Journal of Protein Chemistry

, Volume 12, Issue 6, pp 791–805 | Cite as

Starch- and glycogen-debranching and branching enzymes: Prediction of structural features of the catalytic (β/α)8-barrel domain and evolutionary relationship to other amylolytic enzymes

  • Hans M. Jespersen
  • E. Ann MacGregor
  • Bernard Henrissat
  • Michael R. Sierks
  • Birte Svensson
Article

Abstract

Sequence alignment and structure prediction are used to locate catalytic α-amylase-type (β/α)8-barrel domains and the positions of their β-strands and α-helices in isoamylase, pullulanase, neopullulanase, α-amylase-pullulanase, dextran glucosidase, branching enzyme, and glycogen branching enzymes—all enzymes involved in hydrolysis or synthesis of α-1,6-glucosidic linkages in starch and related polysaccharides. This has allowed identification of the transferase active site of the glycogen debranching enzyme and the locations of β ⇑ α loops making up the active sites of all enzymes studied. Activity and specificity of the enzymes are discussed in terms of conserved amino acid residues and loop variations. An evolutionary distance tree of 47 amylolytic and related enzymes is built on 37 residues representing the four best conserved β-strands of the barrel. It exhibits clusters of enzymes close in specificity, with the branching and glycogen debranching enzymes being the most distantly related.

Key words

α-1,6-Glucosidic bond metabolism amylolytic enzymes structure prediction sequence comparison evolutionary tree 

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References

  1. Aleshin, A., Golubev, A., Firsov, L. M., and Honzatko, R. B. (1992).J. Biol. Chem. 267 19,291–19,298.Google Scholar
  2. Amemura, A., Chakraborty, R., Fujita, M., Noumi, T., and Futai, M. (1988).J. Biol. Chem. 263 9271–9275.Google Scholar
  3. Argos, P., Mahoney, W. C., Hermodson, M. A., and Hanei, M. (1981).J. Biol. Chem. 256 4357–4361.Google Scholar
  4. Baba, T., Kimura, K., Mizuno, K., Etoh, H., Ishida, Y., Shida, O. and Arai, Y. (1991).Biochem. Biophys. Res. Commun. 181 87–94.Google Scholar
  5. Baecker, P. A., Greenberg, E., and Preiss, J. (1986).J. Biol. Chem. 261 8738–8743.Google Scholar
  6. Bahl, H., Burchhardt, G., Spreinat, A., Haeckel, K., Wienecke, A., Schmidt, B., and Antranikian, G. (1991).Appl. Environ. Microbiol. 57 1554–1559.Google Scholar
  7. Boel, E., Brady, L., Brzozowski, A. M., Derewenda, Z., Dodson, G. G., Jensen, V. J., Petersen, S. B., Swift, H., Thim, L., and Woldike, H. F. (1990).Biochemistry 29 6244–6249.Google Scholar
  8. Bränden, C.-I. (1991).Curr. Opin. Struct. Biol. 1 978–983.Google Scholar
  9. Brown, B. I., and Brown, D. H. (1966a).Methods Enzymol. 8 395–403.Google Scholar
  10. Brown, D. H., and Brown, B. I. (1966b).Methods Enzymol. 8 515–524.Google Scholar
  11. Buisson, G., Duée, E., Haser, R., and Payan, F. (1987).EMBO J. 6 3909–3916.Google Scholar
  12. Cid, H., Bunster, M., Arriagada, E., and Campos, M. (1982).FEBS Lett. 150 247–254.Google Scholar
  13. Dayhoff, M. O., Baker, W. C., and Hunt, L. T. (1983).Methods Enzymol. 91 542–545.Google Scholar
  14. Farber, G. K., and Petsko, G. A. (1990).Trends Biochem. Sci. 15 228–234.Google Scholar
  15. Gaboriaud, C., Bissery, V., Benchetrit, T., and Mornon, J. P. (1987).FEBS Lett. 224 149–155.Google Scholar
  16. Garnier, J., Osguthorpe, D. I., and Robson, B. (1978).J. Mol. Biol. 120 97–120.Google Scholar
  17. Henrissat, B. (1991).Biochem. J. 280 309–316.Google Scholar
  18. Holm. L., Koivula, A. K., Lehtovaara, P. M., Hemminki, A., and Knowles, J. K. C. (1990).Protein Eng. 3 181–191.Google Scholar
  19. Hong, S. H., and Marmur, J. (1986).Gene 41 75–84.Google Scholar
  20. Igarashi, K., Ara, K., Saeki, K., Ozaki, K., Kawai, S., and Ito, S. (1992).Biosci. Biotech. Biochem. 56 514–516.Google Scholar
  21. Imanaka, T., and Kuriki, T. (1989).J. Bacteriol. 171 369–374.Google Scholar
  22. Ishikawa, K., Matsui, I., Honda, K., and Nakatani, H. (1992).Biochem. Biophys. Res. Commun. 183 286–291.Google Scholar
  23. Janacek, S. (1992).Biochem. J. 288 1069–1070.Google Scholar
  24. Jespersen, H. M., MacGregor, E. A., Sierks, M. R., and Svensson, B. (1991).Biochem. J. 280 51–55.Google Scholar
  25. Kainuma, K., Kobayashi, S., and Harada, T. (1978).Carbohydr. Res. 61 345–357.Google Scholar
  26. Katsuragi, N., Takizawa, N., and Murooka, Y. (1987).J. Bacteriol. 169 2301–2306.Google Scholar
  27. Kiel, J. A. K. W., Boels, J. M., Beldman, G., and Venema, G. (1990).Gene 89 77–84.Google Scholar
  28. Kiel, J. A. K. W., Boels, J. M., Beldman, G., and Venema, G. (1991).Mol. Gen. Genet. 230 136–144.Google Scholar
  29. Kim, I.-C., Cha, J.-H., Kim, J.-R., Jang, S.-Y., Seo, B.-C., Cheong, T.-K., Lee, D. S., Choi, Y. D., and Park, K.-H. (1992).J. Biol. Chem. 267 22,108–22,114.Google Scholar
  30. Klein, C., and Schulz, G. E. (1991).J. Mol. Biol. 217 737–750.Google Scholar
  31. Klein, C., Hollender, J., Bender, H., and Schulz, G. E. (1992).Biochemistry 31 8740–8746.Google Scholar
  32. Kossmann, J., Visser, R. G. F., Müller-Röber, B., Willmitzer, L., and Sonnewald, U. (1991).Mol. Gen. Genet. 230 39–44.Google Scholar
  33. Kubota, M., Matsuura, Y., Sakai, S., and Katsube, Y. (1990).Protein Eng. 3 328–329.Google Scholar
  34. Kuriki, T., and Imanaka, T. (1989).J. Gen. Microbiol. 135 1521–1528.Google Scholar
  35. Kuriki, T., Park, J.-H., and Imanaka, T. (1990).J. Ferment. Bioeng. 69 204–210.Google Scholar
  36. Kuriki, T., Takata, H., Okada, S., and Imanaka, T. (1991).J. Bacteriol. 173 6147–6152.Google Scholar
  37. Kusunoki, M., and Matsuura, Y. (1988). InHandbook of Amylases and Related Enzymes (The Amylase Research Society of Japan, eds.), Pergamon Press, New York, pp. 72–75.Google Scholar
  38. Lemesle-Verloot, L., Henrissat, B., Gaboriaud, C., Bissery, V., Morgat, A., and Mornon, J. P. (1990).Biochimie 72 555–574.Google Scholar
  39. Lesk, A. M., Bränden, C. I., and Chothia, C. (1989).Proteins 5 139–148.Google Scholar
  40. Levin, J. M., Robson, B., and Garnier, J. (1986).FEBS Lett. 205 303–308.Google Scholar
  41. Lipman, D. J., Altshul, S. F., and Kecicioglu, J. D. (1989),Proc. Natl. Acad. Sci. USA 86 4412–4415.Google Scholar
  42. Liu, W., Madsen, N. B., Braun, C., and Withers, S. G. (1991).Biochemistry 30 1419–1424.Google Scholar
  43. Lowe, D. M., Fersht, A. R., and Wilkinson, A. J. (1985).Biochemistry 24 5106–5109.Google Scholar
  44. MacGregor, E. A. (1988).J. Prot. Chem. 7 399–415.Google Scholar
  45. MacGregor, E. A., and Svensson, B. (1989).Biochem. J. 259 145–152.Google Scholar
  46. Mathupala, S., Saha, B. C., and Zeikus, J. G. (1990).Biochem. Biophys. Res. Commun. 166 126–132.Google Scholar
  47. Matsui, I., Ishikawa, K., Miyairi, S., Fukui, S., and Honda, K. (1991).Biochim. Biophys. Acta. 1077 416–419.Google Scholar
  48. Matsui, I., Ishikawa, K., Miyairi, S., Fukui, S., and Honda, K. (1992a).Biochemistry 31 5232–5236.Google Scholar
  49. Matsui, I., Ishikawa, K., Miyairi, S., Fukui, S., and Honda, K. (1992b).FEBS Lett. 310 216–218.Google Scholar
  50. Matsuura, Y., Kusunoki, M., Harada, W., and Kakudo, M. (1984).J. Biochem. (Tokyo)95 697–702.Google Scholar
  51. Melasniemi, H. (1987).Biochem. J. 246 193–197.Google Scholar
  52. Melasniemi, H., Paloheimo, M., and Hemio, L. (1990).J. Gen. Microbiol. 136 447–454.Google Scholar
  53. Mikami, B., Sato, M., Shibata, T., Hirose, M., Aibara, S., Katsube, Y., and Morita, Y. (1992).J. Biochem. 112 541–546.Google Scholar
  54. Mizuno, K., Kimura, K., Arai, Y., Kawasaki, T., Shimada, H., and Baba, T. (1992).J. Biochem. (Tokyo)112 643–651.Google Scholar
  55. Nagashima, T., Toda, S., Kitamoto, K., Gomi, K., Kumagai, C., and Toda, H. (1992).Biosci. Biotech. Biochem. 56 207–210.Google Scholar
  56. Nakamura, A., Haga, K., Ogawa, S., Kuwano, K., Kimura, K., and Yamane, K. (1992).FEBS Lett. 296 37–40.Google Scholar
  57. Nakamura, Y., and Yamanouchi, H. (1992).Plant Physiol. 99 1265–1266.Google Scholar
  58. Nishizawa, M., Ozawa, F., and Hishinuma, F. (1987).DNA 6 255–265.Google Scholar
  59. Nomenclature Committee of the International Union of Biochemistry (1984).Enzyme Nomenclature Academic Press, New York, pp. 318–319.Google Scholar
  60. Ogiwara, A., Uchiyama, I., Seto, Y., and Kanehisa, H. (1992).Protein Eng. 5 479–488.Google Scholar
  61. Pickett, S. D., Saqi, M. A. S., and Steinberg, M. J. E. (1992).J. Mol. Biol. 228 170–187.Google Scholar
  62. Plant, A. R., Clemens, R. M., Morgan, H. W., and Daniel, R. M. (1987).Biochem. J. 246 537–541.Google Scholar
  63. Podkovyrov, S. M., and Zeikus, J. G. (1992).J. Bacteriol. 174 5400–5405.Google Scholar
  64. Podkovyrov, S. M., Burdette, D., and Zeikus, J. G. (1993).FEBS Lett. 317 259–262.Google Scholar
  65. Raimbaud, E., Buléon, A., Pérez, S., and Henrissat, B. (1989).Int. J. Biol. Macromol. 11 217–225.Google Scholar
  66. Rossmann, M. G., Moras, D., and Olsen, K. W. (1974).Nature (London)250 194–199.Google Scholar
  67. Rumbak, E., Rawlings, D. E., Lindsey, G. G., and Woods, D. R. (1991).J. Bacteriol. 173 6732–6741.Google Scholar
  68. Russell, R. R. B., and Ferretti, J. J. (1990).J. Gen. Microbiol. 136 803–810.Google Scholar
  69. Saitou, N., and Nei, M. (1987).Mol. Biol. Evol. 4 406–425.Google Scholar
  70. Sashihara, N., Nakamura, N., and Horikoshi, K. (1993).Stärke 45 144–150.Google Scholar
  71. Shirokizawa, O., Akiba, T., and Horikoshi, K. (1990).FEMS Microbiol. Lett. 70 131–135.Google Scholar
  72. Søgaard, M., Kadziola, A., Haser, R., and Svensson, B. (1993).Miami Short Reports Proceedings 3 51.Google Scholar
  73. Suzuki, Y., and Imai, T. (1985).Appl. Microbiol. Biotechnol. 21 20–26.Google Scholar
  74. Svensson, B. (1988).FEBS Lett. 230 72–76.Google Scholar
  75. Svensson, B., Jespersen, H. M., Sierks, M. R., and MacGregor, E. A. (1989).Biochem. J. 264 309–311.Google Scholar
  76. Svensson, B., and Søgaard, M. (1993).J. Biotechnol. 29 1–37.Google Scholar
  77. Takase, K., Matsumoto, T., Mizuno, H., and Yamane, K. (1992).Biochim. Biophys. Acta 1120 281–288.Google Scholar
  78. Takata, H., Kuriki, T., Odada, S., Takesada, Y., Iizuka, M., Minamiura, N., and Imanaka, T. (1992).J. Biol. Chem. 267 18,447–18,452.Google Scholar
  79. Thon, V. J., Vigneron-Lesens, C., Marianne-Pepin, T., Montreuil, J., Decq, A., Rachez, C., Ball, S. G., and Cannon, J. F. (1992).J. Biol. Chem. 267 15,224–15,228.Google Scholar
  80. Tonozuka, T., Ohtsuka, M., Mogi, S., Sakai, H., Olita, T., and Sakano, Y. (1993).Biosci. Biotech. Biochem. 57 395–401.Google Scholar
  81. Vihinen, M., Ollikka, P., Niskanen, J., Meyer, P., Suominen, I., Karp, M., Holm, L., Knowles, J., and Mäntsälä, P. (1990).J. Biochem. (Tokyo)107 267–272.Google Scholar
  82. Watanabe, K., Kitamura, K., Iha, H., and Suzuki, Y. (1990).Eur. J. Biochem. 192 609–620.Google Scholar
  83. Watanabe, K., Chishiro, K., Kitamura, K., and Suzuki, Y. (1991).J. Biol. Chem. 266 24,287–24,294.Google Scholar
  84. Yang, B.-Z., Ding, H.-H., Enghild, J. J., Bao, Y., and Chen, Y.-T. (1992).J. Biol. Chem. 267 9294–9299.Google Scholar

Copyright information

© Plenum Publishing Corporation 1993

Authors and Affiliations

  • Hans M. Jespersen
    • 1
  • E. Ann MacGregor
    • 2
  • Bernard Henrissat
    • 3
  • Michael R. Sierks
    • 1
  • Birte Svensson
    • 1
  1. 1.Department of ChemistryCarlsberg LaboratoryCopenhagen ValbyDenmark
  2. 2.Department of ChemistryUniversity of ManitobaWinnipegCanada
  3. 3.Centre de Recherches sur les Macromolécules Végétales, C. N. R. S., B.P.Grenoble cedexFrance

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