Crystal structure of glycogen debranching enzyme and insights into its catalysis and disease-causing mutations

Nature Communications

Volumn 7, Issue , 2016, Pages

  Zhai, Liting ^a   Feng, Lingling ^a,b   Xia, Lin ^a   Yin, Huiyong ^a   Xiang, Song ^a  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN; GLYCOGEN DEBRANCHING ENZYME; OLIGOSACCHARIDE; FUNGAL PROTEIN; PROTEIN BINDING;

CATALYSIS; CRYSTAL STRUCTURE; ENZYME; GENETIC ANALYSIS; GLUCOSE; MOLECULAR ANALYSIS; MUTATION; POLYMER;

AMINO TERMINAL SEQUENCE; ARTICLE; ASPERGILLUS AWAMORI; BINDING SITE; CANDIDA GLABRATA; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISEASE COURSE; DISULFIDE BOND; ENZYME ACTIVE SITE; GLUCONEOGENESIS; GLYCOGEN METABOLISM; HYDROGEN BOND; MISSENSE MUTATION; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; PHOTON CORRELATION SPECTROSCOPY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; AMINO ACID SEQUENCE; ANIMAL; BIOCATALYSIS; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; GLYCOGEN STORAGE DISEASE TYPE 3; HUMAN; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; MUTATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

ANIMALIA; FUNGI;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BIOCATALYSIS; CANDIDA GLABRATA; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; FUNGAL PROTEINS; GLYCOGEN; GLYCOGEN DEBRANCHING ENZYME SYSTEM; GLYCOGEN STORAGE DISEASE TYPE III; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; OLIGOSACCHARIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

EID: 84973369314     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11229     Document Type: Article

References (65)

1. Roach, P. J., Depaoli-Roach, A. A., Hurley, T. D. & Tagliabracci, V. S. Glycogen and its metabolism: some new developments and old themes. Biochem. J. 441, 763-787 (2012).
2. Roach, P. J. Glycogen and its metabolism. Curr. Mol. Med. 2, 101-120 (2002).
3. Dagli, A., Sentner, C. P. & Weinstein, D. A. Glycogen Storage Disease Type III in (eds Pagon, R. A., Adam, M. P., Ardinger, H. H). Available at: http://www.ncbi.nlm.nih.gov/books/NBK26372/ (2012).
4. Lucchiari, S., Santoro, D., Pagliarani, S. & Comi, G. P. Clinical, biochemical and genetic features of glycogen debranching enzyme deficiency. Acta. Myol. 26, 72-74 (2007).
5. Nelson, T. E., Kolb, E. & Larner, J. Purification and properties of rabbit muscle amylo-1,6-glucosidase-oligo-1,4-1,4-transferase. Biochemistry 8, 1419-1428 (1969).
6. Brown, D. H. & Illingworth, B. The properties of an oligo-1,4-1,4-glucantransferase from animal tissues. Proc. Natl Acad. Sci. USA 48, 1783-1787 (1962).
7. Zmasek, C. M. & Godzik, A. Phylogenomic analysis of glycogen branching and debranching enzymatic duo. BMC. Evol. Biol. 14, 183 (2014).
8. Woo, E. J. et al. Structural insight into the bifunctional mechanism of the glycogen-debranching enzyme TreX from the archaeon Sulfolobus solfataricus. J. Biol. Chem. 283, 28641-28648 (2008).
9. Park, H. S. et al. TreX from Sulfolobus solfataricus ATCC 35092 displays isoamylase and 4-alpha-glucanotransferase activities. Biosci. Biotechnol. Biochem. 71, 1348-1352 (2007).
10. Song, H. N. et al. Structural rationale for the short branched substrate specificity of the glycogen debranching enzyme GlgX. Proteins 78, 1847-1855 (2010).
11. Makino, Y. & Omichi, K. Purification of glycogen debranching enzyme from porcine brain: evidence for glycogen catabolism in the brain. Biosci. Biotechnol. Biochem. 70, 907-915 (2006).
12. Tabata, S. & Hizukuri, S. Properties of yeast debranching enzyme and its specificity toward branched cyclodextrins. Eur. J. Biochem. 206, 345-348 (1992).
13. Heizmann, C. W. & Eppenberger, H. M. Glycogen debranching enzyme from chicken pectoralis muscle. Comparison with a 165000 mol. wt myofibrillar protein. FEBS Lett. 105, 35-39 (1979).
14. Becker, J. U., Long, T. J. & Fischer, E. H. Purification and properties of debranching enzyme from dogfish muscle. Biochemistry 16, 291-297 (1977).
15. Taylor, C., Cox, A. J., Kernohan, J. C. & Cohen, P. Debranching enzyme from rabbit skeletal muscle. Purification, properties and physiological role. Eur. J. Biochem. 51, 105-115 (1975).
16. Lee, E. Y., Carter, J. H., Nielsen, L. D. & Fischer, E. H. Purification and properties of yeast amylo-1,6-glucosidase-oligo-1,4-41,4-glucantransferase. Biochemistry 9, 2347-2355 (1970).
17. Bates, E. J., Heaton, G. M., Taylor, C., Kernohan, J. C. & Cohen, P. Debranching enzyme from rabbit skeletal muscle; evidence for the location of two active centres on a single polypeptide chain. FEBS Lett. 58, 181-185 (1975).
18. Liu, W., Madsen, N. B., Braun, C. & Withers, S. G. Reassessment of the catalytic mechanism of glycogen debranching enzyme. Biochemistry 30, 1419-1424 (1991).
19. Gillard, B. K. & Nelson, T. E. Amylo-1,6-glucosidase/4-alpha-glucanotransferase: use of reversible substrate model inhibitors to study the binding and active sites of rabbit muscle debranching enzyme. Biochemistry 16, 3978-3987 (1977).
20. Liu, W. et al. Molecular cloning, sequencing, and analysis of the cDNA for rabbit muscle glycogen debranching enzyme. Arch. Biochem. Biophys. 306, 232-239 (1993).
21. MacGregor, E. A., Janecek, S. & Svensson, B. Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes. Biochim. Biophys. Acta. 1546, 1-20 (2001).
22. Braun, C., Lindhorst, T., Madsen, N. B. & Withers, S. G. Identification of Asp 549 as the catalytic nucleophile of glycogen-debranching enzyme via trapping of the glycosyl-enzyme intermediate. Biochemistry 35, 5458-5463 (1996).
23. Nakayama, A., Yamamoto, K. & Tabata, S. Identification of the catalytic residues of bifunctional glycogen debranching enzyme. J. Biol. Chem. 276, 28824-28828 (2001).
24. Osterlund, B. R., Hayakawa, K., Madsen, N. B. & James, M. N. Crystallization of glycogen debranching enzyme. J. Mol. Biol. 174, 557-559 (1984).
25. Scraba, D. G., Bradley, R. D., Fitzgerald, P. M. & Madsen, N. B. Electron microscopy of glycogen degrading enzymes. FEBS Lett. 240, 133-138 (1988).
26. Sauer, J. et al. Glucoamylase: structure/function relationships, and protein engineering. Biochim. Biophys. Acta. 1543, 275-293 (2000).
27. Aleshin, A. E., Stoffer, B., Firsov, L. M., Svensson, B. & Honzatko, R. B. Crystallographic complexes of glucoamylase with maltooligosaccharide analogs: relationship of stereochemical distortions at the nonreducing end to the catalytic mechanism. Biochemistry 35, 8319-8328 (1996).
28. Brzozowski, A. M. & Davies, G. J. Structure of the Aspergillus oryzae alpha-amylase complexed with the inhibitor acarbose at 2.0 A resolution. Biochemistry 36, 10837-10845 (1997).
29. Yamamoto, E., Makino, Y. & Omichi, K. Active site mapping of amyloalpha-1,6-glucosidase in porcine liver glycogen debranching enzyme using fluorogenic 6-O-alpha-glucosyl-maltooligosaccharides. J. Biochem. 141, 627-634 (2007).
30. Cheng, A., Zhang, M., Okubo, M., Omichi, K. & Saltiel, A. R. Distinct mutations in the glycogen debranching enzyme found in glycogen storage disease type III lead to impairment in diverse cellular functions. Hum. Mol. Genet. 18, 2045-2052 (2009).
31. Aoyama, Y. et al. Molecular features of 23 patients with glycogen storage disease type III in Turkey: a novel mutation p. R1147G associated with isolated glucosidase deficiency, along with 9 AGL mutations. J. Hum. Genet. 54, 681-686 (2009).
32. Watanabe, Y., Makino, Y. & Omichi, K. Donor substrate specificity of 4-alpha-glucanotransferase of porcine liver glycogen debranching enzyme and complementary action to glycogen phosphorylase on debranching. J. Biochem. 143, 435-440 (2008).
33. Stapleton, D. et al. Analysis of hepatic glycogen-associated proteins. Proteomics 10, 2320-2329 (2010).
34. Ko, J. S. et al. A mutation analysis of the AGL gene in Korean patients with glycogen storage disease type III. J. Hum. Genet. 59, 42-45 (2014).
35. Sentner, C. P., Vos, Y. J., Niezen-Koning, K. N., Mol, B. & Smit, G. P. Mutation analysis in glycogen storage disease type III patients in the Netherlands: novel genotype-phenotype relationships and five novel mutations in the AGL gene. JIMD Rep. 7, 19-26 (2013).
36. Goldstein, J. L. et al. Molecular analysis of the AGL gene: identification of 25 novel mutations and evidence of genetic heterogeneity in patients with glycogen storage disease type III. Genet. Med. 12, 424-430 (2010).
37. Cheng, A. et al. A role for AGL ubiquitination in the glycogen storage disorders of Lafora and Cori's disease. Genes Dev. 21, 2399-2409 (2007).
38. Lucchiari, S. et al. Hepatic and neuromuscular forms of glycogenosis type III: nine mutations in AGL. Hum. Mutat. 27, 600-601 (2006).
39. Lucchiari, S. et al. Molecular characterisation of GSD III subjects and identification of six novel mutations in AGL. Hum. Mutat. 20, 480 (2002).
40. Oh, S. H., Park, H. D., Ki, C. S., Choe, Y. H. & Lee, S. Y. Biochemical and molecular investigation of two Korean patients with glycogen storage disease type III. Clin. Chem. Lab. Med. 46, 1245-1249 (2008).
41. Walker, G. J. & Whelan, W. J. The mechanism of carbohydrase action. 8. Structures of the muscle-phosphorylase limit dextrins of glycogen and amylopectin. Biochem. J. 76, 264-268 (1960).
42. Pinotsis, N., Leonidas, D. D., Chrysina, E. D., Oikonomakos, N. G. & Mavridis, I. M. The binding of beta- and gamma-cyclodextrins to glycogen phosphorylase b: kinetic and crystallographic studies. Protein. Sci. 12, 1914-1924 (2003).
43. Baskaran, S. et al. Multiple glycogen-binding sites in eukaryotic glycogen synthase are required for high catalytic efficiency toward glycogen. J. Biol. Chem. 286, 33999-34006 (2011).
44. Raththagala, M. et al. Structural mechanism of laforin function in glycogen dephosphorylation and lafora disease. Mol. Cell. 57, 261-272 (2015).
45. Yamamoto, E., Watanabe, Y., Makino, Y. & Omichi, K. Inspection of the activator binding site for 4-alpha-glucanotransferase in porcine liver glycogen debranching enzyme with fluorogenic dextrins. J. Biochem. 145, 585-590 (2009).
46. Watanabe, Y., Makino, Y. & Omichi, K. Activation of 4-alphaglucanotransferase activity of porcine liver glycogen debranching enzyme with cyclodextrins. J. Biochem. 140, 135-140 (2006).
47. Liu, Y. et al. Laforin-malin complex degrades polyglucosan bodies in concert with glycogen debranching enzyme and brain isoform glycogen phosphorylase. Mol. Neurobiol. 49, 645-657 (2014).
48. Sakoda, H. et al. Glycogen debranching enzyme association with beta-subunit regulates AMP-activated protein kinase activity. Am. J. Physiol. Endocrinol. Metab. 289, E474-E481 (2005).
49. Ritterson Lew, C., Guin, S. & Theodorescu, D. Targeting glycogen metabolism in bladder cancer. Nat. Rev. Urol. 12, 383-391 (2015).
50. Guin, S. et al. Role in tumor growth of a glycogen debranching enzyme lost in glycogen storage disease. J. Natl Cancer Inst. 106, dju062 (2014).
51. Doublie, S. et al. Crystallization and preliminary X-ray analysis of the 9 kDa protein of the mouse signal recognition particle and the selenomethionyl-SRP9. FEBS Lett. 384, 219-221 (1996).
52. Leslie, A. G. W. & Powell, H. R. Processing diffraction data with MOSFLM. Evol. Methods Macromol. Crystallogr. 245, 41-51 (2007).
53. Evans, P. Scaling and assessment of data quality. Acta. Crystallogr. D. Biol. Crystallogr. 62, 72-82 (2006).
54. Dauter, Z. Estimation of anomalous signal in diffraction data. Acta. Crystallogr. D. Biol. Crystallogr. 62, 867-876 (2006).
55. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta. Crystallogr. D. Biol. Crystallogr. 66, 213-221 (2010).
56. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta. Crystallogr. D. Biol. Crystallogr. 60, 2126-2132 (2004).
57. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta. Crystallogr. A. 47, 110-119 (1991).
58. Vagin, A. & Teplyakov, A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025 (1997).
59. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta. Crystallogr. D. Biol. Crystallogr. 53, 240-255 (1997).
60. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291 (1993).
61. Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549 (2010).
62. Lee, B. & Richards, F. M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55, 379-400 (1971).
63. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta. Crystallogr. D. Biol. Crystallogr. 67, 235-242 (2011).
64. Kunst, A., Draeger, B. & Ziegenhorn, J. UV methods with hexokinase and glucose-6-phosphate dehydrogenase. Methods of Enzymatic Analysis. 3rd edn 6, 163-172 (1984).
65. McBride, A., Ghilagaber, S., Nikolaev, A. & Hardie, D. G. The glycogen-binding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor. Cell. Metab. 9, 23-34 (2009).