Abstract
It is widely known that sulfate ion at high concentration serves like an allosteric activator of glycogen phosphorylase (GP). Based on the crystallographic studies on GP, it has been assumed that the sulfate ion is bound close to the phosphorylatable Ser14 site of nonactivated GP, causing a conformational change to catalytically-active GP. However, there are also reports that sulfate ion inhibits allosterically-activated GP by preventing the phosphate substrate from attaching to the catalytic site. In the present study, using a high concentration of sulfate ion, significant enhancement of GP activity was observed when macromolecular glycogen was used as substrate but not when smaller maltohexaose was used. In glycogen solution, nonreducing-end glucose residues are localized on the surface of glycogen and are not distributed homogenously in the solution. Using cyclodextrin-immobilized column chromatography, we found that sulfate at high concentration promoted GP–dextrin binding through the dextrin-binding site (DBS) located away from the catalytic site. This result is consistent with the properties of the DBSs found in glycogen-debranching enzyme and β-amylase. Therefore, we propose a new interpretation of the sulfate activation of GP, wherein sulfate ions at high concentration promote glycogen-binding to the DBS directly, and glycogen-binding to the catalytic site indirectly. Our findings were successfully applied to the affinity purification of porcine brain GP.
Similar content being viewed by others
Abbreviations
- CD:
-
cyclodextrin
- DBS:
-
dextrin-binding site
- GDE:
-
glycogen-debranching enzyme
- Glc:
-
D-glucose
- Glc-1-P:
-
α-D-glucose 1-phosphate
- GlcPA:
-
1-deoxy-1-[(2-pyridyl)amino]-D-glucitol
- GP:
-
glycogen phosphorylase
- HPLC:
-
high-performance liquid chromatography
- MW:
-
molecular weight
- PA:
-
pyridylamino
- Pi :
-
inorganic phosphate
- Ser:
-
L-serine
References
Roach, P.J., Depaoli-Roach, A.J., Hurley, T.D., Tagliabracci, V.S.: Glycogen and its metabolism: some new developments and old themes. Biochem. J. 441, 763–787 (2012)
Brown, A.M.: Brain glycogen re-awakened. J. Neurochem. 89, 537–552 (2004)
Titani, K., Koide, A., Hermann, J., Ericsson, L.H., Kumar, S., Wade, R.D., Walsh, K.A., Neurath, H., Fisher, E.H.: Complete amino acid sequence of rabbit muscle glycogen phosphorylase. Proc. Natl. Acad. Sci. U. S. A. 74, 4762–4766 (1977)
Tagaya, M., Fukui, T.: Catalytic reaction of glycogen phosphorylase reconstituted with a coenzyme-substrate conjugate. J. Biol. Chem. 259, 4860–4865 (1984)
Gordon, R.B., Brown, D.H., Brown, B.I.: Preparation and properties of the glycogen-debranching enzyme from rabbit liver. Biochim. Biophys. Acta. 289, 97–107 (1972)
Zhai, L., Feng, L., Xia, L., Yin, H., Xiang, S.: Crystal structure of glycogen debranching enzyme and insights into its catalysis and disease-causing mutations. Nat. Commun. 7, 11229 (2016)
Sato, S., Ohi, T., Nishino, I., Sugie, H.: Confirmation of the efficiency of vitamin B6 supplementation for McArdle disease by follow-up muscle biopsy. Muscle Nerve. 45, 436–440 (2012)
Cori, C.F., Cori, G.T.: Carbohydrate metabolism. Annu. Rev. Biochem. 10, 151–180 (1941)
Voet D., Voet J.D.: Biochemistry (third edition) pp. 626–656. John Wiley & Sons Inc., Hoboken (2004)
Krebs, E.G., Love, D.S., Bratvold, G.E., Trayser, K.A., Meyer, W.L., Fischer, E.H.: Purification and properties of rabbit skeletal muscle phosphorylase b kinase. Biochemistry. 3, 1022–1033 (1964)
Miyagawa, D., Makino, Y., Sato, M.: Sensitive, nonradioactive assay of phosphorylase kinase through measurement of enhanced phosphorylase activity towards fluorogenic dextrin. J. Biochem. 159, 239–246 (2016)
Lowry, O.H., Schult, D.W., Passonneau, J.V.: Effects of adenylic acid on the kinetics of muscle phosphorylase a. J. Biol. Chem. 239, 1947–1953 (1964)
Engers, H.D., Madsen, N.B.: The effect of anions on the activity of phosphorylase b. Biochem. Biophys. Res. Commun. 33, 49–54 (1968)
Yunis, A.A., Assaf, S.A.: Purification and properties of glycogen phosphorylase from bovine corpus luteum. Kinetics of salt activation. Biochemistry. 9, 4381–4388 (1970)
Stalmans, W., Hers, H.G.: The stimulation of liver phosphorylase b by AMP, fluoride and sulfate. Eur. J. Biochem. 54, 341–350 (1975)
Leonidas, D.D., Oikonomakos, N.G., Papageorgiou, A.C., Xenakis, A., Cazianis, C.T., Bem, F.: The ammonium sulfate activation of phosphorylase b. FEBS Lett. 261, 23–27 (1990)
Zographos, S.E., Oikonomakos, N.G., Dixon, H.B.F., Griffin, W.G., Johnson, L.N., Leonidas, D.D.: Sulfate-activated phosphorylase b: the pH-dependence of catalytic activity. Biochem. J. 310, 565–570 (1995)
Sprang, S.R., Withers, S.G., Goldsmith, E.J., Fletterick, R.J., Madsen, N.B.: Structural basis for the activation of glycogen phosphorylase b by adenosine monophosphate. Science. 254, 1367–1371 (1991)
Makino, Y., Fujii, Y., Taniguchi, M.: Properties and functions of the storage sites of glycogen phosphorylase. J. Biochem. 157, 451–458 (2015)
Barford, D., Johnson, L.N.: The allosteric transition of glycogen phosphorylase. Nature. 340, 609–616 (1989)
Johnson, L.N., Hu, S.H., Barford, D.: Catalytic mechanism of glycogen phosphorylase. Faraday Discuss. 93, 131–142 (1992)
Leonidas, D.D., Oikonomakos, N.G., Papageorgiou, A.C., Acharya, K.R., Barford, D., Johnson, L.N.: Control of phosphorylase b conformation by a modified cofactor: crystallographic studies on R-state glycogen phosphorylase reconstituted with pyridoxal 5′-diphosphate. Protein Sci. 1, 1112–1122 (1992)
Lin, K., Hwang, P.K., Fletterick, R.J.: Distinct phosphorylation signals converge at the catalytic center in glycogen phosphorylases. Structure. 5, 1511–1523 (1997)
Sealock, R.W., Graves, D.J.: Effect of salt solutions on glycogen phosphorylase. A possible role of the phosphoryl group in phosphorylase a. Biochemistry. 6, 201–207 (1967)
Kasvinsky, P.J., Madsen, N.B., Fletterick, R.J., Sygusch, J.: X-ray crystallographic and kinetic studies of oligosaccharide binding to phosphorylase. J. Biol. Chem. 253, 1290–1296 (1978)
Mikami, B., Hehre, E.J., Sato, M., Katsube, Y., Hirose, M., Morita, Y., Sacchettini, J.C.: The 2.0-Å resolution structure of soybean β-amylase complexed with α-cyclodextrin. Biochemistry. 32, 6836–6845 (1993)
Okubo, M., Horinishi, A., Takeuchi, M., Suzuki, Y., Sakura, N., Hasegawa, Y., Igarashi, T., Goto, K., Tahara, H., Uchimoto, S., Omichi, K., Kanno, H., Hayasaka, K., Murase, T.: Heterogeneous mutations in the glycogen-debranching enzyme gene are responsible for glycogen storage disease type IIIa in Japan. Hum. Genet. 106, 108–115 (2000)
Guillén, D., Sánchez, S., Rodríguez-Sanoja, R.: Carbohydrate-binding domains: multiplicity of biological roles. Appl. Microbiol. Biotechnol. 85, 1241–1249 (2010)
Nakayama, A., Yamamoto, K., Tabata, S.: High expression of glycogen-debranching enzyme in Escherichia coli and its competent purification method. Protein Expr. Purif. 19, 298–303 (2000)
Totsuka, A., Fukazawa, C.: Affinity purification of β-amylase originating from plant using cyclomaltohexaose-immobilized Sepharose 6B in the presence of ammonium sulfate. Protein Expr. Purif. 4, 333–336 (1993)
Hase, S., Ikenaka, T., Matsushima, Y.: Structure analyses of oligosaccharides by tagging of the reducing end sugars with a fluorescent compound. Biochem. Biophys. Res. Commun. 85, 257–263 (1978)
Makino, Y., Omichi, K.: Acceptor specificity of 4-α-glucanotransferases of mammalian glycogen debranching enzymes. J. Biochem. 139, 535–541 (2006)
Nakamura, M., Makino, Y., Takagi, C., Yamagaki, T., Sato, M.: Probing the catalytic site of rabbit muscle glycogen phosphorylase using a series of specifically modified maltohexaose derivatives. Glycoconj. J. 34, 563–574 (2017)
Vretblad, P.: Immobilization of ligands for biospecific affinity chromatography via their hydroxyl group: the cyclohexaamylose-β-amylase system. FEBS Lett. 47, 86–89 (2000)
Fiske, C.H., Subbarow, Y.: The colorimetric determination of phosphorus. J. Biol. Chem. 66, 375–400 (1925)
Saheki, S., Takeda, A., Shimazu, T.: Assay of inorganic phosphate in the mild pH range, suitable for measurement of glycogen phosphorylase activity. Anal. Biochem. 148, 277–281 (1985)
Ishimizu, T., Hashimoto, C., Takeda, R., Fujii, K., Hase, S.: A novel α1,2-L-fucosidase acting on xyloglucan oligosaccharides is associated with endo-β-mannosidase. J. Biochem. 142, 721–729 (2007)
Natsuka, S., Masuda, M., Sumiyoshi, W., Nakakita, S.: Improved method for drawing of a glycan map, and the first page of glycan atlas, which is a compilation of glycan maps for a whole organism. PLoS One. 9, e102219 (2014)
Makino, Y., Omichi, K.: Sensitive assay of glycogen phosphorylase activity by analysing the chain-lengthening action on a fluorogenic maltooligosaccharide derivative. J. Biochem. 146, 71–76 (2009)
Pinotsis, N., Leonidas, D.D., Chrysina, E.D., Oikonomakos, N.G., Mavridis, I.M.: The binding of β- and γ-cyclodextrins to glycogen phosphorylase b: kinetic and crystallographic studies. Protein Sci. 12, 1914–1924 (2003)
Zhang, Y., Cremer, P.S.: Interactions between macromolecules and ions: the Hofmeister series. Curr. Opin. Chem. Biol. 10, 658–663 (2006)
Yang, Z.: Hofmeister effects: an explanation for the impact of ionic liquids on biocatalysis. J. Biotechnol. 144, 49–54 (2009)
Philip, G., Gringel, G., Palm, D.: Rabbit muscle phosphorylase derivatives with oligosaccharides covalently bound to the glycogen storage site. Biochemistry. 21, 3043–3050 (1982)
Madsen, N.B., Shechosky, S., Fletterick, R.J.: Site-site interactions in glycogen phosphorylase b probed by ligands specific for each site. Biochemistry. 22, 4460–4465 (1983)
Buchbinder, J.L., Rath, V.L., Fletterick, R.J.: Structural relationships among regulated and unregulated phosphorylases. Annu. Rev. Biophys. Biomol. Struct. 30, 191–209 (2001)
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declare no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Rights and permissions
About this article
Cite this article
Fujii, Y., Makino, Y. & Sato, M. A new interpretation of sulfate activation of rabbit muscle glycogen phosphorylase. Glycoconj J 35, 299–309 (2018). https://doi.org/10.1007/s10719-018-9823-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10719-018-9823-x