Differences in conformational stability of barley alpha-amylase isozymes 1 and 2. Role of charged groups and isozyme 2 specific salt-bridges

Journal of Cereal Science

Volumn 38, Issue 3, 2003, Pages 289-300

  Jensen, M T ^a   Gottschalk, T E ^a   Svensson, B ^a  

^a CARLSBERG LABORATORY   (Denmark)

Author keywords

Barley (Hordeum vulgare) alpha amylase; Isozymes; Salt bridges; Site directed mutagenesis; Thermal stability; Urea unfolding

Indexed keywords

HORDEUM; HORDEUM VULGARE; HORDEUM VULGARE SUBSP. VULGARE;

EID: 0345448173     PISSN: 07335210     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0733-5210(03)00032-8     Document Type: Article

References (47)

1. 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 maltooligosaccharide substrates. Biochimica et Biophysica Acta 1159, 193-202.
2. André, G., Buléon, A., Haser, R., Tran, V., 1999. Amylose chain behavior in an interacting context III. Complete occupancy of the AMY2 barley α-amylase cleft and comparison with biochemical data. Biopolymers 50, 751-762.
3. Bertoft, E., Andtfolk, C., Kulp, S.-E., 1984. Effect of pH, temperature and calcium ions on barley malt α-amylase isoenzymes. Journal of the Institute of Brewing 90, 298-302.
4. Bethke, P.C., Lonsdale, I.E., Fath, A., Jones, R.L., 1999. Hormonally regulated programmed cell death in barley aleurone cells. The Plant Cell 11, 1033-1045.
5. Bush, D.S., Sticher, L., Huystee, R.B.V., Wagner, D., Jones, R.L., 1989. The calcium requirement for stability and enzymatic activity of two isoforms of barley aleurone α-amylase. Journal of Biological Chemistry 264, 19392-19398.
6. Dao-pin, S., Sauer, U., Nicholson, H., Matthews, B.W., 1991. Contributions of engineered surface salt bridges to the stability of T4 lysozyme determined by directed mutagenesis. Biochemistry 30, 7142-7153.
7. Declerck, N., Machius, M., Wiegand, G., Huber, R., Gaillardin, C., 2000. Probing structural determinants specifying high thermostability in Bacillus licheniformis alpha-amylase. Journal of Molecular Biology 301, 1041-1057.
8. Fincher, G.B., 1989. Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Plant Molecular Biology 40, 305-346.
9. Fox, J.D., Robyt, J.F., 1991. Miniaturizing of three carbohydrate analyses using a microsample plate reader. Analytical Biochemistry 195, 93-96.
10. Gibson, R.M., Svensson, B., 1987. Identification of tryptophanyl residues involved in binding of carbohydrate ligands to barley α-amylase 2. Carlsberg Research Communications 52, 373-379.
11. Hendsch, Z.S., Tidor, B., 1994. Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Science 3, 211-226.
12. Huang, N., Stebbins, G.L., Rodriguez, R.L., 1992. Classification and evolution of α-amylase genes in plants. Proceedings of the National Academy of Science, USA 89, 7526-7530.
13. Jones, R.L., Jacobsen, J.V., 1991. Regulation of synthesis and transport of secreted proteins in cereal aleurone. International Review of Cytology 126, 49-88.
14. 8-barrel implication for BASI sensitivity and substrate affinity. FEBS Letters 263, 299-303.
15. Juge, N., Andersen, J.S., Tull, D., Roepstorff, P., Svensson, B., 1996. Overexpression, purification, and characterization of recombinant barley α-amylases 1 and 2 secreted by the methylotrophic yeast Pichia pastoris. Protein Expression and Purification 8, 204-214.
16. Kadziola, A., Abe, J., Svensson, B., Haser, R., 1994. Crystal and molecular structure of barley α-amylase. Journal of Molecular Biology 239, 104-121.
17. Kadziola, A., Søgaard, M., Svensson, B., Haser, R., 1998. Molecular structure of a barley α-amylase-inhibitor complex: implications for starch binding and catalysis. Journal of Molecular Biology 278, 205-217.
18. Khursheed, B., Rogers, J.C., 1988. Barley α-amylase genes. Journal of Biological Chemistry 263, 18953-18960.
19. MacGregor, A.W., 1977. Isolation, purification and electrophoretic properties of an α-amylase from malted barley. Journal of the Institute of Brewing 83, 100-103.
20. MacGregor, A.W., 1978. Alpha-amylase 1 from malted barley-physical properties and action pattern on amylose. Cereal Chemistry 55, 754-765.
21. MacGregor, A.W., 1987. α-Amylase, limit dextrinase and α-glucosidase enzymes in barley and malt. Critical Reviews in Biotechnology 5, 117-128.
22. MacGregor, A.W., Ballance, D.L., 1980. Hydrolysis of large and small starch granules from normal and waxy barley cultivars by alpha-amylases from barley malt. Cereal Chemistry 57, 397-402.
23. MacGregor, A.W., Morgan, J.E., 1986. Hydrolysis of barley starch granules by alpha-amylases from barley malt. Cereal Foods World 31, 688-693.
24. MacGregor, E.A., MacGregor, A.W., Macri, L.J., Morgan, J.E., 1994. Models for the action of barley alpha-amylase isozymes on linear substrates. Carbohydrate Research 257, 249-268.
25. MacGregor, E.A., Janecek, S., Svensson, B., 2001. Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes. Biochimica et Biophysica Acta 1546, 1-20.
26. 8-barrel domain of barley α-amylase. Journal of Biological Chemistry 272, 22456-22463.
27. Matthews, P., Jacobsen, J., 2001 J. Transformation breeding of barley: towards malting quality improvement. Proceedings of the 10th Australian Barley Technical Symposium, Canberra, Australia, www. regional.org.au/au/abts/2001.
28. Mori, H., Bak-Jensen, K.S., Gottschalk, T.E., Motawia, M.S., Damager, I., Moller, B.L., Svensson, B., 2001. Modulation of activity and substrate binding modes by mutation of single and double subsites +1/ +2 and -5/ - 6 of barley alpha-amylase 1. European Journal of Biochemistry 268, 6545-6558.
29. Mundy, J., Svendsen, I., Hejgaard, J., 1983. Barley α-amylase/ subtilisin inhibitor. I. Isolation and charachterization. Carlsberg Research Communications 48, 81-90.
30. Nozaki, Y., 1972. The preparation of guanidine hydrochloride. Methods in Enzymology 26, 43-50.
31. Pace, C.N., 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods in Enzymology 131, 266-279.
32. Robert, X., Gottschalk, T.E., Haser, R., Svensson, B., Aghajari, N., 2002. Expression, purification and preliminary crystallographic studies of alpha-amylase isozyme 1 from barley seeds. Acta Crystallographica Section D Biological Crystallography 58, 683-686.
33. 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. European Journal of Biochemistry 221, 277-284.
34. Rodenburg, K.W., Vallee. F., Juge, N., Aghajari, N., Guo, X., Haser, R., Svensson, B., 2000. 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. European Journal of Biochemistry 267, 1019-1029.
35. Rogers, J.C., 1985. Two barley alpha-amylase gene families are regulated differently in aleurone cells. Journal of Biological Chemistry 260, 3731-3738.
36. Rogers, J.C., Milliman, C., 1983. Isolation and sequence analysis of a barley α-amylase cDNA clone. Journal of Biological Chemistry 258, 8169-8174.
37. Sambrook, J., Fritsch, E.F., Maniatis, T. (Eds.), 1989. Molecular Cloning: A Laboratory Manual, Cold Spring Habor Laboratory, Cold Spring Habor, NY.
38. Søgaard, M., Svensson, B., 1990. Expression of cDNAs encoding barley α-amylase 1 and 2 in yeast and characterization of the secreted proteins. Gene 94, 173-179.
39. Søgaard. M., Olsen, F.L., Svensson, B., 1991. C-terminal processing of barley α-amylase 1 in malt, aleurone protoplasts, and yeast. Proceedings of the National Academy of Science, USA 88, 8140-8144.
40. 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. Biotechnology 11, 1162-1165.
41. 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 acid 291 at the active site and tryptophan 279 at the raw starch binding site in barley α-amylase 1. Journal of Biological Chemistry 268, 22480-22484.
42. Silvanovich, M.P., Hill, R.D., 1976. Affinity chromatography of cereal α-amylase. Analytical Biochemistry 73, 430-433.
43. Vallée, F., Kadziola, A., Bourne, Y., Juy, M., Rodenburg, K.W., Svensson. B., Haser, R., 1998. Barley α-amylase bound to its endogenous protein inhibitor BASI: crystal structure of the complex at 1.9 Å resolution. Structure 6, 649-659.
44. Warren, J.R., Gordon, J.A., 1966. On the refractive indices of aqueous solutions of urea. Journal of Physical Chemistry 70, 297-300.
45. Weselake, R.J., MacGregor, A.W., Hill, R.D., 1983. An endogenous alpha amylase inhibitor in barley kernels. Plant Physiol. 72, 809-812.
46. Yamamoto, T. (Ed.), 1995. The Amylase Research Society of Japan, CRC Press, Boca Raton, FL.
47. Zoller, M.J., Smith, M., 1987. Oligonucleotide-directed mutagenesis: a simple method using two oligonucleotide primers and a single-stranded DNA template. Methods in Enzymology 154, 329-350.