Cross-inhibitory activity of cereal protein inhibitors against α-amylases and xylanases

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1650, Issue 1-2, 2003, Pages 136-144

  Sancho, Ana I ^a   Faulds, Craig B ^a   Svensson, Birte ^b   Bartolomé, Begoña ^c   Williamson, Gary ^a,e   Juge, Nathalie ^a,d  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^b CARLSBERG LABORATORY   (Denmark)

^c INSTITUTO DE FERMENTACIONES INDUSTRIALES CSIC   (Spain)

^d AIX MARSEILLE UNIVERSITY   (France)

^e NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

Barley amylase isozyme; Protein carbohydrate interaction; Proteinaceous inhibitor; Substrate dependent inhibitor binding; Xylanase

Indexed keywords

AMYLASE; AMYLASE INHIBITOR; CALCIUM CHLORIDE; ENZYME INHIBITOR; FUNGAL ENZYME; GLYCOSIDASE; OLIGOSACCHARIDE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; XYLAN ENDO 1,3 BETA XYLOSIDASE; XYLAN ENDO 1,4 BETA XYLOSIDASE; BARLEY ALPHA AMYLASE SUBTILISIN INHIBITOR; BARLEY ALPHA-AMYLASE-SUBTILISIN INHIBITOR; BOVINE SERUM ALBUMIN; ISOENZYME; SOYBEAN TRYPSIN INHIBITOR; XYLAN 1,4 BETA XYLOSIDASE;

ARTICLE; ASPERGILLUS NIGER; BARLEY; CALCULATION; CATALYSIS; CEREAL; COMPLEX FORMATION; ENZYME INHIBITION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; GEL ELECTROPHORESIS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; ANIMAL; CATTLE; DRUG ANTAGONISM; ENZYMOLOGY; ISOLATION AND PURIFICATION; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; WHEAT;

ASPERGILLUS; ASPERGILLUS NIGER; HORDEUM VULGARE SUBSP. VULGARE; TRITICUM AESTIVUM;

ALPHA-AMYLASE; ANIMALS; CALCIUM CHLORIDE; CATTLE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HORDEUM; ISOENZYMES; SERUM ALBUMIN, BOVINE; TRITICUM; TRYPSIN INHIBITOR, KUNITZ SOYBEAN; XYLAN ENDO-1,3-BETA-XYLOSIDASE; XYLOSIDASES;

EID: 0141976290     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1570-9639(03)00209-7     Document Type: Article

References (58)

1. Debyser W., Derdelinckx G., Delcour J.A. Arabinoxylan solubilization and inhibition of the barley malt xylanolytic system by wheat during mashing with wheat wholemeal adjunts: evidence for a new class of enzyme inhibitors in wheat. J. Am. Soc. Brew. Chem. 55:1997;153-156.
2. Rouau X., Surget A. Evidence for the presence of a pentosanase inhibitor in wheat flours. J. Cereal Sci. 28:1998;63-70.
3. McLauchlan W.R., Garcia-Conesa M.T., Williamson G., Roza M., Ravestein P. A novel class of protein from wheat which inhibits xylanases. Biochem. J. 338:1999;441-446.
4. Flatman R., McLauchlan W.R., Juge N., Furniss C.S., Berrin J.G., Hughes R.K., Manzanares P., Ladbury J.E., O'Brien R., Williamson G. Interactions defining the specificity between fungal xylanases and the wheat proteinaceous inhibitor, XIP-I. Biochem. J. 365:2002;773-781.
5. Eliott G.O., McLauchlan W.R., Williamson G., Kroon P.A. A wheat xylanase inhibitor protein (XIP-I) accumulates in the grain and has homologues in other cereals. J. Cereal Sci. 37:2003;187-194.
6. McLauchlan W.R., Flatman R.H., Sancho A.I., Kakuta J., Faulds C.B., Eliott G.O., Kroon P.A., Furniss C.S.M., Juge N., Ravestein P., Williamson G. Xylanase inhibitors from cereals: implications for baking, brewing and plant technology. Simoinen T., Tenkanen M. The Second European Symposium on Enzymes in Grain Processing. 2000;55-61 VTT Technical Research Centre, Finland.
7. Debyser W., Peumans W.J., van Damme E.J.M., Delcour J.A. Triticum aestivum xylanase inhibitor (TAXI), a new class of enzyme inhibitor affecting breadmaking performance. J. Cereal Sci. 30:1999;39-43.
8. Gebruers K., Debyser W., Goesaert H., van Damme J., Delcour J.A. Triticum aestivum L. endoxylanase inhibitor (TAXI) consists of two inhibitors, TAXI I and TAXI II, with different specificities. Biochem. J. 353:2001;239-244.
9. Goesaert H., Gebruers K., Courtin C.M., Proost P., van Damme J., Delcour J.A. A family of 'TAXI'-like endoxylanase inhibitors in rye. J. Cereal Sci. 36:2002;177-185.
10. Goesaert H., Debyser W., Gebruers K., Proost P., van Damme J., Delcour J.A. Purification and partial characterization of an endoxylanase inhibitor from barley. Cereal Chem. 78:2001;453-457.
11. Franco O.L., Rigden D.J., Melo F.R., Grossi-De-Sa M.F. Plant alpha-amylase inhibitors and their interaction with insect alpha-amylases. Eur. J. Biochem. 269:2002;397-412.
12. Mundy J., Svendsen I., Hejgaard J. Barley α-amylase/subtilisin inhibitor, isolation and characterization. Carlsberg Res. Commun. 48:1983;81-90.
13. Weselake R.J., MacGregor A.W., Hill R.D. An endogenous α-amylase inhibitor in barley kernels. Plant Physiol. 72:1983;809-812.
14. Warchalewski J.R. Isolation and purification of native alpha-amylase inhibitors from malted winter wheat. Bull. Pol. Acad. Sci., Biol. 25:1978;731-735.
15. Mundy J., Hejgaard J., Svendsen I. Characterization of a bifunctional wheat inhibitor of endogenous α-amylase and subtilisin. FEBS Lett. 167:1984;210-214.
16. Yamagata H., Kunimatsu K., Kamasaka H., Kuramoto T., Iwasaki T. Rice bifunctional α-amylase/subtilisin inhibitor: characterization, localization, and changes in developing and germinating seeds. Biosci. Biotechnol. Biochem. 62:1998;978-985.
17. Vallée F., Kadziola A., Bourne Y., Juy M., Rodenburg K.W., Svensson B., Haser R. Barley α-amylase bound to its endogenous protein inhibitor BASI: crystal structure of the complex at 1.9 Å resolution. Structure. 6:1998;649-659.
18. Sidenius U., Olsen K., Svensson B., Christensen U. Stopped-flow kinetic studies of the reaction of barley alpha-amylase/subtilisn inhibitor and the high pI barley alpha-amylase. FEBS Lett. 361:1995;250-254.
19. Abe J., Sidenius U., Svensson B. Arginine is essential for the α-amylase inhibitory activity of the α-amylase/subtilisin inhibitor (BASI) from barley seeds. Biochem. J. 293:1993;151-155.
20. Pekkarinen A.I., Jones B.L. Purification and identification of barley (Hordeum vulgare L.) proteins that inhibit the alkaline serine proteinases of Fusarium culmorum. J. Agric. Food Chem. 51:2003;1710-1717.
21. Munck L., Mundy J., Vaag P. Characterization of enzyme inhibitors in barley and their tentative role in malting and brewing. J. Am. Soc. Brew. Chem. 43:1985;35-38.
22. Elliott G.O., Hughes R.K., Juge N., Kroon P.A., Williamsom G. Functional identification of the cDNA coding for a wheat endo-1,4-β-D xylanase inhibitor. FEBS Lett. 519:2002;66-70.
23. Hessing J.G., van Rotterdam C., Verbakel J.M., Roza M., Maat J., van Gorcom R.F., van den Hondel C.A. Isolation and characterization of a 1,4-beta-endoxylanase gene of A. awamori. Curr. Genet. 26:1994;228-232.
24. Berrin J.G., Williamson G., Puigserver A., Chaix J.C., McLauchlan W.R., Juge N. High-level production of recombinant fungal endo-β-1,4-xylanase in the methylotrophic yeast Pichia pastoris. Protein Expr. Purif. 19:2000;179-187.
25. Ajandouz E., Abe J., Svensson B., Marchis-Mouren G. Barley malt α-amylase. Purification, action pattern and subsite mapping of isozyme 1 and two members of the isozyme 2 subfamily using p-nitrophenylated maltooligosaccharide substrates. Biochim. Biophys. Acta. 1159:1992;193-202.
26. Juge N., Svensson B., Williamson G. Secretion, purification, and characterization of barley α-amylase produced by heterologous gene expression in A. niger. Appl. Microbiol. Biotechnol. 49:1998;385-392.
27. Miller G.L. Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal. Chem. 31:1959;426-428.
28. Rodenburg K.W., Juge N., Guo X., Søgaard M., Chaix J., Svensson B. Domain B protruding at the third β strand of the α/β barrel in barley α-amylase confers distinct isozyme-specific properties. Eur. J. Biochem. 221:1994;277-284.
29. Leatherbarrow R.J. GraFit Version 4.0. 1998;Erithacus Software, Staines, UK.
30. Gibson R.M., Svensson B. Chemical modification of barley malt α-amylase 2: involvement of tryptophan and tyrosine residues in enzyme activity. Carlsberg Res. Commun. 51:1986;295-308.
31. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
32. Stone K.L., Williams K.R. Enzymatic digestion of proteins and HPLC peptide isolation. Matsudaira P. A Practical Guide to Protein and Peptide Purification for Microsequencing. 1993;55 Academic Press, New York.
33. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
34. Svendsen I.A., Hejgaard J., Mundy J. Complete amino acid sequence of the α-amylase/subtilisin inhibitor from barley. Carlsberg Res. Commun. 51:1986;43-50.
35. Altshul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215:1990;403-410.
36. Weselake R.J., MacGregor A.W., Hill R.D., Duckworth H.W. Purification and characteristics of an endogenous α-amylase inhibitor from barley kernels. Plant Physiol. 73:1983;1008-1012.
37. Nielsen P.K., Bønsager B.C., Berland C.R., Sigurskjold B.W., Svensson B. Kinetics and energetics of the binding between barley α-amylase/subtilisin inhibitor and barley α-amylase 2 analysed by surface plasmon resonance and isothermal titration calorimetry. Biochemistry. 42:2003;1478-1487.
38. Bush D.S., Sticher L., van Huystee R., Wagner D., Jones R.L. The calcium requirement for stability and enzymatic activity of the two isoform of barley aleurone α-amylases. J. Biol. Chem. 264:1989;19392-19398.
39. MacGregor A.W., Ballance D. Quantitative determination of α-amylase enzymes in germinated barley after separation by isoelectrofocusing. J. Inst. Brew. 86:1980;131-133.
40. Rodenburg K.W., Varallyay E., Svendsen I., Svensson B. Arg-27, Arg-127 and Arg-155 in the beta-trefoil protein barley alpha-amylase/subtilisin inhibitor are interface residues in the complex with barley alpha-amylase 2. Biochem. J. 309:1995;969-976.
41. 8-barrel, implication for BASI sensitivity and substrate affinity. FEBS Lett. 363:1995;299-303.
42. Rodenburg K.W., Vallée F., Juge N., Aghajari N., Guo X., Haser R., Svensson B. Specific inhibition of barley alpha-amylase 2 by barley alpha-amylase/subtilisin inhibitor depends on charge interactions and can be conferred to isozyme 1 by mutation. Eur. J. Biochem. 267:2000;1019-1029.
43. Ohtsubo K., Richardson M. The amino acid sequence of a 20 kDa bifunctional subtilisin/alpha-amylase inhibitor from bran of rice (Oryza sativa L.) seeds. FEBS Lett. 309:1992;68-72.
44. Nagasaki H., Yamamoto K., Shomura A., Koga-Ban Y., Takasuga A., Yano M., Minobe Y., Sasaki T. Rice class III chitinase homologues isolated by random cloning of rice cDNAs. DNA Res. 4:1997;379-385.
45. Bokma E., Spiering M., Chow K.S., Mulder P., Subroto T., Beintema J.J. Determination of cDNA and genomic sequences of hevamine, a chitinase from the rubber tree Hevea brasiliensi. Plant Physiol. Biochem. 39:2001;367-376.
46. Schlesier B., Nong V.H., Horstmann C., Hennig M. Sequence analysis of concanavalin B from Canavalia ensiformis reveals homology to chitinases. J. Plant Physiol. 147:1995;665-674.
47. Payan F., Flatman R., Porciero S., Williamson G., Juge N., Roussel A. Structural analysis of XIP-I, a xylanase proteinaceous inhibitor from wheat. Biochem. J. 372:2003;1-7.
48. Kadziola A., Abe J., Svensson B., Haser R. Crystal and molecular structure of barley alpha-amylase. J. Mol. Biol. 239:1994;104-121.
49. Kadziola A., Søgaard M., Svensson B., Haser R. Molecular structure of a barley α-amylase-inhibitor complex: implications for starch binding and catalysis. J. Mol. Biol. 278:1998;205-217.
50. Krengle U., Dijkstra B.W. Three-dimensional structure of endo-1,4-beta-xylanase I from Aspergillus niger: molecular basis for its low pH optimum. J. Mol. Biol. 263:1996;70-78.
51. Sapag A., Wouters J., Lambert C., de Ioannes P., Eyzaguirre J., Depiereux E. The endoxylanases from family 11: computer analysis of protein sequences reveals important structural and phylogenetic relationships. J. Biotechnol. 95:2002;109-131.
52. Robert X., Haser R., Svensson B., Agharjari N. Comparison of crystal structures of barley α-amylase isozymes 1 and 2: implications for isozyme differences in stability and activity. Biologia, Bratislava. 57(Suppl. 11):2002;59-70.
53. Di Pietro A., Roncero M.I.G. Endopolygalacturonase from Fusarium oxysporum sp. lycopersici: purification, characterization, and production during infection of tomato plants. Phytophatology. 86:1996;1324-1330.
54. Machinandiarena M.F., Olivieri F.P., Daleo G.R., Oliva C.R. Isolation and characterization of a polygalacturonase inhibiting protein from potato leaves. Accumulation in response to salicylic acid, wounding and infection. Plant Physiol. Biochem. 39:2001;129-136.
55. James J.T., Dubery I.A. Inhibition of polygalacturonase from Verticillium dahliae by a polygalacturonase inhibiting protein from cotton. Phytochemistry. 57:2001;149-156.
56. Stotz H.U., Contos J.J.A., Powell A.L.T., Bennett A.B., Labavitch J.M. Structure and expression of an inhibitor of fungal polygalacturonases from tomato. Plant Mol. Biol. 25:1994;607-617.
57. T. Palmer, Understanding Enzymes, 4th ed. Prentice Hall, Ellis Horwood, 1995, pp. 148-151, 243-245, 262-263.
58. Alam N., Gourinath S., Dey S., Srinivasan A., Singh T.P. Substrate-inhibitor interactions in the kinetics of α-amylase inhibition by ragi α-amylase/trypsin inhibitor (RATI) and its various N-terminal fragments. Biochemistry. 40:2001;4229-4233.