Xylanase XYN IV from Trichoderma reesei showing exo- and endo-xylanase activity

FEBS Journal

Volumn 280, Issue 1, 2013, Pages 285-301

  Tenkanen, Maija ^a,d   Vršanská, Mária ^b   Siika Aho, Matti ^a   Wong, Dominic W ^c   Puchart, Vladimír ^b   Penttilä, Merja ^a   Saloheimo, Markku ^a   Biely, Peter ^b  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

^c WESTERN REGIONAL RESEARCH CENTER   (United States)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

exo and endo acting 1,4 xylanase; glycoside hydrolase family 30; Trichoderma reesei; xylan; xylooligosaccharides

Indexed keywords

BETA 1,4 GLUCAN; BETA 1,4 MANNAN; BETA 1,4 XYLAN; CELLULASE; COMPLEMENTARY DNA; EG I PROTEIN; ENDO 1,4 BETA XYLANASE; ENDO BETA 1,4 XYLANASE I; ENDO BETA 1,4 XYLANASE II; ENDO BETA 1,4 XYLANASE III; ENDO BETA 1,4 XYLANASE IV; GLUCAN; MANNAN; OLIGOSACCHARIDE; RECOMBINANT ENZYME; RHODYMENAN; UNCLASSIFIED DRUG; XYLAN; XYLAN ENDO 1,3 BETA XYLOSIDASE; XYLOOLIGOSACCHARIDE; XYLOSE;

ARTICLE; CATALYSIS; DEGRADATION KINETICS; DNA ISOLATION; DNA SEQUENCE; ENDO BETA 1,4 XYLANASE IV GENE; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME ISOLATION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; ENZYME SYNTHESIS; FUNGAL GENE; GENE EXPRESSION; GENE ISOLATION; HYDROLYSIS; HYPOCREA JECORINA; NONHUMAN; NUCLEOTIDE SEQUENCE; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; STEREOCHEMISTRY;

BACTERIA (MICROORGANISMS); FUNGI; HYPOCREA JECORINA; PICHIA PASTORIS;

EID: 84872012985     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12069     Document Type: Article

References (71)

1. Aspinal GO, (1959) Structural chemistry of the hemicelluloses. Adv Carbohydr Chem 14, 429-468.
2. Howard BH, (1957) Hydrolysis of the soluble pentosans of wheat flour and Rhodymenia palmate by ruminal micro-organisms. Biochem J 67, 643-651.
3. Coutinho PM, &, Henrissat B,. Carbohydrate-active enzymes server at www.cazy.org.
4. Keen NT, Boyd C, &, Henrissat B, (1996) Cloning and characterization of a xylanase from corn strains of Erwinia chrysanthemi. Mol Plant-Microbe Interact 9, 651-657.
5. Suzuki T, Ibata K, Hatsu M, Takamizawa K, &, Kawai K, (1997) Cloning and expression of a 58-kDa xylanase VI gene (xynD) of Aeromonas caviae ME-1 in Escherichia coli which is not categorized as a family F or family G xylanase. J Ferment Bioeng 84, 86-89.
6. Hurlbert JC, &, Preston JF, (2001) Functional characterization of a novel xylanase from a corn strain of Erwinia chrysanthemi. J Bacteriol 183, 2093-2100.
7. St John FJ, Rice JD, &, Preston JF, (2006) Characterization of XynC from Bacillus subtilis subsp subtilis strain 168 and analysis of its role in depolymerization of glucuronoxylan. J Bacteriol 188, 8617-8626.
8. Vršanská M, Kolenová K, Puchart V, &, Biely P, (2007) Mode of action of glycoside hydrolase family 5 glucuronoxylan xylanohydrolase from Erwinia chrysanthemi. FEBS J 274, 1666-1677.
9. Valenzuela SV, Diaz P, &, Pastor FIJ, (2012) Modular glucuronoxylan-specific xylanase with a family CBM35 carbohydrate-binding module. Appl Environ Microbiol 78, 3923-3931.
10. Luo HY, Yang J, Li J, Shi PJ, Huang HQ, Bai YG, Fan YL, &, Yao B, (2010) Molecular cloning and characterization of the novel acidic xylanase XYLD from Bispora sp. MEY-1 that is homologous to family 30 glycosyl hydrolases. Appl Microbiol Biotechnol 86, 1829-1839.
11. St John FJ, Gonzales JM, &, Pozharski E, (2010) Consolidation of glycosyl hydrolase family 30: a dual domain 4/7 hydrolase family consisting of two structurally distinct groups. FEBS Lett 584, 4435-4441.
12. Collins T, Meuwis M-A, Stals I, Claeyssens M, Feller G, &, Gerday C, (2002) A novel family 8 xylanase, functional and physicochemical characterization. J Biol Chem 277, 35133-35139.
13. Fushinobu S, Hidaka M, Honsa Y, Wakagi T, Shoun H, &, Kitaoka M, (2005) Structural basis for the specificity of the reducing end xylose-releasing exo-oligoxylanase from Bacillus halodurans C-125. J Biol Chem 280, 17180-17186.
14. Honda Y, &, Kitaoka M, (2004) A family 8 glycoside hydrolase from Bacillus halodurans C-125 (BH2105) is a reducing end xylose-releasing exo-oligoxylanase. J Biol Chem 279, 55097-55103.
15. Correia MAS, Mazumder K, Brás JLA, Firbank SJ, Zhu Y, Lewis RJ, York WS, Fontes CMGA, &, Gilbert HJ, (2011) Structure and function of an arabinoxylan-specific xylanase. J Biol Chem 286, 22510-22520.
16. Biely P, (1985) Microbial xylanolytic systems. Trends Biotechnol 3, 286-290.
17. Tenkanen M, Luonteri E, &, Teleman A, (1996) Effect of side groups on the action of β-xylosidase from Trichoderma reesei against substituted xylo-oligosaccharides. FEBS Lett 399, 303-306.
18. Herrmann MC, Vršanská M, Jurickova M, Hirsch J, Biely P, &, Kubicek CP, (1997) The β- d -xylosidase of Trichoderma reesei is a multifunctional β- d -xylan xylohydrolase. Biochem J 321, 375-381.
19. Margolles-Clark E, Tenkanen M, Nakari-Setälä T, &, Penttilä M, (1996) Cloning of genes encoding α- l -arabinofuranosidase and β-xylosidase from Trichoderma reesei by expression in Saccharomyces cerevisiae. Appl Environ Microbiol 62, 3840-3846.
20. Ganju RK, Vithayathil PJ, &, Murthy SK, (1989) Purification and characterization of two xylanases from Chaetomium thermophile var. coprophile. Can J Microbiol 35, 836-842.
21. Kubata BK, Suzuki T, Horitsu H, Kawai K, &, Takamizawa K, (1994) Purification and characterization of Aeromonas caviae ME-1 xylanase V, which produce exlusively xylobiose from xylan. Appl Environ Microbiol 60, 531-535.
22. Kubata BK, Takamizawa K, Kawai K, Suzuki T, &, Horitsu H, (1995) Xylanase IV, an exoxylanase of Aeromonas caviae ME-1 which produces xylotetraose as the only low-molecular-weight oligosaccharide from xylan. Appl Environ Microbiol 61, 1666-1668.
23. Usui K, Ibata K, Suzuki T, &, Kawai K, (1999) XynX, a possible exo-xylanase of Aeromonas caviae ME-1 that produces exclusively xylobiose and xylotetraose from xylan. Biosci Biotechnol Biochem 63, 1346-1352.
24. Kubata BK, Suzuki T, Ito Y, Naito H, Kawai K, Takamizawa K, &, Horitsu H, (1997) Cloning and expression of xylanase I gene (xynA) of Aeromonas caviae ME-1 in Escherichia coli. J Ferment Bioeng 83, 292-295.
25. Biely P, &, Tenkanen M, (1998) Enzymology of hemicellulose degradation. In Trichoderma and Gliocladium, Vol. 2 (, Kubicek CP, &, Harrman GE, eds), pp. 25-47. Taylor & Francis Ltd, London.
26. Tenkanen M, Puls J, &, Poutanen K, (1992) Two major xylanases of Trichoderma reesei. Enzyme Microb Technol 14, 566-574.
27. Törrönen A, Mach R, Messner R, Gonzales R, Harkki A, Kalkkinen N, &, Kubicek K, (1992) The two major xylanases from Trichoderma reesei: characterization of both enzymes and genes. Biotechnology 10, 1461-1467.
28. Xu J, Takakuwa N, Nogawa M, Okada H, &, Morikawa Y, (1998) A third xylanase from Trichoderma reesei PC-3-7. Appl Microbiol Biotechnol 49, 718-724.
29. Biely P, Vršanská M, &, Claeyssens M, (1991) The endo-1,4-β-glucanase I from Trichoderma reesei. Action on β-1,4-oligomers and polymers derived from d-glucose and d-xylose. Eur J Biochem 200, 157-163.
30. Biely P, Vršanská M, Kremnický L, Tenkanen M, Poutanen K, &, Hayn M, (1993) Catalytic properties of endo-β-1,4- xylanases of Trichoderma reesei. In Proceedings of the TRICEL Symposium on Trichoderma reesei Cellulases and Other Hydrolases (, Suominen P, &, Reinikainen T, eds), pp. 125-135. Foundation for Biotechnical and Industrial Fermentation Research, Helsinki, Finland.
31. Tenkanen M, Siika-aho M, Saloheimo M, Vrsanska M, &, Biely P, (2003) A novel exo-acting xylanase XYN IV from Trichoderma reesei Rut C30. In Recent Advances in Enzymes in Grain Processing (, Courtin CM, Veraverbeke WS, &, Delcour JA, eds), pp. 41-46. ACCO, Leuven, Belgium.
32. Tenkanen M, &, Siika-aho M, (2000) An α-glucuronidase of Schizophyllum commune acting on polymeric xylan. J Biotechnol 75, 149-161.
33. Biely P, Mislovičová D, &, Toman R, (1985) Soluble chromogenic substrates for the assay and detection of endo-1,4-β-xylanases and endo-1,4-β-glucanases. Anal Biochem 144, 142-146.
34. Teleman A, Hausalo T, Tenkanen M, &, Vuorinen T, (1996) Identification of the acidic degradation products of hexenuronic acid and characterization of hexenuronic acid-substituted xylo-oligosaccharides by NMR spectroscopy. Carbohydr Res 280, 197-208.
35. De Vries RP, Poulsen CH, Madrid S, &, Visser J, (1998) aguA, the gene encoding an extracellular α-glucuronidase from Aspergillus tubingensis, is specifically induced on xylose and not on glucuronic acid. J Bacteriol 180, 243-249.
36. Biely P, Hirsch J, la Grange DC, van Zyl WH, &, Prior BA, (2000) A chromogenic substrate for a β-xylosidase-coupled assay of α-glucuronidase. Anal Biochem 286, 289-294.
37. Ryabova O, Vršanská M, Kaneko S, van Zyl WH, &, Biely P, (2009) Novel family of hemicellulolytic α-glucuronidase. FEBS Lett 583, 1457-1462.
38. Biely P, Vršanská M, Tenkanen M, &, Kluepfel D, (1997) Endo-β-1,4-xylanase families: differences in catalytic properties. J Biotechnol 57, 151-166.
39. Vršanská M, Gorbacheva IV, Krátký Z, &, Biely P, (1982) Reaction pathways of substrate degradation by an acidic endo-1,4-β-xylanase of Aspergillus niger. Biochim Biophys Acta 704, 114-122.
40. Biely P, Vršanská M, &, Krátký Z, (1981) Mechanism of substrate digestion by endo-1,4-β-xylanase of Cryptococcus albidus. Lysozyme-type of action. Eur J Biochem 119, 565-571.
41. Suganuma T, Matsuno R, Ohnishi M, &, Hiromi K, (1978) A study of the mechanism of action of Taka-amylase A on linear oligosaccharides by product analysis and computer simulation. J Biochem 84, 293-316.
42. Urbaníková Ľ, Vršanská M, Mørkeberg Krough KBR, Hoff T, &, Biely P, (2011) Structural basis for substrate recognition by Erwinia chrysanthemi GH30 glucuronoxylanase. FEBS J 278, 2105-2116.
43. St John FJ, Hurlbert JC, Rice JD, Preston JF, &, Pozharski E, (2011) Ligand bound structures of a glycosyl hydrolase family 30 glucuronoxylan xylanohydrolase. J Mol Biol 407, 92-109.
44. Margolles-Clark E, Ihnen M, &, Penttilä M, (1997) Expression patterns of ten hemicellulase genes of the filamentous fungus Trichoderma reesei on various carbon sources. J Biotechnol 57, 167-179.
45. Xu J, Nogawa M, Okada H, &, Morikawa Y, (2000) Regulation of xyn3 gene expression in Trichoderma reesei PC-3-7. Appl Microbiol Biotechnol 54, 370-375.
46. Kolenová K, Vršanská M, &, Biely P, (2005) Purification and characterization of two minor endo-β-1,4-xylanases of Schizophyllum commune. Enzyme Microb Technol 36, 903-910.
47. Robyt JF, &, French D, (1970) Action pattern of porcine pancreatic α-amylase in relation to the substrate binding site of the enzyme. J Biol Chem 245, 3917-3927.
48. Allen JD, &, Thoma JA, (1978) Multimolecular substrate reactions catalyzed by carbohydrates. Aspergillus oryzae α-amylase degradation of maltooligosaccharides. Biochemistry 17, 2338-2344.
49. Nishitani K, &, Nevins DJ, (1991) Glucuronoxylan xylanohydrolase. A unique xylanase with the requirement for appendant glucuronosyl residues. J Biol Chem 266, 6539-6543.
50. Gallardo O, Fernandez-Fernandez M, Valls C, Valenzuela SV, Roncero MB, Vidal T, Diaz P, &, Pastor FIJ, (2010) Characterization of a family GH5 xylanase with activity on neutral oligosaccharides and evaluation as a pulp bleaching aid. Appl Environ Microbiol 76, 6290-6294.
51. Larson SB, Day J, Barba de la Rosa AP, Keen NT, &, McPherson A, (2003) First crystallographic structure of a xylanase from glycoside hydrolase family 5: implication for catalysis. Biochemistry 42, 8411-8422.
52. Dung NV, Kamio Y, Abe N, Kaneko J, &, Izaki K, (1991) Purification and properties of β-1,4-xylanase from Aeromonas caviae W-61. Appl Environ Microbiol 57, 445-449.
53. Dung NV, Vetayasuporn S, Kamio Y, Abe N, Kaneko J, &, Izaki K, (1993) Purification and properties of β-1,4-xylanase 2 and 3 from Aeromonas caviae W-61. Biosci Biotechnol Biochem 57, 1708-1712.
54. Naran R, Black S, Decker SR, &, Azali P, (2009) Extraction and characterization of native heteroxylans from delignified corn stover and aspen. Cellulose 16, 661-675.
55. Van Dongen FEM, Van Eylen D, &, Kabel MAS, (2011) Characterization of substituents in xylans from corn cobs and stover. Carbohydr Polym 86, 722-731.
56. Chong SL, Nissila T, Ketola RA, Koutaniemi S, Derba-Maceluch M, Mellerowicz EJ, Tenkanen M, &, Tuomainen P, (2011) Feasibility of using atmospheric pressure matrix-assisted laser desorption/ionization with ion trap mass spectrometry in the analysis of acetylated xylooligosaccharides derived from hardwoods and Arabidopsis thaliana. Anal Bioanal Chem 401, 2995-3009.
57. Kováč P, (1979) Synthesis of a series of positionally isomeric methyl O-(α-and β- d -xylopyranosyl)-β- d -xylopyranoside. Collect Czech Chem Commun 45, 892-900.
58. Kováč P, (1980) Alternative synthesis of methylated sugars. XXII. Synthesis of methyl β-d-xylotrioside. Chemical Papers 34, 234-240.
59. Vršanská M, Nerinckx W, Claeyssens M, &, Biely P, (2008) An alternative approach for the synthesis of fluorogenic substrates of endo-β-(1→4)-xylanases and some applications. Carbohydr Res 343, 541-548.
60. Bailey MJ, Biely P, &, Poutanen K, (1992) Interlaboratory testing of methods for assay of xylanase activity. J Biotechnol 23, 257-270.
61. Poutanen K, &, Rättö M, (1988) Production of mannan-degrading enzymes. Biotechnol Lett 10, 661-664.
62. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
63. Lowry OH, Rosebrough NH, Parr AL, &, Randell RJ, (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193, 265-275.
64. Paleg LG, (1959) Citric acid interference in the estimation of reducing sugars with alkaline copper reagent. Anal Chem 31, 1902-1904.
65. Margolles-Clark E, Tenkanen M, Söderlund H, &, Penttilä M, (1996) Acetyl xylan esterase from Trichoderma reesei contains an active site serine and a cellulose binding domain. Eur J Biochem 237, 553-560.
66. Saloheimo A, Aro N, Ilmén M, &, Penttilä M, (2000) Isolation of the ace1 gene encoding a Cys2-His2 transcription factor involved in regulation of activity of the cellulase promoter cbh1 of Trichoderma reesei. J Biol Chem 275, 5817-5825.
67. Gietz D, St Jean A, Woods RA, &, Schiestl RH, (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20, 1425.
68. Sherman F, (1991) Getting started with yeast. Methods Enzymol 194, 3-21.
69. Penttilä M, Nevalainen H, Rättö M, Salminen E, &, Knowles JKC, (1987) A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei. Gene 61, 155-164.
70. Ilmén M, Saloheimo A, Onnela M-L, &, Penttilä M, (1997) Regulation of cellulase gene expression in the filamentous fungus Trichoderma reesei. Appl Environ Microbiol 63, 1298-1306.
71. Chirgwin JM, Przybyla RJ, McDonald RJ, &, Rutter WJ, (1979) Isolation of biological active ribonucleic acid from sources enriched in ribonucleases. Biochemistry 18, 5294-5299.