Iminosugars as potential inhibitors of glycogenolysis: Structural insights into the molecular basis of glycogen phosphorylase inhibition

Journal of Medicinal Chemistry

Volumn 49, Issue 19, 2006, Pages 5687-5701

  Oikonomakos, Nikos G ^a   Tiraidis, Costas ^a   Leonidas, Demetres D ^a   Zographos, Spyros E ^a   Kristiansen, Marit ^b   Jessen, Claus U ^b   Nørskov Lauritsen, Leif ^b   Agius, Loranne ^c  

^a INSTITUTE OF BIOLOGY   (Greece)

^b NOVO NORDISK A S   (Denmark)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIDEOXY 1,4 IMINOARABINITOL; 2 HYDROXYMETHYLPYRROLIDINE 3,4 DIOL; 5 HYDROXYMETHYL 1 (3 PHENYLPROPYL) 3,4 PIPERIDINEDIOL; CARBONYL DERIVATIVE; ENZYME INHIBITOR; GLUCAGON; GLYCOGEN PHOSPHORYLASE; HISTIDINE; IMINO ACID; ISOFAGOMINE; NNC 42 1007; PHOSPHATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; GLYCOGENOLYSIS; HYDROGEN BOND; IC 50; ION TRANSPORT; LIVER CELL; NONHUMAN; X RAY CRYSTALLOGRAPHY;

ANIMALS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GLUCOSEPHOSPHATES; GLYCOGEN PHOSPHORYLASE; GLYCOGENOLYSIS; IMINO SUGARS; KINETICS; LIVER; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; RABBITS; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 33748871491     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm060496g     Document Type: Article

References (84)

1. McCormack, J. C.; Westergaard, N.; Kristiansen, M.; Brand, C. L.; Lau, J. Pharmacological approaches to inhibit endogenous glucose production as a means of anti-diabetic therapy. Curr. Pharm. Des. 2001, 7, 1451-1474.
2. Treadway, J. L.; Mendys, P.; Hoover, D. J. Glycogen phosphorylase inhibitors for treatment of type 2 diabetes mellitus. Expert Opin. Invest. Drugs 2001, 10, 439-454.
3. Newgard, C. B.; Hwang, P. K.; Fletterick, R. J. The family of glycogen phosphorylases: structure and function. Crit. Rev. Biochem. Mol. Biol. 1989, 24, 69-99.
4. Johnson, L. N. Glycogen phosphorylase: control by phosphorylation and allosteric effectors. FASEB J. 1992, 6, 2274-2282.
5. Oikonomakos, N. G.; Acharya, K. R.; Johnson, L. N. Rabbit muscle glycogen phosphorylase (b) the structural basis of activation and catalysis (review). In Posttranslational Modification of Proteins; Harding, J. J., Crabbe, M. J. C, Eds.; CRC Press, Inc.; Boca Raton, Florida, 1992; pp 81-151.
6. Alemany, S.; Cohen, P. Phosphorylase a is an allosteric inhibitor of the glycogen and microsomal form of rat hepatic protein phosphatase 1. FEBS Lett. 1986, 198, 194-202.
7. Bollen, M.; Stalmans, W. The structure, role, and regulation of type 1 protein phosphatase. Crit. Rev. Biochem. Mol. Biol. 1992, 27, 227-281.
8. Aiston, S.; Green, A.; Mukhtar, M.; Agius, L. Glucose-6-phosphate causes translocation of phosphorylase in hepatocytes and inactivates the enzyme synergistically with glucose. Biochem. J. 2004, 377, 195-204.
9. Aiston, S.; Hampson, L.; Gómez-Foix, A. M.; Guinovart, J. J.; Agius, L. Hepatic glycogen synthesis is highly sensitive to phosphorylase activity. J. Biol. Chem. 2001, 276, 23858-23866.
10. Latsis, T.; Andersen, B.; Agius, L. Diverse effects of two allosteric inhibitors on the phosphorylation state of glycogen phosphorylase in hepatocytes. Biochem. J. 2002, 368, 309-316.
11. Aiston, S.; Coghlan, M. P.; Agius, L. Inactivation of phosphorylase is a major component of the mechanism by which insulin stimulates hepatic glycogen synthesis. Eur. J. Biochem. 2003, 270, 2773-2781.
12. Kristiansen, M.; Andersen, B.; Iversen, L. F.; Westergaard, N. Identification, synthesis, and characterization of new glycogen phosphorylase inhibitors binding to the allosteric AMP site. J. Med. Chem. 2004, 47, 3537-3545.
13. Klabunde, T.; Wendt, U. K.; Kadereit, D.; Brachvogel, V.; Burger, H.-J.; Herling, A. W.; Oikonomakos, N. G.; Kosmopoulou, M. N.; Schmoll, D.; Sarubbi, E.; von Roedern, E.; Schönafinger, K.; Defossa, E. Acyl ureas as human liver glycogen phosphorylase inhibitors for the treatment of type 2 diabetes. J. Med. Chem. 2005, 48, 6178-6193.
14. Baker, D. J.; Greenhaff, P. L.; Timmons, J. A. Glycogen phosphorylase inhibition as a therapeutic target: a review of the recent patent literature. Expert Opin. Ther. Pat. 2006, 16, 459-466.
15. Fosgerau, K.; Mittelman, S. D.; Sunehag, A.; Dea, M. K.; Lundgren, K.; Bergman, R. N. Lack of hepatic "inter-regulation" during inhibition of glycogenolysis in a canine model. Am. J. Physiol. 2001, 281, E375-E383.
16. Oikonomakos, N. G. Glycogen phosphorylase as a molecular target for type 2 diabetes therapy. Curr. Protein Pept. Sci. 2000, 3, 561-586.
17. Kurukulasuriya, R.; Link, J. T.; Madar, D. J.; Pei, Z.; Richards, S. J.; Rohde, J. J.; Souers, A. J.; Szczepankiewicz, B. G. Potential drug targets and progress towards pharmacologic inhibition of hepatic glucose production. Curr. Med. Chem. 2003, 10, 123-153.
18. Lu, Z.; Bohn, J.; Bergeron, R.; Deng, Q.; Ellsworth, K. P.; Geissler, W. M.; Harris, G.; McCann, P. E.; McKeever, B.; Myers, R. W.; Saperstein, R.; Willoughby, C. A.; Yao, J.; Chapman, K. A new class of glycogen phosphorylase inhibitors. Bioorg. Med. Chem. Lett. 2003, 13, 4125-4128.
19. Ogawa, A. K.; Willoughby, C. A.; Bergeron, R.; Ellsworth, K. P.; Geissler, W. M.; Myers, R. W.; Yao, J.; Harris, G.; Chapman, K. T. Glucose-lowering in a db/db mouse model by dihydropyridine diacid glycogen phosphorylase inhibitors. Bioorg. Med. Chem. Lett. 2003, 13, 3405-3408.
20. Somsák, L.; Nagy, V.; Hadady, Z.; Docsa, T.; Gergely, P. Glucose analogue inhibitors of glycogen phosphorylases as potential antidiabetic agents: recent developments. Curr. Pharm. Des. 2003, 9, 1177-1189.
21. Oikonomakos, N. G.; Kosmopoulou, M. N.; Chrysina, E. D.; Leonidas, D. D.; Kostas, I. D.; Wendt, K. U.; Klabunde, T.; Defossa, E. Crystallographic studies on acyl ureas, a new class of glycogen phosphorylase inhibitors, as potential antidiabetic drugs. Protein Sci. 2005, 14, 1760-1771.
22. Somsák, L.; Nagy, V.; Hadady, Z.; Felföldi, N.; Docsa, T.; Gergely, P. Recent developments in the synthesis and evaluation of glucose analogue inhibitors of glycogen phosphorylases as potential antidiabetic agents. In Frontiers in Medicinal Chemistry; Reitz, A. B., Kordik, C. P., Choudhary, M. I., Atta ur Rahman, Eds; Bentham: Pennington, NJ, 2005; Vol. 2, pp 253-272.
23. Wright, S. W.; Rath, V. L.; Genereux, P. E.; Hageman, D. L.; Levy, C. B.; McLure, L. D.; McCoid, S. C.; McPherson, R. K.; Schelhorn, T. M.; Wilder, D. E.; Zavadoski, W. J.; Gibbs, E. M.; Treadway, J. L. 5-Chloroindoloyl glycine amide inhibitors of glycogen phosphorylase: synthesis, in vitro, in vivo, and X-ray crystallographic characterization. Bioorg. Med. Chem. Lett. 2005, 15, 459-465.
24. Martin, J. L.; Veluraja, K.; Johnson, L. N.; Fleet, G. W. J.; Ramsden, N. G.; Bruce, I.; Orchard, M.; Oikonomakos, N. G.; Papageorgiou, A. C.; Leonidas, D. D.; Tsitura, H. S. Glucose analogue inhibitors of glycogen phosphorylase: the design of potential drugs for diabetes. Biochemistry 1991, 30, 10101-10116.
25. Watson, K. A.; Mitchell, E. P.; Johnson, L. N.; Son, J. C.; Bichard, C. J. F.; Orchard, M. G.; Fleet, G. W. J.; Oikonomakos, N. G.; Leonidas, D. D.; Kontou, M.; Papageorgiou, A. C. Design of inhibitors of glycogen phosphorylase: a study of α and β-C-glucosides and 1-thio-β-D-glucose compounds. Biochemistry 1994, 33, 5745-5758.
26. Bichard, C. J. F.; Mitchell, E. P.; Wormald, M. R.; Watson, K. A.; Johnson, L. N.; Zographos, S. E.; Koutra, D. D.; Oikonomakos, N. G.; Fleet, G. W. J. Potent inhibition of glycogen phosphorylase by a spirohydantoin of glucopyranose: first pyranose analogues of hydantocidin. Tetrahedron Lett. 1995, 36, 2145-2148.
27. Oikonomakos, N. G.; Kontou, M.; Zographos, S. E.; Watson, K. A.; Johnson, L. N.; Bichard, C. J. F.; Fleet, G. W. J.; Acharya, K. R. N-acetyl-β-D- glucopyranosylamine: a potent T state inhibitor of glycogen phosphorylase. A comparison with α-D-glucose. Protein Sci. 1995, 4, 2469-2477.
28. Watson, K. A.; Mitchell, E. P.; Johnson, L. N.; Cruciani, G.; Son, J. C.; Bichard, C. J. F.; Fleet, G. W. J.; Oikonomakos, N. G.; Kontou, M.; Zographos, S. E. Glucose analogue inhibitors of glycogen phosphorylase: from crystallographic analysis to drug prediction using GRID force-field and GOLPE variable selection. Acta Crystallogr. 1995, D51, 458-472.
29. Gregoriou, M.; Noble, M. E. M.; Watson, K. A.; Garman, E. F.; Krülle, T. M.; Fuente, C.; Fleet, G. W. J.; Oikonomakos, N. G.; Johnson, L. N. The structure of a glycogen phosphorylase glucopyranose spirohydantoin complex at 1.8 Å resolution and 100 K: the role of the water structure and its contribution to binding. Protein Sci. 1998, 7, 915-927.
30. Somsák, L.; Kovács, L.; Tóth, M.; Õsz, E.; Szilágyi, L.; Györgydeák, Z.; Dinya, Z.; Docsa, T.; Tóth, B.; Gergely, P. Synthesis of and a comparative study on the inhibition of muscle and liver glycogen phosphorylases by epimeric pairs of D-gluco- and D-xylopyranosylidene-spiro-(thio)hydantoins and N-(D-glucopyranosyl) amides. J. Med. Chem. 2001, 44, 2843-2848.
31. Oikonomakos, N. G.; Skamnaki, V. T.; Õsz, E.; Szilágyi, L.; Somsák L.; Docsa, T.; Tóth, B.; Gergely, P. Kinetic and crystallographic studies of glucopyranosylidene spirothiohydantoin binding to glycogen phosphorylase b. Bioorg. Med. Chem. 2002, 10, 261-268.
32. Oikonomakos, N. G.; Kosmopoulou, M.; Zographos, S. E.; Leonidas, D. D.; Chrysina, E. D.; Somsák L.; Nagy, V.; Praly, J.-P.; Docsa, T.; Tóth, B.; Gergely, P. Binding of N-acetyl-N′-β-D- glucopyranosyl urea and N-benzoyl-N′-β-D-glucopyranosyl urea to glycogen phosphorylase b: Kinetic and crystallographic studies. Eur. J. Biochem. 2002, 269, 1-13.
33. Chrysina, E. D.; Oikonomakos, N. G.; Zographos, S. E.; Kosmopoulou, M. N.; Bischler, N.; Leonidas, D. D.; Kovács, L.; Docsa, T.; Gergely, P.; Somsák, L. Crystallographic studies on α- and β-D- glucopyranosyl formamide analogues, inhibitors of glycogen phosphorylase. Biocatal. Biotransform. 2003, 21, 233-242.
34. Györgydeák, Z.; Hadady, Z.; Felföldi, N.; Krakomperger, A.; Nagy, V.; Tóth, M.; Brunyánszki, A.; Docsa, T.; Gergely, P.; Somsák, L. Synthesis of N-(beta-D-glucopyranosyl)- and N-(2-acetamido-2-deozy-beta-D-glucopyranosyl) amides as inhibitors of glycogen phosphorylase. Bioorg. Med. Chem. 2004, 12, 4861-4870.
35. Chrysina, E. D.; Kosmopoulou, M. N.; Kardakaris, R.; Bischler, N.; Leonidas, D. D.; Kannan, T.; Loganathan, T.; Oikonomakos, N. G. Binding of β-D-glucopyranosyl bismethoxyphosphoramidate to glycogen phosphorylase (b) kinetic and crystallographic studies. Bioorg. Med. Chem. 2005, 13, 765-772.
36. Chrysina, E. D.; Kosmopoulou, M. N.; Tiraidis, C.; Kardakaris, R.; Bischler, N.; Leonidas, D. D.; Hadady, Z.; Somsák, L.; Docsa, T.; Gergely, P.; Oikonomakos, N. G. Kinetic and crystallographic studies on 2-(β-D-glucopyranosyl)-5-methyl-1,3,4-oxadiazole, -benzothiazole, and -benzimidazole, inhibitors of muscle glycogen phosphorylase b. Evidence for a new binding site. Protein Sci. 2005, 14, 873-888.
37. Watson, K. A.; Chrysina, E. D.; Tsitsanou, K. E.; Zographos, S. E.; Archontis, G.; Fleet, G. W. J.; Oikonomakos, N. G. Kinetic and crystallographic studies of glucopyranose spirohydantoin and glucopyranosylamine analogues inhibitors of glycogen phosphorylase. Proteins 2005, 61, 966-983.
38. Johnson, L. N.; Acharya, K. R.; Jordan, M. D.; McLaughlin, P. J. Refined crystal structure of the phosphorylase heptulose-2-phosphate oligosaccharide-AMP complex. J. Mol. Biol. 1990, 211, 645-661.
39. Barford, D.; Johnson, L. N. The allosteric transition of glycogen phosphorylase. Nature (London) 1989, 340, 609-614.
40. Watson, K. A.; McCleverty, C.; Geremia, S.; Cottaz, S.; Driguez, H.; Johnson, L. N. Phosphorylase recognition and phosphorolysis of its oligosaccharide substrate: answers to a long outstanding question. EMBO J. 1999, 18, 4619-4632.
41. Lillelund, V. H.; Jensen, H. H.; Liang, X.; Bols, M. Recent developments of transition-state analogue glycosidase inhibitors of nonnatural product origin. Chem. Rev. 2002, 102, 515-553.
42. Zechel, D. L.; Boraston, A. B.; Gloster, T.; Boraston, C. M.; Macdonald, J. M.; Tilbrook, D. M. G.; Stick, R. V.; Davies, G. J. Iminosugar glycosidase inhibitors: structural and thermodynamic dissection of the binding of isofagomine and 1-deoxynojirimycin to β-D-glucosidases. J. Am. Chem. Soc. 2003, 125, 14313-14323.
43. Ariki, M.; Fukui, T. Affinity of glucose analogues for alpha-glucan phosphorylases from rabbit muscle and potato tubers. J. Biochem. (Tokyo) 1977, 81, 1017-1024.
44. Mitchell, E. P.; Withers, S. G.; Ermert, P.; Vasella, A. T.; Garman, E. F.; Oikonomakos, N. G.; Johnson, L. N. Ternary complex crystal structures of glycogen phosphorylase with a transition state analogue nojirimycin tetrazole and phosphate in the T and R states. Biochemistry 1996, 35, 7341-7355.
45. Heightman, T. D.; Vasella, A.; Tsitsanou, K. E.; Zographos, S. E.; Skamnaki, V. T.; Oikonomakos, N. G. Cooperative interactions of the catalytic nucleophile and the catalytic acid in the inhibition of β-glycosidases. Calculations and their validation by comparative kinetic and structural studies of the inhibition of glycogen phosphorylase b. Helv. Chem. Acta 1998, 81, 853-864.
46. Andersen, B.; Rassov, A.; Westergaard, N.; Lundgren, K. Inhibition of glycogenolysis in primary rat hepatocytes by 1,4-dideoxy-1,4-imino-D-arabinitol. Biochem. J. 1999, 342, 545-550.
47. Fosgerau, K.; Westergaard, N.; Quistorff, B.; Grunnet, N.; Kristiansen, M.; Lundgren, K. Kinetic and functional characterization of 1,4-dideoxy-1,4- imino-D-arabinitol: a potent inhibitor of glycogen phosphorylase with anti-hyperglycaemic effect in ob/ob mice. Arch. Biochem. Biophys. 2000, 15, 274-284.
48. Lundgren, K.; Rassov, A.; Bols, M. NNC 42-1007 is a novel, potent inhibitor of hepatic glycogen phosphorylase, and of hepatocyte glycogenolysis. Diabetes 1996, 45 (Suppl 12), 521.
49. Jakobsen, P.; Lundbeck, J. M.; Kristiansen, M.; Breinholt, J.; Demuth, H.; Pawlas, J.; Candela, M. P.; Andersen, B.; Westergaard, N.; Lundgren, K.; Asano, N. Iminosugars: Potential inhibitors of liver glycogen phosphorylase. Bioorg. Med. Chem. 2001, 9, 733-744.
50. Overkleeft, H. S.; van Wittenburg, J.; Pandit, U. K. A facile transformation of sugar lactones to azasugars. Tetrahedron 1994, 50, 4215-4224.
51. Ayad, T.; Génisson, Y.; Broussy, S.; Baltas, M.; Gorrichon, L. A flexible route towards five-membered ring imino sugars and their novel 2-deoxy-2-fluoro analogues. Eur. J. Org. Chem. 2003, 15, 2903-2910.
52. Lundgren, K.; Kirk, O. Piperidines and pyrrolidines. WO 95/24391 September 14, 1995.
53. Hajdu, J.; Acharya, K. R.; Stuart, D. I.; McLaughlin, P. J.; Barford, D.; Oikonomakos, N. G.; Klein, H. W.; Johnson, L. N. Catalysis in the crystal: synchrotron radiation studies with glycogen phosphorylase (b). EMBO J. 1987, 6, 539-546.
54. Notenboom, V.; Williams, S. J.; Hoos, R.; Withers, S. G.; Rose, D. R. Detailed structural analysis of glycosidase/inhibitor interactions: complexes of Cex from Cellulomonas fimi with xylobiose-derived aza-sugars. Biochemistry 2000, 39, 11553-11563.
55. Mark, B. L.; Vocadlo, D. J.; Zhao, D.; Knapp, S.; Withers, S. G.; James, M. N. G. Biochemical and structural assessment of the 1 -N-aza-sugar galNac-isofagomine as a potent family 20 β-N-acetylhexosaminidase inhibitor. J. Biol. Chem. 2001, 276, 42131-42137.
56. Kuntz, D. A.; Ghavami, A.; Johnston, B. D.; Pinto, B. M.; Rose, D. R. Crystallographic analysis of the interactions of Drosophila melanogaster Golgi α-mannosidase II with the naturally occurring glycomimetic salacinol and its analogues. Tetrahedron: Asymmetry 2005, 16, 25-32.
57. Anagnostou, E.; Kosmopoulou, M. N.; Chrysina, E. D.; Leonidas, D. D.; Hadjiloi, T.; Tiraidis, C.; Györgydeák, Z.; Somsák, L.; Docsa, T.; Gergely, P.; Oikonomakos, N. G. Crystallographic studies on two bioisosteric analogues, N-acetyl-β-D-glucopyranosylamine and N-trifluoracetyl-β-D-glucopyranosylamine, potent inhibitors of muscle glycogen phosphorylase. Bioorg. Med. Chem. 2006, 14, 181-189.
58. Hadjiloi, T.; Tiraidis, C.; Chrysina, E. D.; Leonidas, D. D.; Oikonomakos, N. G.; Tsipos, P.; Gimisis, T. Binding of oxalyl derivatives of β-D-glucopyranosylamine to muscle glycogen phosphorylase b. Bioorg. Med. Chem. 2006, 14, 3872-3882.
59. Somsák, L.; Nagy, V.; Docsa, T.; Tóth, B.; Gergely, P. Gram-scale synthesis of a glucopyranosylidene-spiro-thiohydantoin and its effect on hepatic glycogen metabolism studied in vitro and in vivo. Tetrahedron: Asymmetry 2000, 11, 405-408.
60. McLaughlin, P. J.; Stuart, D. I.; Klein, H. W.; Oikonomakos, N. G.; Johnson, L. N. Substrate-cofactor interactions for glycogen phosphorylase b: a binding study in the crystal with heptenitol and heptulose-2-P. Biochemistry 1984, 23, 5862-5873.
61. Barford, D.; Hu, S. H.; Johnson, L. N. Structural mechanism for glycogen phosphorylase control by phosphorylation and AMP. J. Mol. Biol. 1991, 218, 233-260.
62. Leonidas, D. D.; Oikonomakos, N. G.; Papageorgiou, A. C.; Acharya, K. R.; Barford, D.; Johnson, L. N. Control of phosphorylase b by a modified cofactor: Crystallographic studies on R-state glycogen phosphorylase reconstituted with pyridoxal 5′-diphosphate. Protein Sci. 1992, 1, 1112-1122.
63. Sprang, S. R.; Madsen, N. B.; Withers, S. G. Multiple phosphate positions in the catalytic site of glycogen phosphorylase: structure of the pyridoxal-5′-pyrophosphate coenzyme-substrate analogue. Protein Sci. 1992, 1, 1100-1111.
64. O'Reilly, M.; Watson, K. A.; Schinzel, R.; Palm, D.; Johnson, L. N. Oligosaccharide substrate binding to E. coli maltodextrin phosphorylase. Nat. Struct. Biol. 1997, 4, 405-412.
65. O'Reilly, M.; Watson, K. A.; Johnson, L. N. The crystal structure of the E. coli maltodextrin phosphorylase-acarbose complex. Biochemistry 1999, 38, 5337-5345.
66. Geremia, S.; Campagnolo, M.; Schinzel, R.; Johnson, L. N. Enzymatic catalysis in crystals of Escherichia coli maltodextrin phosphorylase. J. Mol. Biol. 2002, 322, 413-423.
67. Fisher, B. M.; Schultz, L. W.; Raines, R. T. Coulombic effects of remote subsites on the active site of ribonuclease A. Biochemistry 1998, 37, 17386-17401.
68. Bergans, N.; Stalmans, W.; Goldmann, S.; Vanstapel, F. Molecular mode of inhibition of glycogenolysis in rat liver by the dihydropyridine derivative, BAY R3401: inhibition and inactivation of glycogen phosphorylase by an activated metabolite. Diabetes 2000, 49, 1419-1426.
69. Martin, W. H.; Hoover, D. J.; Armento, S. J.; Stock, I. A.; McPherson, R. K.; Danley, D. E.; Stevenson, R. W.; Barrett, E. J.; Treadway J. L. Discovery of a human glycogen phosphorylase inhibitor that lowers blood glucose in vivo. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 1776-1781.
70. Bollen, M.; Keppens, S.; Stalmans, W. Specific features of glycogen metabolism. Biochem. J. 1998, 336, 19-31.
71. Zographos, S. E.; Oikonomakos, N. G.; Tsitsanou, K. E.; Leonidas, D. D.; Chrysina, E. D.; Skamnaki, V. T.; Bischoff, H.; Goldman, S.; Schram, M.; Watson, K. A.; Johnson, L. N. The structure of glycogen phosphorylase b with an alkyl-dihydropyridine-dicarboxylic acid compound, a novel and potent inhibitor. Structure 1997, 5, 1413-1425.
72. Hoover, D. J.; Lefkowitz-Snow, S.; Burgess-Henry, J. L.; Martin, W. H.; Armento, S. J.; Stock, I. A.; McPherson, R. K.; Genereaux, P. E.; Gibbs, E. M.; Treadway, J. L. Indole-2-carboxamide inhibitors of human liver glycogen phosphorylase. J. Med. Chem. 1998, 41, 2934-2938.
73. Oikonomakos, N. G.; Skamnaki, V. T.; Tsitsanou, K. E.; Gavalas, N. G.; Johnson L. N. A new allosteric site in glycogen phosphorylase b as a target for drug interactions. Structure 2000, 8, 575-584.
74. Rath, V. L.; Ammirati, M.; Danley, D. E.; Ekstrom, J. L.; Gibbs, E. M.; Hynes, T. R.; Mathiowetz, A. M.; McPherson, R. K.; Olson, T. V.; Treadway, J. L.; Hoover, D. J. Human liver glycogen phosphorylase inhibitors bind at a new allosteric site. Chem. Biol. 2000, 7, 677-682.
75. Kagan, F.; Rebenstorf, M. A.; Heinzelman, R. V. The preparation of glycamines. J. Am. Chem. Soc. 1957, 79, 3541-3544.
76. Oikonomakos, N. G.; Melpidou, A. E.; Johnson, L. N. Crystallization of pig skeletal phosphorylase (b): purification, physical and catalytic characterization. Biochim. Biophys. Acta 1985, 832, 248-256.
77. Otwinowski, Z.; Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276, 307-326.
78. Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Refinement of macromolecular structures by the Maximum-Likelihood Method. Acta Crystallogr. 1997, D53, 240-255.
79. Jones, T. A.; Zou, J. Y.; Cowan, S. W.; Kjeldgaard, M. Improved methods for the building of protein models in electron density maps and the location of errors in these models. Acta Crystallogr. 1991, A47, 110-119.
80. 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. Crystallogr. 1993, 26, 283-291.
81. Collaborative Computational Project No 4. The CCP4 suite: Programs for Protein Crystallography. Acta Crystallogr. 1994, D50, 760-763.
82. Hubbard, S. J.; Thornton, J. M. NACCESS, computer program, Department of Biochemistry and Molecular Biology, University College London: London, 1993.
83. Kraulis, P. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 1991, 24, 946-950.
84. Merritt, E. A.; Bacon, D. J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 1997, 277, 505-524.