Protonation State and Hydration of Bisphosphonate Bound to Farnesyl Pyrophosphate Synthase

Journal of Medicinal Chemistry

Volumn 58, Issue 18, 2015, Pages 7549-7556

  Yokoyama, Takeshi ^a   Mizuguchi, Mineyuki ^a   Ostermann, Andreas ^b   Kusaka, Katsuhiro ^c   Niimura, Nobuo ^c   Schrader, Tabias E ^d   Tanaka, Ichiro ^c  

^a UNIVERSITY OF TOYAMA   (Japan)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c IBARAKI UNIVERSITY   (Japan)

^d FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE; FARNESYL DIPHOSPHATE; ISOPENTENYL DIPHOSPHATE; RISEDRONIC ACID; BONE DENSITY CONSERVATION AGENT; DEUTERIUM; GERANYLTRANSFERASE; HEMITERPENE; HYDROGEN; MAGNESIUM; ORGANOPHOSPHORUS COMPOUND; PROTON;

ARTICLE; BINDING AFFINITY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DRUG BINDING; HYDRATION; HYDROGEN BOND; PROTON TRANSPORT; X RAY DIFFRACTION; CHEMICAL STRUCTURE; CHEMISTRY; NEUTRON DIFFRACTION; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BONE DENSITY CONSERVATION AGENTS; CRYSTALLOGRAPHY, X-RAY; DEUTERIUM; GERANYLTRANSTRANSFERASE; HEMITERPENES; HYDROGEN; MAGNESIUM; MODELS, MOLECULAR; NEUTRON DIFFRACTION; ORGANOPHOSPHORUS COMPOUNDS; PROTEIN CONFORMATION; PROTONS; RISEDRONATE SODIUM;

EID: 84942362144     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/acs.jmedchem.5b01147     Document Type: Article

References (30)

1. Delmas, P. D. Treatment of postmenopausal osteoporosis Lancet 2002, 359, 2018-2026 10.1016/S0140-6736(02)08827-X
2. Hosking, D.; Lyles, K.; Brown, J. P.; Fraser, W. D.; Miller, P.; Curiel, M. D.; Devogelaer, J. P.; Hooper, M.; Su, G.; Zelenakas, K.; Pak, J.; Fashola, T.; Saidi, Y.; Eriksen, E. F.; Reid, I. R. Long-term control of bone turnover in Paget's disease with zoledronic acid and risedronate J. Bone Miner. Res. 2007, 22, 142-148 10.1359/jbmr.061001
3. Coleman, R. E. Bisphosphonates in breast cancer Ann. Oncol 2005, 16, 687-695 10.1093/annonc/mdi162
4. Luckman, S. P.; Hughes, D. E.; Coxon, F. P.; Graham, R.; Russell, G.; Rogers, M. J. Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras J. Bone Miner. Res. 1998, 13, 581-589 10.1359/jbmr.1998.13.4.581
5. Coxon, F. P.; Helfrich, M. H.; Van't Hof, R.; Sebti, S.; Ralston, S. H.; Hamilton, A.; Rogers, M. J. Protein geranylgeranylation is required for osteoclast formation, function, and survival: inhibition by bisphosphonates and GGTI-298 J. Bone Miner. Res. 2000, 15, 1467-1476 10.1359/jbmr.2000.15.8.1467
6. Szkopinska, A.; Plochocka, D. Farnesyl diphosphate synthase; regulation of product specificity Acta Biochim. Pol. 2005, 52, 45-55
7. Dhar, M. K.; Koul, A.; Kaul, S. Farnesyl pyrophosphate synthase: a key enzyme in isoprenoid biosynthetic pathway and potential molecular target for drug development New Biotechnol. 2013, 30, 114-123 10.1016/j.nbt.2012.07.001
8. Onufriev, A. V.; Alexov, E. Protonation and pK changes in protein-ligand binding Q. Rev. Biophys. 2013, 46, 181-209 10.1017/S0033583513000024
9. Nancollas, G. H.; Tang, R.; Phipps, R. J.; Henneman, Z.; Gulde, S.; Wu, W.; Mangood, A.; Russell, R. G.; Ebetino, F. H. Novel insights into actions of bisphosphonates on bone: differences in interactions with hydroxyapatite Bone 2006, 38, 617-627 10.1016/j.bone.2005.05.003
10. Ferrer-Casal, M.; Li, C.; Galizzi, M.; Stortz, C. A.; Szajnman, S. H.; Docampo, R.; Moreno, S. N. J.; Rodriguez, J. B. New insights into molecular recognition of 1,1-bisphosphonic acids by farnesyl diphosphate synthase Bioorg. Med. Chem. 2014, 22, 398-405 10.1016/j.bmc.2013.11.010
11. Ebetino, F. H.; Hogan, A. M.; Sun, S.; Tsoumpra, M. K.; Duan, X.; Triffitt, J. T.; Kwaasi, A. A.; Dunford, J. E.; Barnett, B. L.; Oppermann, U.; Lundy, M. W.; Boyde, A.; Kashemirov, B. A.; McKenna, C. E.; Russell, R. G. The relationship between the chemistry and biological activity of the bisphosphonates Bone 2011, 49, 20-33 10.1016/j.bone.2011.03.774
12. Kavanagh, K. L.; Guo, K.; Dunford, J. E.; Wu, X.; Knapp, S.; Ebetino, F. H.; Rogers, M. J.; Russell, R. G.; Oppermann, U. The molecular mechanism of nitrogen-containing bisphosphonates as antiosteoporosis drugs Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 7829-7834 10.1073/pnas.0601643103
13. Meloun, M.; Ferencikova, Z.; Malkova, H.; Pekarek, T. Thermodynamic dissociation constants of risedronate using spectrophotometric and potentiometric pH-titration Cent. Eur. J. Chem. 2012, 10, 338-353 10.2478/s11532-011-0150-3
14. Kawasaki, Y.; Sekiguchi, M.; Kawasaki, M.; Hirakura, Y. Thermodynamic evaluation of the binding of bisphosphonates to human farnesyl pyrophosphate synthase Chem. Pharm. Bull. 2014, 62, 77-83 10.1248/cpb.c13-00710
15. Harris, T. K.; Turner, G. J. Structural basis of perturbed pKa values of catalytic groups in enzyme active sites IUBMB Life 2002, 53, 85-98 10.1080/15216540211468
16. Koyama, T.; Tajima, M.; Sano, H.; Doi, T.; KoikeTakeshita, A.; Obata, S.; Nishino, T.; Ogura, K. Identification of significant residues in the substrate binding site of Bacillus stearothermophilus farnesyl diphosphate synthase Biochemistry 1996, 35, 9533-9538 10.1021/bi960137v
17. Song, L.; Poulter, C. D. Yeast farnesyl-diphosphate synthase: site-directed mutagenesis of residues in highly conserved prenyltransferase domains I and II Proc. Natl. Acad. Sci. U. S. A. 1994, 91, 3044-3048 10.1073/pnas.91.8.3044
18. Marrero, P. F.; Poulter, C. D.; Edwards, P. A. Effects of site-directed mutagenesis of the highly conserved aspartate residues in domain II of farnesyl diphosphate synthase activity J. Biol. Chem. 1992, 267, 21873-21878
19. Joly, A.; Edwards, P. A. Effect of site-directed mutagenesis of conserved aspartate and arginine residues upon farnesyl diphosphate synthase activity J. Biol. Chem. 1993, 268, 26983-26989
20. Koyama, T.; Tajima, M.; Sano, H.; Doi, T.; Koike-Takeshita, A.; Obata, S.; Nishino, T.; Ogura, K. Identification of significant residues in the substrate binding site of Bacillus stearothermophilus farnesyl diphosphate synthase Biochemistry 1996, 35, 9533-9538 10.1021/bi960137v
21. Desiraju, G. R.; Steiner, T. The Weak Hydrogen Bond in Structural Chemistry and Biology; Oxford University Press: Oxford, U.K., 1999; p xiv, 507 pp.
22. Niimura, N.; Podjarny, A. D. Neutron Protein Crystallography: Hydrogen, Protons, and Hydration in Bio-Macromolecules; International Union of Crystallography Monographs on Crystallography, 25; Oxford University Press: Oxford, U.K., 2011; p xvi, 233 pp of plates.
23. Yokoyama, T.; Mizuguchi, M.; Nabeshima, Y.; Kusaka, K.; Yamada, T.; Hosoya, T.; Ohhara, T.; Kurihara, K.; Tomoyori, K.; Tanaka, I.; Niimura, N. Hydrogen-bond network and pH sensitivity in transthyretin: Neutron crystal structure of human transthyretin J. Struct. Biol. 2012, 177, 283-290 10.1016/j.jsb.2011.12.022
24. Rondeau, J. M.; 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 ChemMedChem 2006, 1, 267-273 10.1002/cmdc.200500059
25. Yokoyama, T.; Ostermann, A.; Mizuguchi, M.; Niimura, N.; Schrader, T. E.; Tanaka, I. Crystallization and preliminary neutron diffraction experiment of human farnesyl pyrophosphate synthase complexed with risedronate Acta Crystallogr., Sect. F: Struct. Biol. Commun. 2014, 70, 470-472 10.1107/S2053230X14004087
26. Tanaka, I.; Kusaka, K.; Hosoya, T.; Niimura, N.; Ohhara, T.; Kurihara, K.; Yamada, T.; Ohnishi, Y.; Tomoyori, K.; Yokoyama, T. Neutron structure analysis using the IBARAKI biological crystal diffractometer (iBIX) at J-PARC Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 1194-1197 10.1107/S0907444910033020
27. Ohhara, T.; Kusaka, K.; Hosoya, T.; Kurihara, K.; Tomoyori, K.; Niimura, N.; Tanaka, I.; Suzuki, J.; Nakatani, T.; Otomo, T.; Matsuoka, S.; Tomita, K.; Nishimaki, Y.; Ajima, T.; Ryufuku, S. Development of data processing software for a new TOF single crystal neutron diffractometer at J-PARC Nucl. Instrum. Methods Phys. Res., Sect. A 2009, 600, 195-197 10.1016/j.nima.2008.11.030
28. Otwinowski, Z.; Minor, W. Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 1997, 276, 307-326 10.1016/S0076-6879(97)76066-X
29. Adams, P. D.; Afonine, P. V.; Bunkoczi, G.; Chen, V. B.; Davis, I. W.; Echols, N.; Headd, J. J.; Hung, L. W.; Kapral, G. J.; Grosse-Kunstleve, R. W.; McCoy, A. J.; Moriarty, N. W.; Oeffner, R.; Read, R. J.; Richardson, D. C.; Richardson, J. S.; Terwilliger, T. C.; Zwart, P. H. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 213-221 10.1107/S0907444909052925
30. Emsley, P.; Cowtan, K. Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 2126-2132 10.1107/S0907444904019158