Barley α-amylase bound to its endogenous protein inhibitor BASI: Crystal structure of the complex at 1.9 Å resolution

Structure

Volumn 6, Issue 5, 1998, Pages 649-659

  Vallée, François ^a,c   Kadziola, Anders ^a,d   Bourne, Yves ^a   Juy, Michel ^a,e   Rodenburg, Kees W ^b,f   Svensson, Birte ^b   Haser, Richard ^a,e  

^a Centre National de la Recherche Scientifique   (France)

^b CARLSBERG LABORATORY   (Denmark)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^f AARHUS UNIVERSITY   (Denmark)

Author keywords

Barley; Bifunctional inhibitor; Protein protein interactions; X ray crystallography; amylase

Indexed keywords

EMBRYOPHYTA; GLYCINE MAX; HORDEUM; HORDEUM VULGARE SUBSP. VULGARE; LOTUS; SUIDAE;

EID: 0032524130     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(98)00066-5     Document Type: Article

References (63)

1. Mundy, J., Svendsen, I. & Hejgaard, J. (1983). Barley α-amylase/subtilisin inhibitor. Isolation and characterization. Carlsberg Res. Commun. 48, 81-90.
2. Svendsen, I., Hejgaard, J. & Mundy, J. (1986). Complete amino acid sequence of the α-amylase/subtilisin inhibitor from barley. Carlsberg Res. Commun. 51, 43-50.
3. Leah, R. & Mundy, J. (1989). The bifunctional α-amylase/subtilisin inhibitor of barley: nucleotide sequence and patterns of seed specific expression. Plant Mol. Biol. 12, 673-682.
4. Garcia-Olmedo, F., Salcedo, G., Sanchez-Monge, R., Gomez, L., Royo, J. & Carbonero, P. (1991). Plant proteinaceous inhibitors of proteinases and α-amylases. Oxford Survey of Plant Mol. Cell Biol. 4, 275-334.
5. Weselake, R.J., MacGregor, A.W. & Hill, R.D. (1985). Effect of endogenous barley α-amylase inhibitor on hydrolysis of starch under various conditions. J. Cereal Sci. 3, 249-259.
6. Abe, J., Sidenius, U. & Svensson, B. (1993). Arginine is essential for the α-amylase inhibitory activity of the α-amylase/subtilisin inhibitor (BASI) from barley seeds. Biochem. J. 293, 151-155.
7. Rodenburg, K.W., Varallyay, E., Svendsen, I. & Svensson, B. (1995). Arg-27, Arg-1 27 and Arg-155 in the β-trefoil protein barley α-amylase/subtilisin inhibitor are interface residues in the complex with barley α-amylase 2. Biochem. J. 309, 969-976.
8. Sidenius, U., Olsen, K., Svensson, B. & Christensen, U. (1995). Stopped-flow kinetic studies of the reaction of barley α-amylase/subtilisin inhibitor and the high pi barley α-amylase. FEBS Lett. 361, 250-254.
9. Swift, H.J., et al., & Wilkinson, A.J. (1991). Structure and molecular model refinement of Aspergillus oryzae (TAKA) α-amylase: an application of the simulated annealing method. Acta Cryst. B 47, 535-544.
10. Brzozowski, A.M. & Davies, G.J. (1997). Structure of the Aspergillus oryzae α-amylase complexed with the inhibitor acarbose at 2.0 Å resolution. Biochemistry 36, 10837-10845.
11. Qian, M., Haser, R. & Payan, F. (1993). Structure and molecular model refinement of pig pancreatic α-amylase at 2.1 A resolution. J. Mol. Biol. 231, 785-799.
12. Larson, S.B., Greenwood, A., Cascio, D., Day, J. & McPherson, A. (1994). Refined molecular structure of pig pancreatic α-amylase at 2.1 A resolution. J. Mol. Biol. 235, 1560-1564.
13. Kadziola, A., Abe, J., Svensson, B. & Haser, R. (1994). Crystal and molecular structure of barley α-amylase. J. Mol. Biol. 239, 104-121.
14. Kadziola, A., Søgaard, M., Svensson, B. & Haser, R. (1998). Molecular structure of a barley α-amylase-inhibitor complex: implications for starch binding and catalysis. J. Mol. Biol. 278, 205-217.
15. Brayer, G.D., Luo, Y. & Withers, S.G. (1995). The structure of human pancreatic α-amylase at 1.8 A resolution and comparisons with related enzymes. Protein Sci. 4, 1730-1742.
16. 2+ depleted Bacillus licheniformis α-amylase at 2.2 Å resolution. J. Mol. Biol. 246, 545-559.
17. Ramasubbu, N., Paloth, V., Luo, Y., Brayer, G.D. & Levine, M.J. (1996). Structure of human salivary α-amylase at 1.6 Å resolution: implications for its role in the oral activity. Acta Cryst. D 52, 435-446.
18. Wiegand, G., Epp, O. & Huber, R. (1995). The crystal structure of porcine pancreatic α-amylase in complex with the microbial inhibitor Tendamistat. J. Mol. Biol. 247, 99-110.
19. Bompard-Gilles, C., Rousseau, P., Rouge, P. & Payan, F. (1996). Substrate mimicry in the active center of a mammalian α-amylase: structural analysis of an enzyme-inhibitor complex. Structure 4, 1441-1452.
20. Aghajari, N., Feller, G., Gerday, Ch. & Haser, R. (1998). Crystal structures of the psychrophilic α-amylase from Alteromonas haloplanctis in its native form and complexed with an inhibitor. Protein Sci. 7, 564-572.
21. Davies, G.J. & Henrissat, B. (1995). Structures and mechanisms of glycosyl hydrolases. Structure 3, 853-859.
22. Reardon, D. & Farber, G.K. (1995). The structure and evolution of α/β barrel proteins. FASEB J. 9, 497-503.
23. Onesti, S. & Blow, D.M. (1991). Crystal structure of a Kunitz-type trypsin inhibitor from Erythrina caffra seeds. J. Mol. Biol. 217, 153-176.
24. Zemke, K.J., Müller-Farhnow, A., Jany, K.-D., Pal, G.P. & Saenger, W. (1991). The three dimensional structure of the bifunctional proteinase K/α-amylase inhibitor from wheat (PKI3) at 2.5 A resolution. FEBS Lett. 279, 240-242.
25. Pal, G.P., Kavounis, C.A., Jany, K.D. & Tsernoglou, D. (1994). The three-dimensional structure of the complex of proteinase K with its naturally occurring inhibitor PKI3. FEBS Lett. 341, 167-170.
26. Swindells, M.B. & Thornton, J.M. (1993). A study of structural determinants in the interleukin-1 fold. Protein Eng. 6, 711-715.
27. Habazetti, J., Gondol, D., Wiltscheck, R., Otlewski, J., Schleicher, M. & Holak, T.A. (1992). Structure of histolactophilin is similar to interleukin-1β and fibroblast growth factor. Nature 359, 855-858.
28. Zhu, X., et al., & Rees, D.C. (1991). Three-dimensional structure of acidic and basic fibroblast growth factor. Science 251, 90-93.
29. Rutenber, E. & Robertus, J.D. (1991). Structure of ricin B-chain at 2.5 Å resolution. Proteins 10, 260-269.
30. McLachlan, A.D. (1979). Three-fold structural pattern in the soybean trypsin inhibitor (Kunitz). J. Mol. Biol. 133, 557-563.
31. Murzin, A.G., Lesk, A.M. & Chothia, C. (1992). β-Trefoil fold patterns of structure and sequence in the Kunitz inhibitors-1β and 1α and fibroblast growth factors. J. Mol. Biol. 223, 531-543.
32. Murzin, A.G., Lesk, A.M. & Chothia, C. (1994). Principles determining the structure of β;-sheet barrels in proteins, (a) A theoretical analysis and (b) the observed structures. J. Mol. Biol. 236, 1369-1400.
33. Blow, D.M., Janin, J. & Sweet, R.M. (1974). Mode of action of soybean trypsin inhibitor (Kunitz) as a model for specific protein-protein interactions. Nature 249, 54-57.
34. Søgaard, M., Kadziola, A., Haser, R. & Svensson, B. (1993). Site-directed mutagenesis of histidine 93, aspartic acid 180, glutamic acid 205, histidine 290, and aspartic 291 at the active site and tryptophan 279 at the new starch binding site in barley α-amylase 1. J. Biol. Chem. 268, 22480-22484.
35. Bhat, T., et al., & Poljak, R.J. (1994). Bound water molecules and conformational stabilization help mediate an antigen-antibody association. Proc. Natl. Acad. Sci. USA 91, 1089-1093.
36. Buckle, M.B., Schreiber, G. & Fersht, A. (1994). Protein-protein recognition: crystal structural analysis of a barnase-barstar complex at 2.0 Å resolution. Biochemistry 33, 8878-8889.
37. Janin, J. & Chothia, C. (1990). Structure of protein-protein recognition sites. J. Biol. Chem. 265, 16027-16030.
38. Bode, W. & Huber, R. (1992). Natural protein proteinase inhibitors and their interaction with proteinases. Eur. J. Biochem. 204, 433-451.
39. Vértesy, L., Oeding, V., Bender, R., Zepf, K. & Nesemann, G. (1984). Tendamistat (Hoe 467), a tight-binding α-amylase inhibitor from Streptomyces tendae 4158. Eur. J. Biochem. 141, 505-512.
40. McPhalen, C.A., Strynadka, N.C.J. & James, M.N.G. (1991). Calcium-binding sites in proteins: a structural perspective. Adv. Protein Chem. 42, 77-144.
41. Rodenburg, K.W., Juge, N., Guo, X.-J., Søgaard, M., Chaix, J.-C. & Svensson, B. (1994). 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, 277-284.
42. Juge, N., et al., & Guo. X.-J. (1993). Comparison of barley malt α-amylase isozymes 1 and 2: construction of cDNA hybrids by in vivo recombination and their expression in yeast. Gene 130, 159-166.
43. 8 barrel. Implication for BASI sensitivity and substrate affinity. FEBS Lett. 363, 299-303.
44. Rodenburg, K.W., et al., & Svensson, B. (1995). Mutational analysis of residues determining the sensitivity of barley α-amylase 2 to the barley α-amylase/subtilisin inhibitor. Miami Bio/Technology Winter Symposia, Miami, Florida. Protein Eng. 8, 9.
45. Søgaard, M., Andersen, J.S., Roepstorff, P. & Svensson, B. (1993). Electrospray mass spectrometry characterization of post-translational modifications of barley α-amylase 1 produced in yeast. Bio/Technology 11, 1162-1165.
46. 8-barrel domain of barley α-amylase 1. J. Biol. Chem. 272, 22456-22463.
47. Chandler, P.M., Zwar, J.A., Jacobsen, J.V., Higgins, T.J.V. & Inglis, A.S. (1984). The effects of gibberellic acid and abscisic acid on α-amylase mRNA levels in barley aleurone layers studies using an α-amylase cDNA clone. Plant Mol. Biol. 3, 407-418.
48. Bush, D.S. & Jones, R.L. (1988). Cytoplasmic calcium and α-amylase secretion from barley aleurone protoplasts. Eur. J. Cell Biol. 46, 466-469.
49. Jones, R.L. & Jacobsen, J.V. (1991). Regulation of synthesis and transport of secreted proteins in cereal aleurone. Int. Rev. Cytol. 126, 49-87.
50. Jacobsen, J.V. & Beach, L.R. (1985). Control of transcription of α-amylase and RNA genes in barley aleurone protoplasts by gibberellin and abscisic acid. Nature 316, 275-277.
51. Lin, L.S. & Ho, T. (1986). Mode of action of abscisic acid in barley aleurone layers. Plant Physiol. 82, 289-297.
52. Giraudat, J., et al., & Vartanian, N. (1994). Current advances in abscisic acid action and signalling. Plant Mol. Biol. 94, 1557-1577.
53. Chandler, P.M. & Robertson, M. (1994). Gene expression regulated by abscisic acid and its relation to stress tolerance. Annu. Rev. Plant Physiol. 45, 113-141.
54. Roussel, A. & Cambillau, C. (1989). TURBO-FRODO. In Silicon Graphics Geometry Partners Directory. (Silicon Graphics eds.), pp. 77-78, Silicon Graphics Mountain View, CA.
55. Ajandouz, E.H., Abe, J., Svensson, B. & Marchis-Mouren, G. (1992). Barley malt α-amylase, purification, action pattern, and subsite mapping of isozyme 1 and two members of the isozyme 2 subfamily using p-nitrophenylated malto-oligosaccharide substrates. Biochim. Biophys. Acta 1159, 193-202.
56. Vallée, F., Kadziola, A., Bourne, Y., Abe, J., Svensson, B. & Haser, R. (1994). Characterization, crystallization and preliminary X-ray crystallographic analysis of the complex between barley α-amylase and the bifunctional α-amylase/subtilisin inhibitor from barley seeds. J. Mol. Biol. 236, 368-371.
57. Kabsch, W. (1988). Evaluation of single crystal X-ray diffraction data from a position-sensitive detector. J. Appl. Cryst. 21, 916-924.
58. Navaza, J. (1994). AMoRe: an automated package for molecular replacement. Acta Cryst. A 50, 157-163.
59. Brünger, AT. (1992). X-PLOR, Version 3.1. A system for X-ray Crystallography and NMR. Yale University Press, New Haven, CT.
60. CCP4. (1994). The CCP4 suite: programs for protein crystallography. Acta Cryst. D 50, 760-763.
61. Brünger, AT. (1992). Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475.
62. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check, the stereochemistry of protein structures. J. Appl. Cryst. 26, 283-291.
63. Nicholls, A., Bharadwaj, R. & Honig, B. (1993). GRASP: graphical representation and analysis of surface properties. Biophys. J. 64, A166.