Processivity and substrate-binding in family 18 chitinases

Biocatalysis and Biotransformation

Volumn 30, Issue 3, 2012, Pages 353-365

  Sorlie, Morten ^a   Zakariassen, Henrik ^a   Norberg, Anne Line ^a   Eijsink, Vincent G H ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Chitinase; Glycoside hydrolase; Processivity; Substrate binding

Indexed keywords

BIOREFINERIES; BIOREFINING; CHITINASES; ENZYMATIC CONVERSIONS; GLYCOSIDE HYDROLASES; KEY TECHNOLOGIES; PROCESSIVITY; STRUCTURAL BASIS; SUBSTRATE-BINDING;

ENZYMES; POLYSACCHARIDES; REFINING;

BINDING ENERGY;

CELLULOSE; CHITIN; CHITINASE; POLYSACCHARIDE;

BIOMASS; CATALYSIS; DEPOLYMERIZATION; ENZYME ANALYSIS; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; REVIEW;

BINDING; BIOMASS; CATALYSTS; CELLULOSE; CHITIN; ENZYMES; POLYSACCHARIDES; SUBSTRATES;

EID: 84861176066     PISSN: 10242422     EISSN: 10292446     Source Type: Journal    
DOI: 10.3109/10242422.2012.676282     Document Type: Review

References (90)

1. Aam BB, Heggset EB, Norberg AL, Sårlie M, Vårum KM, Eijsink VGH. 2010. Production of chitooligosaccharides and their potential applications in medicine. Marine Drugs 8:1482-1517.
2. Aronson NN, Halloran BA, Alexyev MF, Amable L, Madura JD, Pasupulati L, Worth C, Van Roey P. 2003. Family 18 chitinaseoligosaccharide substrate interaction: subsite preference and anomer selectivity of Serratia marcescens chitinase A. Biochem J 376:87-95. (Pubitemid 37487205)
3. Baban J, Fjeld S, Sakuda S, Eijsink VGH, Sårlie M. 2010. The roles of three serratia marcescens chitinases in chitin conversion are refl ected in different thermodynamic signatures of allosamidin binding. J Phys Chem B 114:6144-6149.
4. Baker BM, Murphy KP. 1997. Dissecting the energetics of a protein-protein interaction: the binding of ovomucoid third domain to elastase. J Mol Biol 268:557-569. (Pubitemid 27208074)
5. Baldwin RL. 1986. Temperature dependence of the hydrophobic interaction in protein folding. Proc Natl Acad Sci USA 83:8069-8072. (Pubitemid 17182445)
6. Beckham Gregg T, Michael F. Crowley. 2011. Examination of the a -Chitin structure and decrystallization thermodynamics at the nanoscale. J Phys Chem B 115:4516-4522.
7. Biarnes X, Ardevol A, Planas A, Rovira C, Laio A, Parrinello M. 2007. The conformational free energy landscape of ae-DGlucopyranose. Implications for substrate preactivation in ae-Glucoside Hydrolases. J Am Chem Soc 129:10686-10693. (Pubitemid 350067477)
8. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. 2004. Carbohydratebinding modules: fi ne-tuning polysaccharide recognition. Biochem J 382:769-781. (Pubitemid 39312891)
9. Bozonnet S, Jensen MT, Nielsen MM, Aghajari N Jensen MH, Kramhåft B, Willemo as M, Tranier Sl, Haser R, Svensson B. 2007. The 'pair of sugar tongs' site on the non-catalytic domain C of barley a -amylase participates in substrate binding and activity. FEBS J 274:5055-5067. (Pubitemid 47481177)
10. Breyer WA, Mattthews BW. 2001. A structural basis for processivity. Protein Sci 10:1699-1711. (Pubitemid 32851041)
11. Cederkvist FH, Parmer MP, Vårum KM, Eijsink VGH, Sårlie M. 2008. Inhibition of a family 18 chitinase by chitooligosaccharides. Carbohyd Polym 74:41-49.
12. Cederkvist FH, Saua SF, Karlsen V, Sakuda S, Eijsink VGH, Sårlie M. 2007. Thermodynamic analysis of allosamidin binding to a family 18 chitinase. Biochemistry 46:12347-12354. (Pubitemid 350022389)
13. Cooper A, Johnson CM, Lakey JH, Nollmann M. 2001. Heat does not come in different colours: entropy-enthalpy compensation, free energy windows, quantum confi nement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions. Biophys Chem 93:215-230. (Pubitemid 34142188)
14. Davies G, Henrissat B. 1995. Structures and mechanisms of glycosyl hydrolases. Structure 3:853-859.
15. Davies GJ, Tolley SP,Henrissat B,Hjort C, Schulein M. 1995. Structures of oligosaccharide-bound forms of the endoglucanase V from Humicola insolens at 1.9 A resolution. Biochemistry 34:16210-16220.
16. Divne C, Ståhlberg J, Teeri TT, Alwyn Jones T. 1998. Highresolution crystal structures reveal how a cellulose chain is bound in the 50ålong tunnel of cellobiohydrolase I from Trichoderma reesei . J Mol Biol 275:309-325. (Pubitemid 28030006)
17. Donnelly LE, Barnes PJ. 2004. Acidic mammalian chitinase-a potential target for asthma therapy. Trends Pharmacol Sci 25:509-511. (Pubitemid 39233562)
18. Dunitz JD. 1995. Win some, lose some-Enthalpy-entropy compensation in weak intermolecular interactions. Chem Biol 2:709-712.
19. Eijsink VGH, Vaaje-Kolstad G, Vårum KM, Horn SJ. 2008. Towards new enzymes for biofuels: lessons from chitinase research. Trends Biotechnol 26:228-235.
20. Harjunpaa V, Teleman A, Koivula A, Ruohonen L, Teeri TT, Teleman O, Drakenberg T. 1996. Cello-oligosaccharide hydrolysis by cellobiohydrolase II from Trichoderma reesei. Association and rate constants derived from an analysis of progress curves. Eur J Biochem 240:584-591. (Pubitemid 26321159)
21. Heggset EB, Hoell IA, Kristoffersen M, Eijsink VG, Vårum KM. 2009. Degradation of chitosans with chitinase G from Streptomyces coelicolor A3(2): production of chito-oligosaccharides and insight into subsite specifi cities. Biomacromolecules 10:892-899.
22. Henrissat B, Davies GJ. 1997. Structural and sequence-based classifi cation of glycoside hydrolases. Curr Opin Struct Biol 7:637-644. (Pubitemid 27472582)
23. Hervá C, Rogowski A, Blake AW, Marcus SE, Gilbert HJ, Knox JP. 2010. Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects. Proc Natl Acad Sci USA 107:15293-15298.
24. Hoell IA, Dalhus B, Heggset EB, Aspmo SI, Eijsink VGH. 2006. Crystal structure and enzymatic properties of a bacterial family 19 chitinase reveal differences from plant enzymes. FEBS J 273:4889-4900. (Pubitemid 44583513)
25. Horn SJ, Sikorski P, Cederkvist JB, Vaaje-Kolstad G, Sårlie M, Synstad B, Vriend G, Vårum KM, Eijsink VGH. 2006a. Costs and benefi ts of processivity in enzymatic degradation of recalcitrant polysaccharides. Proc Natl Acad Sci USA 103:18089-18094. (Pubitemid 44871617)
26. Horn SJ, Sårbotten A, Synstad B, Sikorski P, Sårlie M, Vårum KM, Eijsink VGH. 2006b. Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS J 273:491-503.
27. Horn SJ, Sårlie M, Vaaje-Kolstad G, Norberg AL, Synstad B, Vårum KM, Eijsink VGH. 2006c. Comparative studies of chitinases A, B and C from Serratia marcescens Biocatal Biotransfor 24:39-53. (Pubitemid 43771944)
28. Hu GH, Oguro A, Li CZ, Gershon PD, Quiocho FA. 2002. The ''cap-binding slot'' of an mRNA cap-binding protein: Quantitative effects of aromatic side chain choice in the double-stacking sandwich with cap. Biochemistry 41:7677-7687. (Pubitemid 34627795)
29. Hult EL, Katouno F, Uchiyama T, Watanabe T, Sugiyama J. 2005. Molecular directionality in crystalline beta-chitin: hydrolysis by chitinases A and B from Serratia marcescens 2170. Biochem J 388:851-856. (Pubitemid 40941572)
30. Igarashi K, Koivula A, Wada M, Kimura S, Penttila M, Samejima M. 2009. High speed atomic force microscopy visualizes processive movement of Trichoderma reesei cellobiohydrolase I on crystalline cellulose. J Biol Chem 284:36186-36190.
31. Jalak J, Valjamae P. 2010. Mechanism of initial rapid rate retardation in cellobiohydrolase catalyzed cellulose hydrolysis. Biotechnol Bioeng 106:871-883.
32. Je JY, Kim EK, Ahn CB, Moon SH, Jeon BT, Kim B, Park TK, Park PJ. 2007. Sulfated chitooligosaccharides as prolyl endopeptidase inhibitor. Int J Biol Macromol 41: 529-533. (Pubitemid 47575748)
33. Kipper K, Våljamåe P, Johansson G. 2005. Processive action of cellobiohydralese Cel7A from Trichoderma reesei is revealed as 'burst 'kinetics on fl uoroscent polymeric model substrates. Biochem J 385:527-535. (Pubitemid 40165086)
34. Koivula A, Kinnari T, Harjunpaa V, Ruohonen L, Teleman A, Drakenberg T, Rouvinen J, Jones TA, Teeri TT. 1998. Tryptophan 272: an essential determinant of crystalline cellulose degradation by Trichoderma reesei cellobiohydrolase Cel6A. FEBS Lett 429:341-346. (Pubitemid 28300388)
35. Kuraain M, Våljamåe P. 2011. Processivity of cellobiohydrolases is limited by the substrate. J Biol Chem 286:169-177.
36. Li Y, Irwin DC, Wilson DB. 2007. Processivity, substrate binding, and mechanism of cellulose hydrolysis by Thermobifi da fusca Cel9A. Appl Environ Microbiol 73:3165-3172. (Pubitemid 46834966)
37. Lienemann M, Boer H, Paananen A, Cottaz S, Koivula A. 2009. Toward understanding of carbohydrate binding and substrate specifi city of a glycosyl hydrolase 18 family (GH-18) chitinase from Trichoderma harzianum . Glycobiology 19:1116-1126.
38. L ä Y, Yang H, Hu H, Wang Y, Rao Z, Jin C. 2008. Mutation of Trp137 to glutamate completely removes transglycosyl activity associated with Aspergillus fumigatus AfChiB1. Glycoconj J 26:525-534.
39. Mackenzie LF, Sulzenbacher G, Divne C, Jones TA, Woldike HF, Schulein M, Withers SG, Davies GJ. 1998. Crystal structure of the family 7 endoglucanase I (Cel7B) from Humicola insolens at 2.2 angstrom resolution and identifi cation of the catalytic nucleophile by trapping of the covalent glycosyl-enzyme intermediate. Biochem J 335:409-416.
40. Mandelman D, Belaich A, Belaich JP, Aghajari N, Driguez H, Haser R. 2003. X-ray crystal structure of the multidomain endoglucanase Cel9G from Clostridium cellulolyticum complexed with natural and synthetic cello-oligosaccharides. J Bacteriol 185:4127-4135. (Pubitemid 36835252)
41. Merino S, Cherry J. 2007. Progress and challenges in enzyme development for biomass utilization. Adv Biochem Eng Biotechnol 108:95-120. (Pubitemid 47434544)
42. Meyer JE, Schulz GE. 1997. Energy profi le of maltooligosaccharide permeation through maltoporin as derived from the structure and from a statistical analysis of saccharide-protein interactions. Protein Sci 6:1084-1091. (Pubitemid 27194149)
43. Murphy KP. 1994. Hydration and convergence temperatures-on the use and interpretation of correlation plots. Biophys Chem 51:311-326.
44. Nishio M, Hirota M, Umezwa Y. 1998. The CH/p Interaction: Evidence, Nature, and Consequences. New York: Wiley.
45. Norberg AL, Dybvik AI, Zakariassen H, Mormann M, Peter-Katalinic AJ, Eijsink VGH, Sårlie M. 2011. Substrate positioning in chitinase A, a processive chito-biohydrolase from Serratia marcescens . FEBS Letters DOI: 10.1016/j.febslet.2011.06.002.
46. Norberg AL, Eijsink VGH, Sårlie M. 2010a. Dissecting Factors that Contribute to Ligand-Binding Energetics for Family 18 Chitinases. Thermochim.Acta 511:189-193.
47. Norberg AL, Karlsen V, Hoell IA, Bakke I, Eijsink VGH, Sårlie M. 2010b. Determination of substrate binding energies in individual subsites of a family 18 chitinase. FEBS Lett 584:4581-4585.
48. Papanikolau Y, Prag G, Tavlas G, Vorgias CE, Oppenheim AB, Petratos K. 2001. High resolution structural analyses of mutant chitinase A complexes with substrates provide new insight into the mechanism of catalysis. Biochemistry 40:11338-11343. (Pubitemid 32911276)
49. Papanikolau Y, Tavlas G, Vorgias CE, Petratos K. 2003. De novo purifi cation scheme and crystallization conditions yield high-resolution structures of chitinase A and its complex with the inhibitor allosamidin. Acta Crystallographica Section D-Biological Crystallography 59:400-403. (Pubitemid 36224875)
50. Parsiegla G, Juy M, Reverbel-Leroy C, Tardif C, Belaich JP, Driguez H, Haser R. 1998. The crystal structure of the processive endocellulase CelF of Clostridium cellulolyticum in complex with a thiooligosaccharide inhibitor at 2.0 angstrom resolution. EMBO J. 17:5551-5562. (Pubitemid 28445967)
51. Parsiegla G, Reverbel-Leroy C, Tardif C, Belaich JP, Driguez H, Haser R. 2000. Crystal structures of the cellulase Ce148F in complex with inhibitors and substrates give insights into its processive action. Biochemistry 39:11238-11246.
52. Parsiegla G, Reverbel C, Tardif C, Driguez H, Haser R. 2008. Structures of mutants of cellulase Cel48F of Clostridium cellulolyticum in complex with long hemithiocellooligosaccharides give rise to a new view of the substrate pathway during processive action. J Mol Biol 375:499-510. (Pubitemid 350199663)
53. Perrakis A, Tews I, Dauter Z, Oppenheim AB, Chet I, Wilson KS, Vorgias CE. 1994. Crystal structure of a bacterial chitinase at 2.3 A resolution. Structure. 2:1169-1180. (Pubitemid 124001316)
54. Quiocho FA. 1989. Protein-Carbohydrate interactions-Basic molecular-features. Pure Appl Chem 61:1293-1306.
55. Rahman A, Kumar SG, Kim SW, Hwang HJ, Baek YM, Lee SH, Hwang HS, Shon YH, Nam KS, Yun JW. 2008. Proteomic analysis for inhibitory effect of chitosan oligosaccharides on 3T3-L1 adipocyte differentiation. Proteomics 8:569-581. (Pubitemid 351252014)
56. Robert X, Haser R, Mori H, Svensson B, Aghajari N. 2005. Oligosaccharide binding to Barley a -Amylase 1. J Biol Chem 280:32968-32978.
57. Roby D, Gadelle A, Toppan A. 1987. Chitin oligosaccharides as elicitors of chitinase activity in melon plants. Biochem Biophys Res Commun 143:885-892.
58. Rouvinen J, Bergfors T, Teeri T, Knowles JK, Jones TA. 1990. Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science 249:380-386.
59. Sakon J, Irwin D, Wilson DB, Karplus PA. 1997. Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca . Nat Struct Mol Biol 4:810-818. (Pubitemid 27435346)
60. Sikorski P, Sårbotten A, Horn SJ, Eijsink VGH, Vårum KM. 2006. Serratia marcescens chitinases with tunnel-shaped substratebinding grooves show endo activity and different degrees of processivity during enzymatic hydrolysis of chitosan. Biochemistry 45:9566-9574. (Pubitemid 44223260)
61. Sårbotten A, Horn SJ, Eijsink VGH, Vårum KM. 2005. Degradation of chitosans with chitinase B from Serratia marcescens. Production of chito-oligosaccharides and insight into enzyme processivity. FEBS J 272:538-549.
62. Spezio M, Wilson DB, Karplus PA. 1993. Crystal-structure of the catalytic domain of a thermophilic endocellulase Biochemistry 32:9906-9916. (Pubitemid 23312416)
63. Synowiecki J, Al-Khateeb NA. 2003. Production, properties, and some new applications of chitin and its derivatives. Crit Rev Food Sci 43:145-171. (Pubitemid 38552306)
64. Synstad B, Gåseidnes S, van Aalten DMF, Vriend G, Nielsen JE, Eijsink VGH. 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)
65. Taira T, Fujiwara M, Dennhart N, Hayashi H, Onaga S, Ohnuma T, Letzel T, Sakuda S, Fukamizo T. 2010. Transglycosylation reaction catalyzed by a class V chitinase from cycad, Cycas revoluta: A study involving site-directed mutagenesis, HPLC, and real-time ESI-MS. Biochimica et Biophysica Acta (BBA)-Proteins & Proteomics 1804:668-675.
66. Teeri TT. 1997. Crystalline cellulose degradation: new insight into the function of cellobiohydrolases. Trends Biotechnol 15: 160-167. (Pubitemid 27219573)
67. Terwisscha van Scheltinga AC, Armand S, Kalk KH, Isogai A, Henrissat B, Dijkstra BW. 1995. Stereochemistry of chitin hydrolysis by a plant chitinase/lysozyme and X-ray structure of a complex with allosamidin: evidence for substrate assisted catalysis. Biochemistry 34:15619-15623.
68. Tews I, Terwisscha van Scheltinga AC, Perrakis A, Wilson KS, Dijkstra BW. 1997. Substrate-assisted catalysis unifi es two families of chitinolytic enzymes. J Am Chem Soc 119:7954-7959. (Pubitemid 27380255)
69. Uchiyama T, Katouno F, Nikaidou N, Nonaka T, Sugiyama J, Watanabe T. 2001. Roles of the exposed aromatic residues in crystalline chitin hydrolysis by chitinase a from Serratia marcescens 2170. J Biol Chem 276:41343-41349.
70. Vaaje-Kolstad G, Houston DR, Rao FV, Peter MG, Synstad B, van Aalten DMF, Eijsink VGH. 2004. Structure of the D142N mutant of the family 18 chitinase ChiB from Serratia marcescens and its complex with allosamidin. Biochim Biophys Acta 1696:103- 111. (Pubitemid 38223890)
71. van Aalten DMF, Komander D, Synstad B, Gåseidnes S, Peter MG, Eijsink VGH. 2001. Structural insights into the catalytic mechanism of a family 18 exo-chitinase. Proc Natl Acad Sci USA 98:8979-8984. (Pubitemid 32743855)
72. van Aalten DMF, Synstad B, Brurberg MB, Hough E, Riise BW, Eijsink VGH, Wierenga RK. 2000. Structure of a two-domain chitotriosidase from Serratia marcescens at 1.9-angstrom resolution. Proc Natl Acad Sci USA 97:5842-5847. (Pubitemid 30367486)
73. van Eijk M, van Roomen CPAA, Renkema GH, Bussink AP, Andrews L, Blommaart EFC, Sugar A, Verhoeven AJ, Boot RG, Aerts JMFG. 2005. Characterization of human phagocytederived chitotriosidase, a component of innate immunity. Int Immun 17:1505-1512. (Pubitemid 41631326)
74. Varrot A, Frandsen TP, von Ossowski I, Boyer V, Cottaz S, Driguez H, Schulein M, Davies GJ. 2003. Structural basis for ligand binding and processivity in Cellobiohydrolase Cel6A from Humicola insolens . Structure 11:855-864. (Pubitemid 36833271)
75. Varrot A, Hastrup S, Sch ä lein M, Davies GJ. 1999a. Crystal structure of the catalytic core domain of the family 6 cellobiohydrolase II, Cel6A, from Humicola insolens , at 1.92 A resolution. Biochem J 337:297-304. (Pubitemid 29052024)
76. Varrot A, Schulein M, Davies GJ. 1999b. Structural changes of the active site tunnel of Humicola insolens cellobiohydrolase, Cel6A, upon oligosaccharide binding. Biochemistry 38:8884-8891.
77. Varrot A, Schulein M, Davies GJ. 2000. Insights into ligandinduced conformational change in Cel5A from Bacillus agaradhaerens revealed by a catalytically active crystal form. J Mol Biol 297:819-828.
78. von Ossowski I, Stahlberg J, Koivula A, Piens K, Becker D, Boer H, Harle R, Harris M, Divne C, Mahdi S, Zhao Y, Driguez H, Claeyssens M, Sinnott ML, Teeri TT. 2003. Engineering the exo-loop of Trichoderma reesei Cellobiohydrolase, Cel7A. A comparison with Phanerochaete chrysosporium Cel7D. J Mol Biol 333:817-829. (Pubitemid 37268020)
79. Vuong TV, Wilson DB. 2009. Processivity, synergism, and substrate specifi city of Thermobifi da fusca Cel6B. Appl Environ Microbiol 75:6655-6661.
80. Vyas Nand K. 1991. Atomic features of protein-carbohydrate interactions. Curr Opin Struct Biol 1:732-740.
81. Watanabe T, Ito Y, Yamada T, Hashimoto M, Sekine S, 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. J Bacteriol 176:4465-4472. (Pubitemid 24237947)
82. Williams SJ, Davies GJ. 2001. Protein-carbohydrate interactions: learning lessons from nature. Trends Biotechnol 19:356-362. (Pubitemid 32769890)
83. Zakariassen H, Eijsink VGH, Sårlie M. 2010a. Signatures of activation parameters reveal substrate-dependent rate determining steps in polysaccharide turnover by a family 18 chitinase. Carbohyd Polym 81:14-20.
84. Zakariassen H, Hansen MC, Jåranli M, Eijsink VGH, Sårlie M. 2011. Mutational effects on transglycosylating activity of family 18 chitinases and construction of a hypertransglycosylating mutant. Biochemistry 50:5693-5703.
85. Zakariassen H, Klemetsen L, Sakuda S, Vaaje-Kolstad G, Vårum KM, Sårlie M, Eijsink VGH. 2010b. Effect of enzyme processivity on the effi cacy of a competitive chitinase inhibitor. Carbohyd Polym 82:779-785.
86. Zakariassen H, Aam BB, Horn SJ, Vårum KM, Sårlie M, Eijsink VGH. 2009. Aromatic residues in the catalytic center of chitinase A from Serratia marcescens affect processivity, enzyme activity, and biomass converting effi ciency. J Biol Chem 284:10610-10617.
87. Zhang S, Wilson DB. 1997. Surface residue mutations which change the substrate specifi city of Thermomonospora fusca endoglucanase E2. J Biotechnol 57:101-113. (Pubitemid 27397475)
88. Zhou W, Irwin DC, Escovar-Kousen J, Wilson DB. 2004. Kinetic studies of Thermobifi da fusca Cel9A active site mutant enzymes. Biochemistry 43:9655-9663. (Pubitemid 38993815)
89. Zhu Z, Zheng T, Homer RJ, Kim YK, Chen NY, Cohn L, Hamid Q, Elias JA. 2004. Acidic mammalian chitinase in asthmatic Th2 infl ammation and IL-13 pathway activation. Science 304:1678-1682. (Pubitemid 38765861)
90. Zou J, Kleywegt GJ, Stahlberg J, Driguez H, Nerinckx W, Claeyssens M, Koivula A, Teeri TT, Jones TA. 1999. Crystallographic evidence for substrate ring distortion and protein conformational changes during catalysis in cellobiohydrolase Ce16A from trichoderma reesei. Structure 7: 1035-1045. (Pubitemid 29436501)