Skip to main content
Log in

Plant α-glucosidases of the glycoside hydrolase family 31. Molecular properties, substrate specificity, reaction mechanism, and comparison with family members of different origin

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  1. Alam S, Nakashima S, Deyashiki Y, Banno Y, Hara A, Nozawa Y: Molecular cloning of a gene encoding acid α-glucosidase from Tetrahymena pyriformis. J Eukaryot Microbiol 43: 295–303 (1996).

    Google Scholar 

  2. Arendt CW, Ostergaard HL: Identification of the CD45associated 116kDa and 80kDa proteins as the α-and βsubunits of α-glucosidase II. J Biol Chem 272: 13117–13125 (1997).

    Google Scholar 

  3. Bairoch A, Bucher P, Hofmann K: The PROSITE database: its status in 1995. Nucl Acids Res 24: 189–196 (1995).

    Google Scholar 

  4. Beers EP, Duke SH, Henson CA: Partial characterization and subcellular localization of three α-glucosidase isoforms in pea (Pisum sativum L.) seedlings. Plant Physiol 94: 738–744 (1990).

    Google Scholar 

  5. Braun C, Brayer GD, Withers SG: Mechanismbased inhibition of yeast α-glucosidase and human pancreatic α-amylase by a new class of inhibitors. J Biol Chem 270: 26778–26781 (1995).

    Google Scholar 

  6. Brzozowski AM, Davies GJ: Structure of the Aspergillus oryzae α-amylase complexed with the inhibitor acarbose at 2.α-0 Å resolution. Biochemistry 36: 10837–10845 (1997).

    Google Scholar 

  7. Chantret I, Lacasa M, Chevalier G, Ruf J, Islam I, Mantei N, Edwards Y, Swallow D, Rousset M: Sequence of the complete cDNA and the 5 structure of the human sucraseisomaltase gene. Possiblehomology with a yeast glucoamylase. Biochem J 285: 915–923 (1992).

    Google Scholar 

  8. Chiba S: α-Glucosidases. In: The Amylase Research Society of Japan (ed) Handbook of Amylases and Related Enzymes, pp. 104–105. Pergamon Press, Oxford (1988).

    Google Scholar 

  9. Chiba S: Molecular mechanism in α-glucosidase and glucoamylase. Biosci Biotechnol Biochem 61: 1233–1239 (1997).

    Google Scholar 

  10. Chiba S, Shimomura T: Purification and some properties of flint corn α-glucosidase. Agric Biol Chem 39: 1033–1040 (1975).

    Google Scholar 

  11. Chiba S, Inomata S, Matsui H, Shimomura T: Purification and properties of an α-glucosidase (glucoamylase) in sugar beet seeds. Agric Biol Chem 42: 241–245 (1978).

    Google Scholar 

  12. Chiba S, Kanaya K, Hiromi K, Shimomura T: Substrate specificity and subsite affinities of buckwheat α-glucosidase. Agric Biol Chem 43: 237–242 (1979).

    Google Scholar 

  13. Cogoli A, Semenza G: A probable oxocarbonium ion in the reaction mechanism of small intestinal sucrase and isomaltase. J Biol Chem 250: 7802–7809 (1975).

    Google Scholar 

  14. Davies GJ, Henrissat B: Structures and mechanisms of glycosyl hydrolases. Structure 3: 853–859 (1995).

    Google Scholar 

  15. Davies GJ, Wilson KS, Henrissat B: Nomenclature for sugarbinding subsites in glycosyl hydrolases. Biochem J 321: 557–559 (1997).

    Google Scholar 

  16. Dohmen JR, Strasser AWM, Dahlems UM, Hollenberg CP: Cloning of the Schwanniomyces occidentalis glucoamylase gene (GAM1) and its expression in Saccharamyces cerevisiae. Gene 95: 111–121 (1990).

    Google Scholar 

  17. Fierobe HP, Stoffer BB, Frandsen TP, Svensson B: Mutational modulation of substrate bondtype specificity and thermostability of glucoamylase from Aspergillus awamori by replacement with short homologue active site sequences and thiol/disulfide engineering. Biochemistry 35: 8696–8704 (1996).

    Google Scholar 

  18. Frandsen TP: Structure/function studies of exoacting glucosyl hydrolases. Ph. D. Thesis, University of Odense, Odense, Denmark (1997).

    Google Scholar 

  19. Frandsen TP, Stoffer BB, Palcic MM, Hof S, Svensson, B: Structure and energetics of the glucoamylaseisomaltose transitionstate complex probed by using modeling and deoxygenated substrates coupled with sitedirected mutagenesis. J Mol Biol 263: 79–89 (1996).

    Google Scholar 

  20. Gray GM, Lally BC, Conklin KA: Action of intestinal sucraseisomaltase and its free monomers on an α-limit dextrin. J Biol Chem 254: 6038–6043 (1979).

    Google Scholar 

  21. Grinna LS, Robbins PW: Substrate specificity of rat liver microsomal glucosidases which process glycoproteins. J Biol Chem 255: 2255–2258 (1980).

    Google Scholar 

  22. Henrissat B: A classification of glycosyl hydrolases based on amino acid sequence similarity. Biochem J 280: 309–316 (1991).

    Google Scholar 

  23. Henrissat B, Bairoch A: New families in the classification of glycosyl hydrolases based on amino acid similarities. Biochem J 293: 781–788 (1993).

    Google Scholar 

  24. Henson CA, Sun Z: Barley seed α-glucosidases: their characteristics and roles in starch degradation. In: Saddler JN, Penner, MH (eds) ACS Symposium Series 618, pp. 51–58. ACS, Washington, DC (1995).

    Google Scholar 

  25. Hermans MMP, de Graaff E, Kroos MA, Mohkamsing S, Eussen BJ, Joosse M, Willemsen R, Kleijer WJ, Oostra BA, Reuser AJJ: The effect of a single base pair deletion (ΔT525) and a C1634T missense mutation (pro545leu) on the expression of lysosomal α-glucosidase in patients with glycogen storage disease type II. Hum Mol Genet 3: 2213–2218 (1994).

    Google Scholar 

  26. Hermans MMP, de Graaff E, Kroos MA, Wisselaar HA, Oostra BA, Reuser AJJ: Identification of a point mutation in the human lysosomal α-glucosidase gene causing infantile glycogenosis type II. Biochem Biophys Res Commun 179: 919–926 (1991).

    Google Scholar 

  27. Hermans MMP, deGraaff E, Kroos MA, Wisselaar HA, Willemsen R, Oostra BA, Reuser AJJ: The conservative substitution Asp645→Glu in lysosomal α-glucosidase affects transport and phosphorylation of the enzyme in an adult patient with glycogenstorage disease type II. Biochem J 289: 687–693 (1993).

    Google Scholar 

  28. Hermans MMP, Kroos MA, van Beeumen J, Oostra BA, Reuser AJJ: Human lysosomal α-glucosidase. Characterization of the catalytic site. J Biol Chem 266: 13507–13512 (1991).

    Google Scholar 

  29. Hermans MMP, Kroos MA, de Graaff, E, Oostra BA, Reuser AJ: Two mutations affecting the transport and maturation of lysosomal α-glucosidase in an adult case of glycogen storage disease type II. Hum Mut 2: 268–273 (1993).

    Google Scholar 

  30. Hiromi K, Ohnishi M, Tanaka A: Subsite structure and ligand binding mechanism of glucoamylase. Mol Cell Biochem 51: 79–95 (1983).

    Google Scholar 

  31. Hoefsloot LH, Hoogeveen Westerveld M, Kroos MA, van Beeumen J, Reuser AJ, Oostra BA: Primary structure and processing of lysosomal α-glucosidase; homology with the intestinal sucraseisomaltase complex. EMBO J 7: 1697–1704 (1988).

    Google Scholar 

  32. Huie ML, Chen AS, Brooks SS, Grix A, Hirschorn R: A de novo 13 nt deletion, a newly identified C647W missense mutation and a deletion of exon 18 in infantile onset glycogen storage disease type II (GSDII). Hum Mol Genet 3: 1081–1087 (1994).

    Google Scholar 

  33. Hülseweh B, Dahlems UM, Dohmen J, Strasser AWM, Hollenberg CP: Characterization of the active site of Schwanniomyces occidentalis glucoamylase by in vitro mutagenesis. Eur J Biochem 244: 128–133 (1997).

    Google Scholar 

  34. Hunziker W, Spiess M, Semenza G, Lodish HF: The sucraseisomaltase complex: primary structure, membraneorientation, and evolution of a stalked, intrinsic brush border protein. Cell 46: 227–234 (1986).

    Google Scholar 

  35. Im H, Henson CA: Characterization of high pI α-glucosidase from germinated barley seeds: substrate specificity, subsite affinities and activesite residues. Carbohydr Res 277: 145–159. (1995).

    Google Scholar 

  36. InoharaOchiai M, Nakayama T, Goto R, Nakao M, Ueda T, Shibano Y: Altering substrate specificity of Bacillus sp. SAM1606 α-glucosidase by comparative sitespecific mutagenesis. J Biol Chem 272: 1601–1607 (1997).

    Google Scholar 

  37. Iwanami S, Matsui H, Kimura A, Ito H, Mori H, Honma M, Chiba S: Chemical modification and amino acid sequence of active site in sugar beet α-glucosidase. Biosci Biotechnol Biochem 59: 459–463 (1995).

    Google Scholar 

  38. Iwanami S, Nishimoto Y, Murata S, Ito H, Matsui H, Honma M, Chiba S: Identification of essential ionizable groups of rice α-glucosidase II. J Appl Glucosci 43: 67–71 (1996).

    Google Scholar 

  39. Jespersen HM, MacGregor EA, Sierks MR, Svensson B: Comparison of the domainlevel organization of starch hydrolases and related enzymes. Biochem J 280: 51–55 (1991).

    Google Scholar 

  40. Jespersen HM, MacGregor EA, Henrissat B, Sierks MR, Svensson B: Starchand glycogendebranching and branching enzymes: Prediction of structural features of the catalytic (β/ α-)8barrel domain and evolutionary relationship to other amylolytic enzymes. J Prot Chem 12: 791–805 (1993).

    Google Scholar 

  41. Kadziola A: Structure of an α-amylase complexed with acarbose. Ph.D. thesis, University of Copenhagen, Copenhagen, Denmark (1993).

    Google Scholar 

  42. Kanaya KI, Chiba S, Shimomura T, Nishi K: Improvedmethod for purification of buckwheat α-glucosidase and some kinetic properties. Agric Biol Chem 40: 1929–1936 (1976).

    Google Scholar 

  43. Kaushal GP, Pastuszak I, Hatanaka K, Elbein AD: Purification to homogeneity and properties of glucosidase II from mung bean seedlings and suspensioncultured soybean cells. J Biol Chem 265: 16271–16279.

  44. Killilea SD, Clancy MJ: Properties of potato α-glucosidase. Phytochemistry 17: 1429–1431 (1978).

    Google Scholar 

  45. Kimura A, Takata M, Sakai O, Matsui H, Takai N, Takayanagi T, Nishimura T, Uozumi T, Chiba S: Complete amino acid sequence of crystalline α-glucosidase from Aspergillus niger. Biosci Biotechnol Biochem 56: 1368–1370 (1992).

    Google Scholar 

  46. Kimura A, Takata M, Fukushi Y, Mori H, Matsui H, Chiba S: A catalytic amino acid and primary structure of active site in Aspergillus niger α-glucosidase. Biosci Biotechnol Biochem 61: 1091–1098 (1997).

    Google Scholar 

  47. Kinsella BT, Hogan S, Larkin A, Cantwell BA: Primary structure and processing of the Candida tsukubaensis α-glucosidase. Homology with the rabbit intestinal sucraseisomaltase complex and human lysosomal α-glucosidase. Eur J Biochem 202: 657–664 (1991).

    Google Scholar 

  48. Konishi Y, Kitazato S, Nakatani N: Partial purification and characterization of acid and neutral α-glucosidases from preclimacteric banana pulp tissues. Biosci Biotechnol Biochem 56: 2046–2051 (1992).

    Google Scholar 

  49. Koshland DE: Stereochemistry and the mechanism of enzymatic reactions. Biol Rev 28: 416–436 (1953).

    Google Scholar 

  50. Kuriki T, Kaneko H, Yanase M, Takata H, Shimada J, Handa S, Takada T, Umeyama H, Okada S: Controlling substrate preference and transglycosylation activity of neopullulanase bymanipulating steric constraint and hydrophobicity in active center. J Biol Chem 271: 17321–17329 (1996).

    Google Scholar 

  51. Lawson SL, Wakarchuk WW, Withers SG: Effects of both shortening and lengthening the active site nucleophile of Bacillus circulans xylanase on catalytic activity. Biochemistry 35: 10110–10118 (1996).

    Google Scholar 

  52. Legler G: Glycoside hydrolases: mechanistic information from studies with reversible and irreversible inhibitors. Adv Carb Chem Biochem 48: 319–385 (1990).

    Google Scholar 

  53. Lemieux RU: The hydrated polargroup ‘gate’ effect on the specificity and strength of the binding of oligosaccharides by protein receptor sites. In: Dahlbon R, Nilsson JLG (eds) Proceedings from the VIIIth International Symposium on Medical Chemistry 1, pp. 329–351. Swedish Pharmaceutical Press, Stockholm (1984).

    Google Scholar 

  54. Lemieux RU, Spohr U, Bach M, Cameron DR, Frandsen TP, Stoffer BB, Svensson B, Palcic MM: Chemical mapping of the active site of glucoamylase of Aspergillus niger. Can J Chem 74: 319–335 (1996).

    Google Scholar 

  55. Lin CY, Shieh JJ: Identification of a de novo point mutation resulting in infantile form of Pompe's disease. Biochem Biophys Res Commun 208: 886–893 (1995).

    Google Scholar 

  56. MacGregor AW: α-Amylase, limit dextrinase, and α-glucosidase enzymes in barley and malt. CRC Crit Rev Biotechnol 5: 117–128 (1987).

    Google Scholar 

  57. Matsui H, Chiba S, Shimomura T: Substrate specificity of an α-glucosidase in sugar beet seeds. Agric Biol Chem 42: 1855–1860 (1978).

    Google Scholar 

  58. Matsui H, Ito H, Chiba S: Lowmolecularactivity α--glucosidase from ungerminated rice seeds. Agric Biol Chem 52: 1859–1860 (1988).

    Google Scholar 

  59. Matsui H, Iwanami S, Ito H, Mori H, Honma M, Chiba S: Cloning and sequencing of a cDNA encoding α-glucosidase from sugar beet. Biosci Biotechnol Biochem 61: 875–880 (1997).

    Google Scholar 

  60. Matsui I, Svensson B: Improved activity andmodulated action pattern obtained by random mutagenesis at the fourth β-α-loop involved in substrate binding to the catalytic (β/α-)8-barrel domain of barley α-amylase. J Biol Chem 272: 22456–22463 (1997).

    Google Scholar 

  61. Matsui I, Yoneda S, Ishikawa K, Miyairi S, Fukui S, Umeyama H, Honda K: Roles of the aromatic residues conserved in the active center of Saccharomycopsis α-amylase for transglycosylation and hydrolysis activity. Biochemistry 33: 451–458 (1994).

    Google Scholar 

  62. McCarter JD, Withers SG: Mechanisms of enzymatic glycoside hydrolysis. Curr Opin Struct Biol 4: 885–892 (1994).

    Google Scholar 

  63. McCarter JD, Withers SG: 5-Fluoro glucosides: a newclass of mechanismbased inhibitors of both α-and α--glucosidases. J Am Chem Soc 118: 241–242 (1996).

    Google Scholar 

  64. McCarter JD, Withers SG: Unequivocal identification of Asp214 as the catalytic nucleophile of Saccharomyces cerevisiae α--glucosidase using 5fluoro glycosyl fluorides. J Biol Chem 271: 6889–6894 (1996).

    Google Scholar 

  65. McIntosh LP, Hand G, Johnson PE, Joshi MD, Körner M, Plesniak LA, Ziser L, Wakarchuk WW, Withers SG: The pKa of the general acid/base carboxyl group of a glycosidase cycles during catalysis: A 13CNMR study of Bacillus circulans xylanase. Biochemistry 35: 9958–9966 (1996).

    Google Scholar 

  66. Minamiura N: Mammalian α-glucosidases (Mammalian blood serum and human urine). In: The Amylase Research Society of Japan (ed) Handbook of Amylases and Related Enzymes, pp. 105–109. Pergamon Press, Oxford (1988).

    Google Scholar 

  67. Minetoki T, Gomi K, Kitamoto K, Kumagai C, Tamura G: Nucleotide sequence and expression of α-glucosidaseencoding gene (agdA) from Aspergillus oryzae. Biosci Biotechnol Biochem 59: 1516–1521 (1995).

    Google Scholar 

  68. Moremen KW, Trimble RB, Herscovics A: Glycosidases of the asparaginelinked oligosaccharide processing pathway. Glycobiology 4: 113–125 (1994).

    Google Scholar 

  69. Naim HY, Niermann T, Kleinhans U, Hollenberg CP, Strasser AWM: Striking structural and functional similarities suggest that intestinal sucraseisomaltase, human lysosomal α-glucosidase and Schwanniomyces occidentalis glucoamylase are derived from a common ancestral gene. FEBS Lett 294: 109–112 (1991).

    Google Scholar 

  70. Nichols BL, Quaroni A, Avery SA, Eldering JA, Sterchi EE: Homology of human maltaseglucoamylase (MGA) with sucraseisomaltase (SIM). FASEB J 11: A609 (1997).

    Google Scholar 

  71. Nikrad PV, Beierbeck H, Lemieux RU: Molecular recognition X. A novel procedure for the detection of the intermolecular hydrogen bonds present in a proteinoligosaccharide complex. Can J Chem 70: 241–253 (1992).

    Google Scholar 

  72. Peruffo ADB, Renosto F, Pallavicini C: α-Glucosidase from grape berries: partial purification and characterization. Planta 142: 195–201 (1978).

    Google Scholar 

  73. Qian M, Haser R, Buisson G, Duée E, Payan F: The active centre of a mammalian α-amylase. Structure of the complex of a pancreatic α-amylase with a carbohydrate inhibitor refined to 2.2 Å resolution. Biochemistry 33: 6284–6294 (1994).

    Google Scholar 

  74. Quaroni A, Semenza G: Partial amino acid sequences around the essential carboxylate in the active sites of the intestinal sucraseisomaltase complex. J Biol Chem 251: 3250–3253 (1976).

    Google Scholar 

  75. Quiocho FA: Probing the atomic interactions between proteins and carbohydrates. Biochem Soc Trans 21: 442–448 (1993).

    Google Scholar 

  76. Sierks MR, Svensson B: Kinetic identification of a hydrogen bonding pair in the glucoamylase/maltose transition state complex. Protein Eng 5: 185–188 (1992).

    Google Scholar 

  77. Sierks MR, Bock K, Refn S, Svensson B: Active site similarities of glucose dehydrogenase, glucose oxidase and gluc13 oamylase probed by deoxygenated substrates. Biochemistry 31: 8972–8977 (1992).

    Google Scholar 

  78. Sinnott ML: Catalyticmechanisms of enzymic glycosyl transfer. Chem Rev 90: 1171–1202 (1990).

    Google Scholar 

  79. Sissons, MJ, MacGregor AW: Hydrolysis of barley starch granules by α-glucosidases from malt. J Cereal Sci 19: 161–169 (1994).

    Google Scholar 

  80. Strokopytov B, Penninga D, Rozeboom HJ, Kalk KH, Dijkhuizen L, Dijkstra BW: Xray structure of cyclodextrin glycosyltransferase complexed with acarbose. Implications for the catalytic mechanism of glycosidases. Biochemistry 34: 2234–2240 (1995).

    Google Scholar 

  81. Strokopytov B, Knegtel RMA, Penninga D, Rozeboom HJ, Kalk KH, Dijkhuizen L, Dijkstra BW: Structure of cyclodextrin glycosyltransferase complexed with a maltononaose inhibitor at 2.6 Å resolution. Implications for product specificity. Biochemistry 35: 4241–4249 (1996).

    Google Scholar 

  82. Sugimoto M, Suzuki Y: Molecular cloning, sequencing, and expression of a cDNA encoding α-glucosidase from Mucor javanicus. J Biochem 119: 500505 (1996).

    Google Scholar 

  83. Sugimoto M, Furui S, Suzuki Y: Multiple molecular forms of α-glucosidase from spinach seeds, Spinacia oleracea L. Biosci Biotechnol Biochem 59: 673–677 (1995).

    Google Scholar 

  84. Sugimoto M, Furui S, Suzuki Y: Molecular cloning and characterization of a cDNAencoding α-glucosidase from spinach. Plant Mol Biol 33: 765–768 (1997).

    Google Scholar 

  85. Sun Z, Henson CA: Degradation of native starch granules by barley α-glucosidases. Plant Physiol 94: 320–327 (1990).

    Google Scholar 

  86. Sun Z, Duke SH, Henson CA: The role of pea chloroplast α--glucosidase in transitory starch degradation. Plant Physiol 108: 211–217 (1995).

    Google Scholar 

  87. Suzuki Y, Uchida K: Three forms of α-glucosidase from welsh onion (Allium fistulosum L.). Agric Biol Chem 48: 1343–1345 (1984).

    Google Scholar 

  88. Svensson B: Protein engineering in the α-amylase family: catalytic mechanism, substrate specificity, and stability. Plant Mol Biol 25: 141–157 (1994).

    Google Scholar 

  89. Svensson B, Søgaard M: Mutational analysis of glycosylase function. J Biotechnol 29: 1–37 (1993).

    Google Scholar 

  90. Szumilo T, Kaushal GP, Elbein AD: Purification and properties of glucosidase I from mung bean seedlings. Arch Biochem Biophys 247: 261–271 (1986).

    Google Scholar 

  91. Takahashi N, Shimomura T, Chiba S: Studies on α-glucosidase in rice. Part I. Isolation and some properties of α-glucosidase I and α-glucosidase II. Agric Biol Chem 35: 2015–2024 (1971).

    Google Scholar 

  92. Tanaka Y, Tao W, Blanchard JS, Hehre EJ: Transition state structures for the hydrolysis of α-D-glucopyranosyl fluoride by retaining and inverting reactions of glycosylases. J Biol Chem 269: 32306–32312 (1994).

    Google Scholar 

  93. Tai VWF, Fung PH, Wong YS, Shing TKM: Kinetic studies on cyclophellitol analoguesmechanismbased inactivators. Biochem Biophys Res Commun 213: 175–180 (1995).

    Google Scholar 

  94. Tibbot BK, Skadsen RW: Molecular cloning and characterization of a gibberellininducible, putative α-glucosidase gene from barley. Plant Mol Biol 30: 229–241 (1996).

    Google Scholar 

  95. Watanabe K, Hata Y, Kizaki H, Katsube Y, Suzuki Y: The refined structure of Bacillus cereus oligo1,6glucosidase at 2.0 Å resolution: structural characterization of prolinesubstitution sites for protein thermostabilization. J Mol Biol 269: 142–153 (1997).

    Google Scholar 

  96. Withers SG, Aebersold R: Approaches to labelling and identification of active site residues in glycosidases. Protein Sci 4: 361–372 (1995).

    Google Scholar 

  97. Yamasaki Y, Suzuki Y: Purification and properties of three forms of α-glucosidase from germinated green gram (Phaseolus vidissimus Ten.). Agric Biol Chem 43: 481–489 (1979).

    Google Scholar 

  98. Yamasaki Y, Suzuki Y: Two forms of α-glucosidase from sugarbeet seeds. Planta 148: 354–361 (1980).

    Google Scholar 

  99. Yamasaki Y, Konno H: Two forms of α-glucosidase from soybean callus. Agric Biol Chem 49: 849–850 (1985).

    Google Scholar 

  100. Yoshioka Y, Hasegawa K, Matsuura Y, Katsube Y, Kubota M: Crystal structures of a mutant maltotetraoseforming exoamylase cocrystallized with maltopentaose. J Mol Biol 271: 619–628 (1997).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Frandsen, T.P., Svensson, B. Plant α-glucosidases of the glycoside hydrolase family 31. Molecular properties, substrate specificity, reaction mechanism, and comparison with family members of different origin. Plant Mol Biol 37, 1–13 (1998). https://doi.org/10.1023/A:1005925819741

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005925819741

Navigation