. 71–86. New York:Elsevier Applied Science.
131. Robertus, J. D., Monzingo, A.F., Marcotte, E.M. and Hart, P.J. (1998). Structural analysis shows five glycohydrolase families diverged from a common ancestor. Journal of Experimental Zoology282, 127–32.
132. Robyt, J. F. and French, D. (1967). Multiple attack hypothesis of alpha-amylase action - action of porcine pancreatic human salivary and Aspergillus oryzae alpha-amylases. Archives of Biochemistry and Biophysics122, 8–16.
133. Robyt, J. F. and French, D. (1970). Multiple attack and polarity of action of porcine pancreatic alpha-amylase. Archives of Biochemistry and Biophysics138, 662–70.
134. Rye, C.S. and Withers, S.G. (2000). Glucosidase mechanisms. Current Opinion in Chemical Biology4, 573–80.
135. Saito, J., A. Kita, Higuchi, Y., Nagata, Y., ando, A. and Miki, K. (1999a). Crystal structure of chitosanase from Bacillus circulans MH-K1 at 1.6-A resolution and its substrate recognition mechanism. Journal of Biological Chemistry274, 30818–25.
136. Saito, A., Fujii, T., Redenbach, M., Ohno, T., Watanabe, T. and Miyashita, K. (1999b). High-multiplicity of chitinase genes in Streptomyces coelicolor A3(2). Bioscience, Biotechnology, and Biochemistry63, 710–8.
137. Saito, A., M. Ishizaka, Francisco, P.B., Fujii, T. and Miyashita, K. (2000). Transcriptional co-regulation of five chitinase genes scattered on the Streptomyces coelicolor A3(2) chromosome. Microbiology-UK146, 2937–46.
138. Sasaki, C., Itoh, Y., Takehara, H., Kuhara, S. and Fukamizo, T. (2003). Family 19 chitinase from rice (Oryza sativa L.):substrate-binding subsites demonstarted by kinetic and molecular modeling studies. Plant Molecular Biology52, 43–52.
139. Seidl, V., Huemer, B., Seiboth, B. and Kubicek, C.P. (2005). A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. FEBS Journal272, 5923–39.
140. Shahidi, F., Arachchi, J.K.V. and Jeon, Y.J. (1999). Food applications of chitin and chitosans. Trends in Food Science and Technology10, 37–51.
141. Shimono, K., Shigeru, K., Tsuchiya, A., Itou, N., Ohta, Y., Tanaka, K., Nakagawa, T., Matsuda, H. and Kawamukai, M. (2002). Two glutamic acids in chitosanase A from Matsuebacter chitosanotabidus 3001 are the catalytically important residues. Journal of Biochemistry131, 87–96.
142. Shimosaka, M., Kumehara, M., Zhang, X.Y., Nogawa, M. and Okazaki, M. (1996). Cloning and characterization of a chitosanase gene from the plant pathogenic fungus Fusarium solani. Journal of Fermentation and Bioengineering82, 426–31.
143. Shimosaka, M., Sato, K., Nishiwaki, N., Miyazawa, T. and Okazaki, W. (2005). Analysis of essential carboxylic amino acid residues for catalytic activity of fungal chitosanases by site-directed mutagenesis. Journal of Bioscience and Bioengineering100, 545–50.
144. Shoseyov, O., Shani, Z. and Levy, I. (2006). Carbohydrate binding modules:biochemical properties and novel applications. Microbiology and Molecular Biology Reviews70, 283–95.
145. Sikorski, P., Sorbotten, A., Horn, S.J., Eijsink, V.G.H. and VÅrum, K.M. (2006). Serratia marcescens chitinases with tunnel-shaped substrate-binding grooves show endo activity and different degrees of processivity during enzymatic hydrolysis of chitosan. Biochemistry45, 9566–74.
146. Sinnott, M. L. (1990). Catalytic mechanisms of enzymatic glycosyl transfer. Chemical Reviews90, 1171–1202.
147. Song, H. K. and Suh, S.W. (1996). Refined structure of the chitinase from barley seeds at 2.0 angstrom resolution. Acta Crystallographica. Section D, Biological Crystallography52, 289–98.
148. Sorbotten, A., Horn, S.J., Eijsink, V.G.H. and VÅrum, K.M. (2005). Degradation of chitosans with chitinase B from Serratia marcescens - production of chito-oligosaccharides and insight into enzyme processivity. FEBS Journal272, 538–49.
149. Strand, S. P., Issa, M.M., Christensen, B.E., Varum, K.M. and Artursson, P. (2008). Tailoring of chitosans for gene delivery:novel self-branched glycosylated chitosan oligomers with improved functional properties. Biomacromolecules9, 3268–76.
150. Suzuki, K., Sugawara, N., Suzuki, M., Uchiyama, T., Katouno, F., Nikaidou, N. and Watanabe, T. (2002). Chitinases A, B, and C1 of Serratia marcescens 2170 produced by recombinant Escherichia coli:Enzymatic properties and synergism on chitin degradation. Bioscience, Biotechnology, and Biochemistry66, 1075–83.
151. Suzuki, K., Suzuki, M., Taiyoji M., Nikaidou, N. and Watanabe, T. (1998). Chitin binding protein (CBP21) in the culture supernatant of Serratia marcescens 2170. Bioscience, Biotechnology, and Biochemistry62, 128–35.
152. Suzuki, K., Taiyoji, M., Sugawara, N., Nikaidou, N., Henrissat, B. and Watanabe, T. (1999). The third chitinase gene (chiC) of Serratia marcescens 2170 and the relationship of its product to other bacterial chitinases. Biochemical Journal343, 587–96.
153. Synstad, B., Gaseidnes, S., van Aalten, D.M.F., Vriend, G., Nielsen, J.E. and Eijsink, V.G.H. (2004). Mutational and computational analysis of the role of conserved residues in the active site of a family 18 chitinase. European Journal of Biochemistry271, 253–62.
154. Tang, C. M., Chye, M.L., Ramalingam, S., Ouyang, S.W., Zhao, K.J., Ubhayasekera, W. and Mowbray, S.L. (2004). Functional analyses of the chitin-binding domains and the catalytic domain of Brassica juncea chitinase BjCHI1. Plant Molecular Biology56, 285–98.
155. Taylor, E. J., Gloster, T.M., Turkenburg, J.P., Vincent, F., Brzozowski, A.M., Dupont, C., Shareck, F., Centeno, M.S.J., Prates, J.A.M., Puchart, V., Ferreira, L.M.A., Fontes, C.M.G.A., Biely, P. and Davies, G.J. (2006). Structure and activity of two metal ion-dependent acetylxylan esterases involved in plant cell wall degradation reveals a close similarity to peptidoglycan deacetylases. Journal of Biological Chemistry281, 10968–75.
156. Tews, I., Perrakis, A., Oppenheim, A., Dauter, Z., Wilson, K.S. and Vorgias, C.E. (1996). Bacterial chitobiase structure provides insight into catalytic mechanism and the basis of Tay-Sachs disease. Nature Structural Biology3, 638–48.
157. Tews, I., Van Scheltinga, A.C.T., Perrakis, A., Wilson, K.S. and Dijkstra, B.W. (1997). Substrate-assisted catalysis unifies two families of chitinolytic enzymes. Journal of American Chemical Society119, 7954–9.
158. Tharanathan, R. N. and Kittur, F.S. (2003). Chitin - The undisputed biomolecule of great potential. Critical Reviews in Food Science and Nutrition43, 61–87.
159. Tokuyasu, K., Ohnishi-Kameyama, M., Hayashi, K. and Mori, Y. (1999). Cloning and expression of chitin deacetylase gene from a Deuteromycete, Colletotrichum lindemuthianum. Journal of Bioscience and Bioengineering87, 418–23.
160. Tronsmo, A. (1991). Biological and Integrated Controls of Botrytis cinerea on Apple with Trichoderma harzianum. Biological Control1, 59–62.
161. Tsigos, I., Martinou, A., Kafetzopoulos, D. and Bouriotis, V. (2000). Chitin deacetylases:new, versatile tools in biotechnology. Trends in Biotechnology18, 305–12.
162. Ubhayasekera, W., Tang, C.M., Ho, S.W.T., Berglund, G., Bergfors, T., Chye, M.L. and Mowbray, S.L. (2007). Crystal structures of a family 19 chitinase from Brassica juncea show flexibility of binding cleft loops. FEBS Journal274, 3695–703.
163. Vaaje-Kolstad, G., Horn, S.J., van Aalten, D.M.F., Synstad, B. and Eijsink, V.G.H. (2005a). The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. Journal of Biological Chemistry280, 28492–7.
164. Vaaje-Kolstad, G., Houston, D.R., Riemen, A.H.K., Eijsink. V.G.H. and van Aalten, D.M.F. (2005b). Crystal structure and binding properties of the Serratia marcescens chitin-binding protein CBP21. Journal of Biological Chemistry 280, 11313–9.
165. Vaaje-Kolstad, G., Bunaes, A.C., Mathiesen, G. and Eijsink, V.G.H. (2009). The chitinolytic system of Lactococcus lactis ssp lactis comprises a nonprocessive chitinase and a chitin-binding protein that promotes the degradation of alpha- and beta-chitin. FEBS Journal276, 2402–15.
166. Van Aalten, D.M.F., Komander, D., Synstad, B., Gaseidnes, S., Peter, M.G. and Eijsink, V.G.H. (2001). Structural insights into the catalytic mechanism of a family 18 exo-chitinase. Proceedings of the National Academy of Sciences of the United States of America98, 8979–84.
167. Van Aalten, D.M.F., Synstad, B., Brurberg, M.B., Hough, E., Riise, B.W., Eijsink, V.G.H. and Wierenga, R.K. (2000). Structure of a two-domain chitotriosidase from Serratia marcescens at 1.9 angstrom resolution. Proceedings of the National Academy of Sciences of the United States of America97, 5842–7.
168. Van Petegem, F., Collins, T., Meuwis, M.A., Gerday, C., Feller, G. and Van Beeumen, J. (2003). The structure of a cold-adapted family 8 xylanase at 1.3 angstrom resolution - Structural adaptations to cold and investigation of the active site. Journal of Biological Chemistry278, 7531–9.
169. Van Scheltinga, A. C. T., Armand, S., Kalk, K.H., Isogai, A., Henrissat, B. and Dijkstra, B.W. (1995). Stereochemistry of chitin hydrolysis by a plant chitinase lysozyme and X-ray structure of a complex with allosamidin - evidence for substrate assisted catalysis. Biochemistry34, 15619–23.
170. Van Scheltinga, A. C. T., Kalk, K.H., Beintema, J.J. and Dijkstra, B.W. (1994). Crystal-structures of hevamine, a plant defense protein with chitinase and lysozyme activity, and its complex with an inhibitor. Structure2, 1181–9.
171. Varrot, A., Frandsen, T.P., von Ossowski, I., Boyer, V., Cottaz, S., Driguez, H., Schulein, M. and Davies, G.J. (2003). Structural basis for ligand binding and processivity in cellobiohydrolase Cel6A from Humicola insolens. Structure11, 855–64.
172. Vårum, K. M., Ottoy, M.H. and Smidsrød, O. (1994). Water-solubility of partially N-acetylated chitosans as a function of pH - effect of chemical-composition and depolymerization. Carbohydrate polymers25, 65–70.
173. Vårum, K.M., Holme, H.K., Izume, M., Stokke, B.T. and Smidsrød, O. (1996). Determination of enzymatic hydrolysis specificity of partially N-acetylated chitosans. Biochimica et Biophysica Acta1291, 5–15.
174. Verburg, J.G., Rangwala, S.H., Samac, D.A., Luckow, V.A. and Huynh, Q.K. (1993). Examination of the role of tyrosine-174 in the catalytic mechanism of the Arabidopsis thaliana chitinase:comparison of variant chitinases generated by site-directed mutagenesis and expressed in insect cells using baculovirus vectors. Archives of Biochemistry and Biophysics300, 223–30.
175. Vincent, F., Charnock, S.J., Verschueren, K.H.G., Turkenburg, J.P., Scott, D.J., Offen, W.A., Roberts, S., Pell, G., Gilbert, H.J., Davies, G.J. and Brannigan, J.A. (2003). Multifunctional xylooligosaccharide/cephalosporin C deacetylase revealed by the hexameric structure of the Bacillus subtilis enzyme at 1.9 angstrom resolution. Journal of Molecular Biology330, 593–606.
176. Viterbo, A., Haran, S., Friesem, D., Ramot, O. and Chet, I. (2001). Antifungal activity of a novel endochitinase gene (chit36) from Trichoderma harzianum Rifai TM. FEMS Microbiology Letters200, 169–74.
177. Viterbo, A., Montero, M., Ramot, O., Friesem, D., Monte, E., Llobell, A. and Chet, I. (2002). Expression regulation of the endochitinase chit36 from Trichoderma asperellum (T. harzianum T-203). Current Genetics42, 114–22.
178. Vocadlo, D. J., Davies, G.J., Laine, R. and Withers, S.G. (2001). Catalysis by hen egg-white lysozyme proceeds via a covalent intermediate. Nature412, 835–8.
179. Vocadlo, D. J. and Withers, S.G. (2005). Detailed comparative analysis of the catalytic mechanisms of beta-N-acetylglucosaminidases from families 3 and 20 of glycoside hydrolases. Biochemistry44, 12809–18.
180. Vollmer, W. and Tomasz, A. (2000). The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. Journal of Biological Chemistry275, 20496–501.
181. Watanabe, T., Ito, Y., Yamada, T., Hashimoto, M., Sekine, S. and Tanaka, H. (1994). The roles of the C-terminal domain and type III domains of chitinase A1 from Bacillus circulans WL-12 in chitin degradation. Journal of Bacteriology176, 4465–72.
182. 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. Biochemical Journal376, 237–44.
183. 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 Wl12 as essential residues for chitinase activity. Journal of Biological Chemistry268, 18567–72.
184. Woo, S. L., Donzelli, B., Scala, F., Mach, R., Harman, G.E., Kubicek, C.P., Del Sorbo, G. and Lorito, M. (1999). Disruption of the ech42 (endochitinase-encoding) gene affects biocontrol activity in Trichoderma harzianum P1. Molecular Plant Microbe Interaction12, 419–29.
185. Wu, H. G., Yao, Z., Bal, X.F., Du, Y.G. and Lin, B.C. (2008). Anti-angiogenic activities of chitooligosaccharides. Carbohydrate Polymers73, 105–10.
186. Xia, W., Liu, P., and Liu, J. (2008). Advance in chitosan hydrolysis by non-specific cellulases. Bioresource Technology99, 6751–62.
187. Xu, J. G., Zhao, X.M., Han, X.W. and Du, Y.G. (2007). Antifungal activity of oligochitosan against Phytophthora capsici and other plant pathogenic fungi in vitro. Pesticide Biochemistry and Physiology87, 220–8.
188. Zakariassen, H., Aam, B.B., Horn, S.J., Vårum, K.M., Sorlie, M. and Eijsink, V.G.H. (2009). Aromatic residues in the catalytic center of chitinase A from Serratia marcescens affect processivity, enzyme activity, and biomass converting efficiency. Journal of Biological Chemistry284, 10610–7.
189. Usefulness of Kinetic Enzyme Parameters in Biotechnological Practice