Bisphosphonate inhibition of phosphoglycerate kinase: Quantitative structure-activity relationship and pharmacophore modeling investigation

Journal of Medicinal Chemistry

Volumn 49, Issue 23, 2006, Pages 6692-6703

  Kotsikorou, Evangelia ^a   Sahota, Gurmukh ^b   Oldfield, Eric ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BISPHOSPHONIC ACID DERIVATIVE; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE KINASE INHIBITOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CRYSTALLOGRAPHY; DRUG ACTIVITY; DRUG PROTEIN BINDING; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; GLYCOLYSIS; HUMAN; HYDROPHOBICITY; IC 50; MOLECULAR MODEL; NONHUMAN; PHARMACOPHORE; PREDICTION; QUANTITATIVE STRUCTURE ACTIVITY RELATION; SEQUENCE HOMOLOGY; SPECIES COMPARISON; THREE DIMENSIONAL IMAGING; TRYPANOSOMA;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CONSERVED SEQUENCE; DIPHOSPHONATES; ELECTROSTATICS; GLYCOLYSIS; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; PHOSPHOGLYCERATE KINASE; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; TRYPANOCIDAL AGENTS; TRYPANOSOMA BRUCEI BRUCEI;

EID: 33751019465     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm0604833     Document Type: Article

References (48)

1. Bressi, J. C.; Choe, J.; Hough, M. T.; Buckner, F. S.; Van Voorhis, W. C.; Verlinde, C. L. M. J.; Hol, W. G. J.; Gelb, M. H. Adenosine analogues as inhibitors of Trypanoma brucei phosphoglycerate kinase: Elucidation of a novel binding mode for a 2-amino-N6-substituted adenosine. J. Med. Chem. 2000, 43, 4135-4150 .
2. Bakker, B. M.; Michels, P. A. M.; Opperdoes, F. R.; Westerhoff, H. V. Glycolysis in bloodstream form Trypanosoma brucei can be understood in terms of the kinetics of the glycolytic enzymes. J. Biol. Chem. 1997, 272, 3207-3215.
3. Bakker, B. M.; Michels, P. A. M.; Opperdoes, F. R.; Westerhoff, H. V. What controls glycolysis in bloodstream form Trypanosoma brucei. J. Biol. Chem. 1998, 274, 14551-14559.
4. Bellingham. A. J.; Detter, J. C.; Lenfant, C. Regulatory mechanisms of hemoglobin oxygen affinity in acidosis and alkalosis. J. Clin. Invest. 1971, 50, 700-706.
5. Benesch, R. E.; Benesch, R.; Yu. C. I. The oxygenation of hemoglobin in the presence of 2,3-diphosphoglycerate. Effect of temperature. pH, ionic strength, and hemoglobin concentration. Biochemistry 1969, 8, 2567-2571.
6. McHarg, J.; Littlechild, J. A. Studies with inhibitors of the glycolytic enzyme phosphoglycerate kinase for potential treatment of cardiovascular and respiratory disorders. J. Pharm. Pharmacol. 1996, 48, 201-205.
7. Caplan, N. A.; Pogson, C. I.; Hayes, D. J.; Blackburn G. M. Novel bisphosphonate inhibitors of phosphoglycerate kinase. Bioorg. Med. Chem. Lett. 1998, 8, 515-520.
8. Jakeman, D. L.; Ivory, A. J.; Williamson, M. P.; Blackburn, G. M. Highly potent bisphosphonate ligands for phosphoglycerate kinase. J. Med. Chem. 1998, 41, 4439-4452.
9. Caplan, N. A.; Pogson, C. I.; Hayes, D. J.; Blackburn, G. M. The synthesis of novel bisphosphonates as inhibitors of phosphoglycerate kinase (3-PGK). J. Chem. Soc., Perkin Trans, 1 2000, 3, 421-437.
10. Blackburn, G. M.; England, D. A.; Kolkmann, F. Monofluoro- and difluoro-methylenebisphosphonic acids: isopolar analogues of pyrophosphoric acid. J. Chem. Soc., Chem. Commun. 1981, 930-932.
11. Thatcher, G. R. J.; Campbell, A. S. Phosphonates as mimics of phosphate biomolecules: ab initio calculations on tetrahedral ground states and pentacoordinate intermediates for phosphoryl transfer. J. Org. Chem. 1993, 58, 2272-2281.
12. Yardley, V.; Khan, A. A.; Martin, M. B.; Slifer, T. R.; Araujo, F. G.; Moreno, S. N.; Docampo, R.; Croft, S. L.; Oldfield, E. In vivo activities of farnesyl pyrophosphate synthase inhibitors against Leishmania donovani and Toxoplasma gondii. Antimicrob. Agents Chemother. 2002, 46, 929-931.
13. Rodriguez, N.; Bailey, B. N.; Martin, M. B.; Oldfield, E.; Urbina, J. A.; Docampo, R. Radical cure of experimental cutaneous leishmaniasis by the bisphosphonate pamidronate. J. Infect. Dis. 2002, 186, 138-140.
14. Martin, M. B.; Grimley, J. S.; Lewis, J. C.; Heath, H. T., 3rd; Bailey, B. N.; Kendrick, H.; Yardley, V.; Caldera, A.; Lira, R.; Urbina, J. A.; Moreno, S. N.; Docampo, R.; Croft, S. L.; Oldfield, E. Bisphosphonates inhibit the growth of Trypanosoma brucei, Trypanosoma cruzi, Leishmania donovani, Toxoplasma gondii, and Plusmodium falciparum: a potential route to chemotherapy. J. Med. Chem. 2001, 44, 909-916.
15. Martin, M. B.; Sanders, J. M.; Kendrick, H.; de Luca-Fradley, K.; Lewis, J. C.; Grimley, J. S.; Van Brussel, E. M.; Olsen, J. R.; Meints, G. A.; Burzynska, A.; Katarski, P.; Croft, S. L.; Oldfield, E. Activity of bisphosphonates against Trypanosoma brucei rhodesiense. J. Med. Chem. 2002, 45, 2904-2914.
16. Sanders, J. M.; Gomez, A. O.; Mao, J.; Meints, G. A.; Van Brussel, E. M.; Burzynska, A.; Kafarski, P.; Gonzalez-Pacanowska, D.; Oldfield, E. 3-D QSAR investigations of the inhibition of Leishmania major farnesyl pyrophosphate synthase by bisphosphonates. J. Med. Chem. 2003, 46, 5171-5183.
17. Sanders, J. M.; Song, Y.; Chan, J. M.; Zhang, Y.; Jennings, S.; Kosztowski, T.; Odeh, S.; Flessner, R.; Schwerdtfeger, C.; Kotsikorou, E.; Melts, G. A.; Gomez, A. O.; Gonzalez-Pacanowska, D.; Raker, A. M.; Wang, H.; van Beek, E. R.; Papapoulos, S. E.; Morita, C. T.; Oldfield, E. Pyridinium-1-yl bisphosphonates are potent inhibitors of farnesyl diphosphate synthase and bone resorption. J. Med. Chem. 2005, 48, 2957-2963.
18. Hudock, M. P.; Sanz-Rodriguez, C. E.; Song, Y.; Chan, J. M.; Zhang, Y.; Odeh, S.; Kosztowski, T.; Leon-Rossell, A.; Concepcion, J. L.; Yardley, V.; Croft, S. L.; Urbina, J. A.; Oldfield, E. Inhibition of Trypanosoma cruzi hexokinase by bisphosphonates. J. Med. Chem. 2006, 49, 215-223.
19. Cramer, R. D., 3rd; Patterson, D. E.; Bunce, J. D. Recent advances in comparative molecular field analysis (CoMFA). Prog. Clin. Biol. Res. 1989, 291, 161-165.
20. Klebe, G.; Abraham, U.; Mietzner, T. Molecular similarity indices in a comparative analysis (CoMS1A) of drug molecules to correlate and predict their biological activity. J. Med. Chem. 1994, 37, 4130-4146.
21. Accelrys. Catalyst 4.8: Accelrys Inc.: San Diego, CA.
22. Tripos. SYBYL 7.0; Tripos Inc.: St. Louis. MO.
23. Powell, M. J. D. Restart procedures of the conjugate gradient method. Math Programming 1977, 12, 241-254.
24. Press, W. H. Numerical recipes in C: the art of scientific computing; Cambridge University Press: New York, 1988; p 324.
25. Gasteiger, J.; Marsili, M. Iterative partial equalization of orbital electronegativity-rapid access to atomic charges. Tetrahedron 1980, 36, 3219-3228.
26. Coodsell, D. S.; Morris, G. M.; Olson, A. J. Automated docking of flexible ligands: applications of AutoDock. J. Mol. Recognit. 1996, 9, 1-5.
27. Bernstein, B. E.; Michels, P. A.; Hol, W. G. Synergistic effects of substrate-induced conformational changes in phosphoglycerate kinase activation. Nature 1997, 385, 275-278.
28. Cheng, F.; Oldfield, E. Inhibition of isoprene biosynthesis pathway enzymes by phosphonates, bisphosphonates, and diphosphates. J. Med. Chem. 2004, 47, 5149-5158.
29. Hosfield, D. J.; Zhang, Y.; Dougan, D. R.; Brown, A.; Tari, L. W.; Swanson, R. V.; Finn, J. Structural basis for bisphosphonate-mediated inhibition of isoprenoid biosynthesis. J. Biol. Chem. 2004, 279, 8526-8529.
30. Gabelli, S. B.; McLellan, J. S.; Montalvetti, A.; Oldfield, E.; Docampo, R.; Amzel, L. M. Structure and mechanism of the farnesyl diphosphate synthase from Trypanosoma cruzi: implications for drug design. Proteins: Struct., Funct. Bioinf. 2006, 62, 80-88.
31. Rondeau, J.; Bitsch, F.; Bourgier, E.; Geiser, M.; Hemmig, R.; Kroemer, M.; Lehmann, S.; Ramage, P.; Rieffel, S.; Strauss, A.; Green, J. R.; Jahnke, W. Structural basis for the exceptional in vivo efficacy of bisphosphonate drugs. Chem. Med. Chem. 2006, 1, 267-273.
32. (a) Kavanagh, K. L.; Guo, K.; Wu, X.; Von Delft, F.; Arrowsmith, C.; Sundstrom, M.; Edwards, A.; Opperman, U. X-ray structure of farnesyl diphosphate synthase protein, PDB file IZW5.
33. (b) Kavanagh, K. L.; Guo, K.; Von Delft, F.; Arrowsmith, C.; Sundstrom, M.; Edwards, A.; Opperman, U. Human farnesyl diphosphate synthase complexed with Mg and risedronate, PDB file 1YV5.
34. Szilagyi, A. N.; Ghosh, M.; Garman, E.; Vas, M. A 1.8 Å resolution structure of pig muscle 3-phosphoglycerate kinase with bound MgADP and 3-phosphoglycerate in open conformation: new insight into the role of the nucleotide in domain closure. J. Mol. Biol. 2001, 306, 499-511.
35. Watson, H. C.; Walker, N. P.; Shaw, P. J.; Bryunt, T. N.; Wendell, P. L.; Fothergill, L. A.; Perkins, R. E.; Conroy, S. C.; Dobson, M. J.; Tuite, M. F.; Kingsman, A. J.; Kingsman, S. M. Sequence and structure of yeast phosphoglycerate kinase. EMBO J. 1982, 1, 1635-1640.
36. Szabo, C. M.; Oldfield, E. An investigation of bisphosphonate inhibition of a vacuolar proton-pumping pyrophosphatase. Biochem. Biophys. Res. Commun. 2001, 287, 468-473.
37. Szabo, C. M.; Matsumura, Y.; Fukura, S.; Martin, M. B.; Sanders, J. M.; Sengupta, S.; Cieslak, J. A.; Loftus, T. C.; Lea, C. R.; Lee, H. J.; Koohang, A.; Coates, R. M.; Sagami, H.; Oldfield, E. Inhibition of geranylgeranyl diphosphate synthase by bisphosphonates and diphosphates: a potential route to new bone antiresorption and antiparasitic agents. J. Med. Chem. 2002, 45, 2185-2196.
38. Szabo, C. M.; Martin, M. B.; Oldfield, E. An investigation of bone resorption and Dictyostelium discoideum growth inhibition by bisphosphonate drugs. J. Med. Chem. 2002, 45, 2894-2903.
39. Kotsikorou, E.; Oldfield, E. A quantitative structure-activity relationship and pharmacophore modeling investigation of aryl-X and heterocyclic bisphosphonates as bone resorption agents. J. Med. Chem. 2003, 46, 2932-2944.
40. Sanders, J. M.; Ghosh, S.; Chan, J. M.; Meints, G.; Wang, H.; Raker, A. M.; Song, Y.; Colantino, A.; Burzynska, A.; Kafarski, P.; Morita, C. T.; Oldfield, E. Quantitative structure-activity relationships for γδ T cell activation by bisphosphonates. J. Med. Chem. 2004, 47, 375-384.
41. Ling, Y.; Sahota, G.; Odeh, S.; Chan, J. M.; Araujo, F. G.; Moreno, S. N.; Oldfield, E. Bisphosphonate inhibitors of Toxoplasma gondii growth: in vitro, QSAR, and in vivo investigations. J. Med. Chem. 2005, 48, 3130-3140.
42. Kotsikorou, E.; Song, Y.; Chan, J. M.; Faelens, S.; Tovian, Z.; Broderick, E.; Bakalara, N.; Docampo, R.; Oldfield, E. Bisphosphonate inhibition of the exopolyphosphatase activity of the Trypanosoma brucei soluble vacuolar pyrophosphatase. J. Med. Chem. 2005, 48, 6128-6139.
43. Bush, B. L.; Nachbar, R. B., Jr. Sample-distance partial least squares: PLS optimized for many variables, with application to CoMFA. J. Comput.-Aided Mol. Des. 1993, 7, 587-619.
44. Burt, C. T. Phosphorus NMR in Biology; CRC Press: Boca Raton, FL, 1987.
45. Jakeman, D. L.; Ivory, A. J.; Blackburn, G. M.; Williamson, M. P. Orientation of 1,3-bisphosphoglycerate analogues bound to phosphoglycerate kinase. J. Biol. Chem. 2003, 278, 10957-10962.
46. Davies, G. J.; Gamblin, S. J.; Littlechild, J. A.; Dauter, Z.; Wilson, K. S.; Watson, H. C. Structure of the ADP complex of the 3-phosphoglycerate kinase from Bacillus stearothermophilus at 1.65 Å. Acta Crystallogr. 1994, D50, 202-209.
47. Harlos, K.; Vas, M.; Blake, C. F. Crystal structure of the binary complex of pig muscle phosphoglycerate kinase and its substrate 3-phospho-D-glycerate. Proteins: Struct., Funct., Genet. 1992, 12, 133-144.
48. Montalvetti, A.; Fernandez, A.; Sanders, J. M.; Ghosh, S.; van Brussel, E.; Oldfield, E.; Docampo, R. Farnesyl Pyrophosphate Synthase Is an Essential Enzyme in Trypanosoma brucei. J. Biol. Chem. 2003, 278, 17075-17083.