Structural basis of glycogen branching enzyme deficiency and pharmacologic rescue by rational peptide design

Human Molecular Genetics

Volumn 24, Issue 20, 2015, Pages 5667-5676

  Sean Froese, D ^a,g   Michaeli, Amit ^b   McCorvie, Thomas J ^a   Krojer, Tobias ^a   Sasi, Meitav ^c   Melaev, Esther ^c   Goldblum, Amiram ^b,d   Zatsepin, Maria ^b   Lossos, Alexander ^c   Álvarez, Rafael ^e   Escribá, Pablo V ^e   Minassian, Berge A ^f   Von Delft, Frank ^a   Kakhlon, Or ^c   Yue, Wyatt W ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Pepticom LTD   (Israel)

^c HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

^g UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 ALPHA GLUCAN BRANCHING ENZYME; AMYLASE; GLYCOGEN BRANCHING ENZYME 1; HEPTASACCHARIDE; LEUCYLTHREONYLLYSYLGLUTAMIC ACID; MUTANT PROTEIN; OLIGOSACCHARIDE; RECOMBINANT ENZYME; TETRAPEPTIDE; TETRASACCHARIDE; UNCLASSIFIED DRUG; GBE1 PROTEIN, HUMAN; GLYCOGEN DEBRANCHING ENZYME; PEPTIDE;

ADULT POLYGLUCOSAN BODY DISEASE; ALLELE; ANIMAL CELL; ARTICLE; COMPLEX FORMATION; COMPUTER MODEL; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DRUG DESIGN; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME DEFICIENCY; ENZYME STRUCTURE; GLYCOGEN BRANCHING ENZYME 1 DEFICIENCY; GLYCOGEN STORAGE DISEASE TYPE 4; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MISSENSE MUTATION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN EXPRESSION; SOLUBILITY; WILD TYPE; AMINO ACID SEQUENCE; BIOLOGY; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; GLYCOGEN STORAGE DISEASE; METABOLISM; MOLECULAR GENETICS; NERVOUS SYSTEM DISEASES; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; GLYCOGEN DEBRANCHING ENZYME SYSTEM; GLYCOGEN STORAGE DISEASE; GLYCOGEN STORAGE DISEASE TYPE IV; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NERVOUS SYSTEM DISEASES; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

EID: 84943763050     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv280     Document Type: Article

References (34)

1. Roach, P.J. (2002) Glycogen and its metabolism. Curr. Mol. Med., 2, 101-120.
2. Smythe, C. and Cohen, P. (1991) The discovery of glycogenin and the priming mechanism for glycogen biogenesis. Eur. J. Biochem., 200, 625-631.
3. Cid, E., Geremia, R.A., Guinovart, J.J. and Ferrer, J.C. (2002) Glycogen synthase: towards a minimum catalytic unit? FEBS Lett., 528, 5-11.
4. Boyer, C. and Preiss, J. (1977) Biosynthesis of bacterial glycogen. Purification and properties of the Escherichia coli b alpha-1,4,-glucan: alpha-1,4-glucan 6-glycosyltansferase. Biochemistry, 16, 3693-3699.
5. Thon, V.J., Khalil, M. and Cannon, J.F. (1993) Isolation of human glycogen branching enzyme cDNAs by screening complementation in yeast. J. Biol. Chem., 268, 7509-7513.
6. Melendez, R., Melendez-Hevia, E. and Canela, E.I. (1999) The fractal structure of glycogen: a clever solution to optimize cell metabolism. Biophys. J., 77, 1327-1332.
7. Nishi, A.,Nakamura,Y., Tanaka, N. and Satoh,H. (2001) Biochemical and genetic analysis of the effects of amylose-extendermutation in rice endosperm. Plant Physiol., 127, 459-472.
8. Magoulas, P.L., El-Hattab, A.W., Roy, A., Bali, D.S., Finegold, M. J. and Craigen, W.J. (2012) Diffuse reticuloendothelial system involvement in type IV glycogen storage disease with a novel GBE1 mutation: a case report and review. Hum. Pathol., 43, 943-951.
9. Moses, S.W. and Parvari, R. (2002) The variable presentations of glycogen storage disease type IV: a review of clinical, enzymatic and molecular studies. Curr. Mol. Med., 2, 177-188.
10. Kishnani, P.S., Koeberl, D. and Chen, Y.T. (2009) Glycogen Storage Diseases. McGraw-Hill, New York.
11. Bao, Y., Kishnani, P.,Wu, J.Y. and Chen, Y.T. (1996) Hepatic and neuromuscular forms of glycogen storage disease type IV caused by mutations in the same glycogen-branching enzyme gene. J. Clin. Invest., 97, 941-948.
12. Bruno, C., Cassandrini, D., Assereto, S., Akman, H.O., Minetti, C. and Di Mauro, S. (2007) Neuromuscular forms of glycogen branching enzyme deficiency. Acta Myol., 26, 75-78.
13. Bruno, C., Servidei, S., Shanske, S., Karpati, G., Carpenter, S., McKee, D., Barohn, R.J., Hirano, M., Rifai, Z. and DiMauro, S. (1993) Glycogen branching enzyme deficiency in adult polyglucosan body disease. Ann. Neurol., 33, 88-93.
14. Ban, H.R., Kim, K.M., Jang, J.Y., Kim, G.H., You, H.W., Kim, K., Yu, E., Kim, D.Y., Kim, K.H., Lee, Y.J. et al. (2009) Living donor liver transplantation in a Korean child with glycogen storage disease Type IV and a GBE1 mutation. Gut. Liver, 3, 60-63.
15. Stam, M.R., Danchin, E.G., Rancurel, C., Coutinho, P.M. and Henrissat, B. (2006) Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of alpha-amylase-related proteins. Protein Eng. Des. Sel., 19, 555-562.
16. MacGregor, E.A., Janecek, S. and Svensson, B. (2001) Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes. Biochim. Biophys Acta, 1546, 1-20.
17. Noguchi, J., Chaen, K., Vu, N.T., Akasaka, T., Shimada, H., Nakashima, T., Nishi, A., Satoh, H., Omori, T., Kakuta, Y. et al. (2011) Crystal structure of the branching enzyme I (BEI) from Oryza sativa L with implications for catalysis and substrate binding. Glycobiology, 21, 1108-1116.
18. Abad, M.C., Binderup, K., Rios-Steiner, J., Arni, R.K., Preiss, J. and Geiger, J.H. (2002) The X-ray crystallographic structure of Escherichia coli branching enzyme. J. Biol. Chem., 277, 42164-42170.
19. Pal, K., Kumar, S., Sharma, S., Garg, S.K., Alam, M.S., Xu, H.E., Agrawal, P. and Swaminathan, K. (2010) Crystal structure of full-length Mycobacterium tuberculosis H37Rv glycogen branching enzyme: insights of N-terminal beta-sandwich in substrate specificity and enzymatic activity. J. Biol. Chem., 285, 20897-20903.
20. Janecek, S., Svensson, B. and MacGregor, E.A. (2011) Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals. Enzyme Microb. Technol., 49, 429-440.
21. Chaen, K., Noguchi, J., Omori, T., Kakuta, Y. and Kimura, M. (2012) Crystal structure of the rice branching enzyme I (BEI) in complex with maltopentaose. Biochem. Biophys. Res. Commun., 424, 508-511.
22. Kuriki, T., Stewart, D.C. and Preiss, J. (1997) Construction of chimeric enzymes out of maize endosperm branching enzymes I and II: activity and properties. J. Biol. Chem., 272, 28999-29004.
23. Brzozowski, A.M., Lawson, D.M., Turkenburg, J.P., Bisgaard-Frantzen, H., Svendsen, A., Borchert, T.V., Dauter, Z., Wilson, K.S. and Davies, G.J. (2000) Structural analysis of a chimeric bacterial alpha-amylase. High-resolution analysis of native and ligand complexes. Biochemistry, 39, 9099-9107.
24. Payan, F. and Qian, M. (2003) Crystal structure of the pig pancreatic alpha-amylase complexed with malto-oligosaccharides. J. Protein Chem., 22, 275-284.
25. Kumar, V. (2011) Identification of the sequence motif of glycoside hydrolase 13 family members. Bioinformation, 6, 61-63.
26. Lossos, A., Kakhlon, O. and Soffer, D. (2014) In Vallat, J.-M., Weis, J., Gray, F. and Keohane, K. (eds), Peripheral Nerve Disorders: Pathology & Genetics. John Wiley & Sons, Ltd, pp. 167-171.
27. Lossos, A., Meiner, Z., Barash, V., Soffer, D., Schlesinger, I., Abramsky, O., Argov, Z., Shpitzen, S. and Meiner, V. (1998) Adult polyglucosan body disease in Ashkenazi Jewish patients carrying the Tyr329Ser mutation in the glycogenbranching enzyme gene. Ann. Neurol., 44, 867-872.
28. Gomes, C.M. (2012) Protein misfolding in disease and small molecule therapies. Curr. Top Med. Chem., 12, 2460-2469.
29. Fang, L., Chow, K.M., Hou, S., Xue, L., Chen, X., Rodgers, D.W., Zheng, F. and Zhan, C.G. (2014) Rational design, preparation, and characterization of a therapeutic enzyme mutant with improved stability and function for cocaine detoxification. ACS Chem. Biol., 9, 1764-1772.
30. Kelly, K.A., Reynolds, F., Weissleder, R. and Josephson, L. (2004) Fluorescein isothiocyanate-hapten immunoassay for determination of peptide-cell interactions. Anal. Biochem., 330, 181-185.
31. Gregersen, N., Bross, P., Vang, S. and Christensen, J.H. (2006) Protein misfolding and human disease. Annu. Rev. Genomics Hum. Genet., 7, 103-124.
32. Jha, S. and Komar, A.A. (2011) Birth, life and death of nascent polypeptide chains. Biotechnol. J., 6, 623-640.
33. Boyd, R.E., Lee, G., Rybczynski, P., Benjamin, E.R., Khanna, R., Wustman, B.A. and Valenzano, K.J. (2013) Pharmacological chaperones as therapeutics for lysosomal storage diseases. J. Med. Chem., 56, 2705-2725.
34. Akman, H.O., Kakhlon, O., Coku, J., Peverelli, L., Rosenmann, H., Rozenstein-Tsalkovich, L., Turnbull, J., Meiner, V., Chama, L., Lerer, I. et al. (2015) Deep intronic GBE1 mutation in manifesting heterozygous patients with adult polyglucosan body disease. JAMA Neurol., doi:10.1001/jamaneurol. 2014.4496.