Barley α-amylase/subtilisin inhibitor: Structure, biophysics and protein engineering

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1696, Issue 2, 2004, Pages 157-164

  Nielsen, Peter K ^a   Bønsager, Birgit C ^a   Fukuda, Kenji ^a   Svensson, Birte ^a  

^a CARLSBERG LABORATORY   (Denmark)

Author keywords

Binding thermodynamics; Calcium; Interface structure; Kinetics; Mutational analysis; Protein protein interaction

Indexed keywords

AMYLASE INHIBITOR; CALCIUM ION; HYBRID PROTEIN; SERINE PROTEINASE INHIBITOR; SUBTILISIN INHIBITOR; TREFOIL PEPTIDE; UNCLASSIFIED DRUG;

BARLEY; BINDING KINETICS; CALORIMETRY; CRYSTALLOGRAPHY; DISSOCIATION CONSTANT; ENZYME KINETICS; ENZYME STRUCTURE; ISOTHERM; MUTATIONAL ANALYSIS; NONHUMAN; PLANT DEFENSE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; REVIEW; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS; THREE DIMENSIONAL IMAGING; TITRIMETRY;

HORDEUM VULGARE SUBSP. VULGARE; LOTUS;

EID: 1042289398     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2003.09.019     Document Type: Review

References (61)

1. Mundy J., Svendsen I., Hejgaard J. Barley α-amylase/subtilisin inhibitor: I. Isolation and characterization. Carlsberg Res. Commun. 48:1983;81-91.
2. Lecommandeur D., Lauriére C., Daussant J. α-Amylase inhibitor in barley seeds: localization and quantification. Plant Physiol. Biochem. 25:1987;711-715.
3. Leah R., Mundy J. The bifunctional α-amylase/subtilisin inhibitor of barley: nucleotide sequence and patterns of seed-specific expression. Plant Mol. Biol. 12:1989;673-682.
4. Jones R.L., Jacobsen J.V. Regulation of synthesis and transport of secreted proteins in cereal aleurone. Int. Rev. Cyt. 126:1991;49-88.
5. Yoshikawa M., Iwasaki T., Fujii M., Oogaki M. Isolation and some properties of a subtilisin inhibitor from barley. J. Biochem. 79:1976;765-773.
6. 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.
7. Svendsen I., Hejgaard J., Mundy J. Complete amino acid sequence of the α-amylase/subtilisin inhibitor from barley. Carlsberg Res. Commun. 51:1986;43-50.
8. Zemke K.J., Müller-Fahrnow A., Jany K.D., Pal G.P., Saenger W. The three-dimensional structure of the bifunctional proteinase K/α-amylase inhibitor from wheat (PK13) at 2.5 Å resolution. FEBS Lett. 279:1991;240-242.
9. Mundy J., Svendsen I., Hejgaard J. Characterization of a bifunctional wheat inhibitor of endogenous α-amylase and subtilisin. FEBS Lett. 167:1984;210-214.
10. Ohtsubo K., Richardson M. The amino acid sequence of a 20 kDa bifunctional subtilisin/α-amylase inhibitor from bran of rice (Oryza sativa L.) seeds. FEBS Lett. 309:1992;68-72.
11. 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.
12. 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 analyzed by surface plasmon resonance and isothermal titration calorimetry. Biochemistry. 42:2003;1478-1487.
13. Murzin A.G., Lesk A.M., Chothia C. β-Trefoil fold. Patterns of structure and sequence in the Kunitz inhibitors interleukins-1 β and 1 α and fibroblast growth factors. J. Mol. Biol. 223:1992;531-543.
14. Orengo C.A., Jones D.T., Thornton J.M. Protein superfamilies and domain superfolds. Nature. 372:1994;631-634.
15. Swindells M.B., Thornton J.M. A study of structural determinants in the interleukin-1 fold. Protein Eng. 6:1993;711-715.
16. Habazettl J., Gondol D., Wiltscheck R., Otlewski J., Schleicher M., Holak T.A. Structure of hisactophilin is similar to interleukin-1 β and fibroblast growth factor. Nature. 359:1992;855-858.
17. Zhu X., Komiya H., Chirino A., Faham S., Fox G.M., Arakawa T., Hsu B.T., Rees D.C. Three-dimensional structures of acidic and basic fibroblast growth factors. Science. 251:1991;90-93.
18. Rutenber E., Katzin B.J., Ernst S., Collins E.J., Mlsna D., Ready M.P., Robertus J.D. Crystallographic refinement of ricin to 2.5 Å Proteins. 10:1991;240-250.
19. Lacy D.B., Tepp W., Cohen A.C., DasGupta B.R., Stevens R.C. Crystal structure of botulinum neurotoxin type A and implications for toxicity. Nat. Struct. Biol. 5:1998;898-902.
20. Liu Y., Chirino A.J., Misulovin Z., Leteux C., Feizi T., Nussenzweig M.C., Bjorkman P.J. Crystal structure of the cysteine-rich domain of mannose receptor complexed with a sulfated carbohydrate ligand. J. Exp. Med. 191:2000;1105-1116.
21. Kaneko S., Kuno A., Fujimoto Z., Shimizu D., Machida S., Sato Y., Yura K., Go M., Mizuno H., Taira K., Kusakabe I., Hayashi K. An investigation of the nature and function of module 10 in a family F/10 xylanase FXYN of Streptomyces olivaceoviridis E-86 by module shuffling with the Cex of Cellulomonas fimi and by site-directed mutagenesis. FEBS Lett. 460:1999;61-66.
22. Jany K.D., Lederer G. Proteinase K-protein inhibitors from wheat. Biol. Chem. 366:1985;807-808.
23. Kim S.H., Hara S., Hase S., Ikenaka T., Toda H., Kitamura K., Kaizuma N. Comparative study on amino acid sequences of Kunitz-type soybean trypsin inhibitors Tia, Tib, and Tic. J. Biochem. 98:1985;435-448.
24. Bode W., Huber R. Natural protein proteinase inhibitors and their interaction with proteinases. Eur. J. Biochem. 204:1992;433-451.
25. Joubert F.J., Merrifield E.H., Dowdle E.B. The reactive sites of proteinase inhibitors from Erythrina seeds. Int. J. Biochem. 19:1987;601-606.
26. Onesti S., Brick P., Blow D.M. Crystal structure of a Kunitz-type trypsin inhibitor from Erythrina caffra seeds. J. Mol. Biol. 217:1991;153-176.
27. 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.
28. Franco O.L., Rigden D.J., Melo F.R., Grossi-De-Sà M.F. Plant α-amylase inhibitors and their interaction with insect α-amylases. Eur. J. Biochem. 269:2002;397-412.
29. Pal G.P., Kavounis C.A., Jany K.D., Tsernoglou D. The three-dimensional structure of the complex of proteinase K with its naturally occurring protein inhibitor, PKI3. FEBS Lett. 341:1994;167-170.
30. Coutinho P.M., Henrissat B. Gilbert H.J., Davies G.J., Henrissat B., Svensson B. Recent Advances in Carbohydrate Bioengineering. 1999;3-12 The Royal Society, Cambridge.
31. MacGregor E.A., Janecek S., Svensson B. Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochim. Biophys. Acta. 1546:2001;1-20.
32. MacGregor E.A., MacGregor A.W. Studies on cereal α-amylase using cloned DNA. Crit. Rev. Biochem. 5:1987;129-142.
33. Jacobsen J.V., Higgins T.J. Characterization of the α-amylases synthesized by aleurone layers of Himalaya barley in response to gibberellic-acid. Plant Physiol. 70:1982;1647-1653.
34. Bertoft E., Andtfolk C., Kulp S.E. Effect of pH, temperature, and calcium ions on barley malt α-amylase isozymes. J. Inst. Brew. 90:1984;298-302.
35. Rodenburg K.W., Juge N., Guo X.J., Sogaard M., Chaix J.C., 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.
36. Bush D.S., Sticher L., van Huystee R., Wagner D., Jones R.L. The calcium requirement for stability and enzymatic activity of two isoforms of barley aleurone α-amylase. J. Biol. Chem. 264:1989;19392-19398.
37. Weselake R.J., MacGregor A.W., Hill R.D. An endogeneous α-amylase inhibitor in barley kernels. Plant Physiol. 72:1983;809-812.
38. Kadziola A., Abe J., Svensson B., Haser R. Crystal and molecular structure of barley α-amylase. J. Mol. Biol. 239:1994;104-121.
39. Kadziola A., Sogaard 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.
40. Robert X., Haser R., Svensson B., Aghajari N. Comparison of crystal structures of barley α-amylase 1 and 2: implications for isozyme differences in stability and activity. Biologia. 57(Suppl. 11):2002;59-70.
41. Søgaard M., Kadziola A., Haser R., Svensson B. Site-directed mutagenesis of histidine 93, aspartic acid 180, glutamic acid 205, histidine 290, and aspartic acid 291 at the active site and tryptophan 279 at the raw starch binding site in barley α-amylase 1. J. Biol. Chem. 268:1993;22480-22484.
42. Juge N., Rodenburg K.W., Guo X.J., Chaix J.C., Svensson B. Isozyme hybrids within the protruding third loop domain of the barley α-amylase (α/β) 8-barrel. Implication for BASI sensitivity and substrate affinity. FEBS Lett. 363:1995;299-303.
43. Janin J., Chothia C. The structure of protein-protein recognition sites. J. Biol. Chem. 265:1990;16027-16030.
44. Stites W.E. Protein-protein interactions: interface structure, binding thermodynamics, and mutational analysis. Chem. Rev. 97:1997;1233-1250.
45. Wiegand G., Epp O., Huber R. The crystal structure of porcine pancreatic α-amylase in complex with the microbial inhibitor Tendamistat. J. Mol. Biol. 247:1995;99-110.
46. Bompard-Gilles C., Rousseau P., Rougé P., Payan F. Substrate mimicry in the active center of a mammalian α-amylase: structural analysis of an enzyme-inhibitor complex. Structure. 4:1996;1441-1452.
47. Strobl S., Maskos K., Wiegand G., Huber R., Gomis-Rüth F.X., Glockshuber R. A novel strategy for inhibition of α-amylases: yellow meal worm α-amylase in complex with the Ragi bifunctional inhibitor at 2.5 Å resolution. Structure. 6:1998;911-921.
48. Barbosa Pereira P.J., Lozanov V., Patthy A., Huber R., Bode W., Pongor S., Strobl S. Specific inhibition of insect α-amylases: yellow meal worm α-amylase in complex with the amaranth α-amylase inhibitor at 2.0 Å resolution. Struct. Fold. Des. 7:1999;1079-1088.
49. Lu S., Deng P., Liu X., Luo J., Han R., Gu X., Liang S., Wang X., Li F., Lozanov V., Patthy A., Pongor S. Solution structure of the major α-amylase inhibitor of the crop plant amaranth. J. Biol. Chem. 274:1999;20473-20478.
50. Søgaard M., Svensson B. Expression of cDNAs encoding barley α-amylase 1 and 2 in yeast and characterization of the secreted proteins. Gene. 94:1990;173-179.
51. Rodenburg K.W., Vallée F., Juge N., Aghajari N., Guo X., Haser R., Svensson B. Specific inhibition of barley α-amylase 2 by barley α-amylase/subtilisin inhibitor depends on charge interactions and can be conferred to isozyme 1 by mutation. Eur. J. Biochem. 267:2000;1019-1029.
52. Bønsager B.C., Prætorius-Ibba M., Nielsen P.K., Svensson B. Purification and characterization of the β-trefoil fold protein barley α-amylase/subtilisin inhibitor overexpressed in Escherichia coli. Protein Expr. Purif. 30:2003;185-193.
53. Wells J.A., de Vos A.M. Hematopoietic receptor complexes. Ann. Rev. Biochem. 65:1996;609-634.
54. Halayko A.J., Hill R.D., Svensson B. Characterization of the interaction of barley α-amylase II with an endogenous α-amylase inhibitor from barley kernels. Biochim. Biophys. Acta. 873:1986;92-101.
55. Selzer T., Albeck S., Schreiber G. Rational design of faster associating and tighter binding protein complexes. Nat. Struct. Biol. 7:2000;537-541.
56. 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.
57. Doyle M.L., Brigham-Burke M., Blackburn M.N., Brooks I.S., Smith T.M., Newman R., Reff M., Stafford W.F. III, Sweet R.W., Truneh A., Hensley P., O'Shannessy D.J. Measurement of protein interaction bioenergetics: application to structural variants of anti-sCD4 antibody. Methods Enzymol. 323:2000;207-230.
58. Koren R., Hammes G.G. A kinetic study of protein-protein interactions. Biochemistry. 15:1976;1165-1171.
59. Northrup S.H., Erickson H.P. Kinetics of protein-protein association explained by Brownian dynamics computer simulation. Proc. Natl. Acad. Sci. U. S. A. 89:1992;3338-3342.
60. Sidenius U., Olsen K., Svensson B., Christensen U. Stopped-flow kinetic studies of the reaction of barley α-amylase/subtilisin inhibitor and the high pI barley α-amylase. FEBS Lett. 361:1995;250-254.
61. Xie D., Freire E. Molecular basis of cooperativity in protein folding: V. Thermodynamic and structural conditions for the stabilization of compact denatured states. Proteins. 19:1994;291-301.