Taxodione and arenarone inhibit farnesyl diphosphate synthase by binding to the isopentenyl diphosphate site

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 25, 2014, Pages

  Liu, Yi Liang ^a   Lindert, Steffen ^b,c   Zhu, Wei ^a   Wang, Ke ^a   McCammon, J Andrew ^b,c,d   Oldfield, Eric ^a  

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

^b San Diego   (United States)

^c NATIONAL SCIENCE FOUNDATION   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Crystallography; Drug discovery; Molecular dynamics; Prenyl synthase; Prenylation

Indexed keywords

ARENARONE; GERANYLTRANSFERASE; ISOPENTENYL DIPHOSPHATE; QUINONE DERIVATIVE; TAXODIONE; UNCLASSIFIED DRUG; ZOLEDRONIC ACID;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING SITE; CALORIMETRY; CONFORMATION; CRYSTAL STRUCTURE; ENZYME INHIBITION; ENZYME MODIFICATION; HUMAN; HYDROGEN BOND; IC 50; IONIZATION; MOLECULAR DYNAMICS; NUCLEOPHILICITY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; TAUTOMER;

CRYSTALLOGRAPHY; DRUG DISCOVERY; MOLECULAR DYNAMICS; PRENYL SYNTHASE; PRENYLATION;

ALLOSTERIC SITE; ANTI-INFECTIVE AGENTS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CRYSTALLOGRAPHY, X-RAY; DITERPENES; ENZYME INHIBITORS; GERANYLTRANSTRANSFERASE; HEMITERPENES; HUMANS; ORGANOPHOSPHORUS COMPOUNDS; PROTOZOAN PROTEINS; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84903462149     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1409061111     Document Type: Article

References (71)

1. Oldfield E, Lin FY (2012) Terpene biosynthesis: Modularity rules. Angew Chem Int Ed Engl 51(5):1124-1137.
2. Liu CI, et al. (2008) A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence. Science 319(5868):1391-1394.
3. Russell RG (2011) Bisphosphonates: The first 40 years. Bone 49(1):2-19.
4. Martin MB, et al. (2001) Bisphosphonates inhibit the growth of Trypanosoma brucei, Trypanosoma cruzi, Leishmania donovani, Toxoplasma gondii, and Plasmodium falciparum: A potential route to chemotherapy. J Med Chem 44(6):909-916. (Pubitemid 32861615)
5. Kunzmann V, Bauer E, Wilhelm M (1999) Gamma/delta T-cell stimulation by pamidronate. N Engl J Med 340(9):737-738.
6. Coscia M, et al. (2010) Zoledronic acid repolarizes tumour-associated macrophages and inhibits mammary carcinogenesis by targeting the mevalonate pathway. J Cell Mol Med 14(12):2803-2815.
7. Shipman CM, Croucher PI, Russell RG, Helfrich MH, Rogers MJ (1998) The bisphosphonate incadronate (YM175) causes apoptosis of human myeloma cells in vitro by inhibiting the mevalonate pathway. Cancer Res 58(23):5294-5297. (Pubitemid 28551102)
8. Wood J, et al. (2002) Novel antiangiogenic effects of the bisphosphonate compound zoledronic acid. J Pharmacol Exp Ther 302(3):1055-1061. (Pubitemid 34920226)
9. Mukherjee S, Huang C, Guerra F, Wang K, Oldfield E (2009) Thermodynamics of bisphosphonates binding to human bone: A two-site model. J Am Chem Soc 131(24):8374-8375.
10. Jahnke W, et al. (2010) Allosteric non-bisphosphonate FPPS inhibitors identified by fragment-based discovery. Nat Chem Biol 6(9):660-666.
11. Leon A, et al. (2006) Isoprenoid biosynthesis as a drug target: Bisphosphonate inhibition of Escherichia coli K12 growth and synergistic effects of fosmidomycin. J Med Chem 49(25):7331-7341. (Pubitemid 44913394)
12. Tarshis LC, Yan M, Poulter CD, Sacchettini JC (1994) Crystal structure of recombinant farnesyl diphosphate synthase at 2.6-A resolution. Biochemistry 33(36):10871-10877. (Pubitemid 24296339)
13. Rondeau JM, et al. (2006) Structural basis for the exceptional in vivo efficacy of bisphosphonate drugs. ChemMedChem 1(2):267-273.
14. Kavanagh KL, et al. (2006) The molecular mechanism of nitrogen-containing bisphosphonates as antiosteoporosis drugs. Proc Natl Acad Sci USA 103(20):7829-7834.
15. Hosfield DJ, et al. (2004) Structural basis for bisphosphonate-mediated inhibition of isoprenoid biosynthesis. J Biol Chem 279(10):8526-8529. (Pubitemid 38295905)
16. Salcius M, et al. (2014) SEC-TID: A label-free method for small-molecule target identification. J Biomol Screen, 10.1177/1087057114522691.
17. Zhang Y, et al. (2009) Lipophilic bisphosphonates as dual farnesyl/geranylgeranyl diphosphate synthase inhibitors: An X-ray and NMR investigation. J Am Chem Soc 131(14):5153-5162.
18. Zhang Y, et al. (2010) Lipophilic pyridinium bisphosphonates: Potent gammadelta T cell stimulators. Angew Chem Int Ed Engl 49(6):1136-1138.
19. No JH, et al. (2012) Lipophilic analogs of zoledronate and risedronate inhibit Plasmodium geranylgeranyl diphosphate synthase (GGPPS) and exhibit potent antimalarial activity. Proc Natl Acad Sci USA 109(11):4058-4063.
20. Lindert S, et al. (2013) Farnesyl diphosphate synthase inhibitors from in silico screening. Chem Biol Drug Des 81(6):742-748.
21. Liu J, et al. (2014) Syntheses and characterization of non-bisphosphonate quinoline derivatives as new FPPS inhibitors. Biochim Biophys Acta 1840(3):1051-1062.
22. Christen M, et al. (2005) The GROMOS software for biomolecular simulation: GROMOS05. J Comput Chem 26(16):1719-1751. (Pubitemid 43076183)
23. Schrödinger LLC (2012) Schrodinger Suite 2012 (Schrödinger, LLC, New York).
24. Trott O, Olson AJ (2010) AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31(2):455-461.
25. Friesner RA, et al. (2004) Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J Med Chem 47(7):1739-1749. (Pubitemid 38380917)
26. Friesner RA, et al. (2006) Extra precision glide: Docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J Med Chem 49(21):6177-6196. (Pubitemid 44595196)
27. Halgren TA, et al. (2004) Glide: A new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J Med Chem 47(7):1750-1759. (Pubitemid 38380918)
28. Montalvetti A, et al. (2003) Farnesyl pyrophosphate synthase is an essential enzyme in Trypanosoma brucei. In vitro RNA interference and in vivo inhibition studies. J Biol Chem 278(19):17075-17083. (Pubitemid 36799584)
29. Webb MR (1992) A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc Natl Acad Sci USA 89(11):4884-4887.
30. Paris D, et al. (2010) Reduction of beta-amyloid pathology by celastrol in a transgenic mouse model of Alzheimer's disease. J Neuroinflammation 7:17.
31. Sha M, et al. (2014) Celastrol induces apoptosis of gastric cancer cells by miR-21 inhibiting PI3K/Akt-NF-κB signaling pathway. Pharmacology 93(1-2):39-46.
32. Yang C, et al. (2014) Celastrol increases glucocerebrosidase activity in Gaucher disease by modulating molecular chaperones. Proc Natl Acad Sci USA 111(1):249-254.
33. Liu Z, et al. (2014) Cancerous inhibitor of PP2A is targeted by natural compound celastrol for degradation in non-small-cell lung cancer. Carcinogenesis 35(4):905-914.
34. Zapata B, et al. (2013) Cytotoxic, immunomodulatory, antimycotic, and antiviral activities of semisynthetic 14-hydroxyabietane derivatives and triptoquinone C-4 epimers. Med. Chem. Commun. 4:1239-1246.
35. Burmistrova O, et al. (2013) Antiproliferative activity of abietane diterpenoids against human tumor cells. J Nat Prod 76(8):1413-1423.
36. Kuźma L, et al. (2012) Antimicrobial and anti-biofilm properties of new taxodione derivative from hairy roots of Salvia austriaca. Phytomedicine 19(14):1285-1287.
37. Gordaliza M (2010) Cytotoxic terpene quinones from marine sponges. Mar Drugs 8(12):2849-2870.
38. Tada M, Kurabe J, Yoshida T, Ohkanda T, Matsumoto Y (2010) Syntheses and antibacterial activities of diterpene catechol derivatives with abietane, totarane and podocarpane skeletons against methicillin-resistant Staphylococcus aureus and Propionibacterium acnes. Chem Pharm Bull (Tokyo) 58(6):818-824.
39. Zaghloul AM, Gohar AA, Naiem ZA-AM, Abdel Bar FM (2008) Taxodione, a DNA-binding compound from Taxodium distichum L. (Rich.). Z Naturforsch C 63(5-6):355-360.
40. Raja SM, et al. (2011) Anticancer activity of Celastrol in combination with ErbB2-targeted therapeutics for treatment of ErbB2-overexpressing breast cancers. Cancer Biol Ther 11(2):263-276.
41. Schmitz FJ, Lakshmi V, Powell DR, Van der Helm D (1984) Arenarol and arenarone: Sesquiterpenoids with rearranged drimane skeletons from the marine sponge Dysidea arenaria. J Org Chem 49(2):241-244.
42. Valdar WS (2002) Scoring residue conservation. Proteins 48(2):227-241.
43. Wallace AC, Laskowski RA, Thornton JM (1995) LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8(2):127-134.
44. Durrant JD, de Oliveira CA, McCammon JA (2011) POVME: An algorithm for measuring binding-pocket volumes. J Mol Graph Model 29(5):773-776.
45. Epand RF, Epand RM, Jung CY (2001) Ligand-modulation of the stability of the glucose transporter GLUT 1. Protein Sci 10(7):1363-1369. (Pubitemid 32568103)
46. Cooper A (1992) Effect of cyclodextrins on the thermal stability of globular proteins. J Am Chem Soc 114(23):9208-9209.
47. Choi BS, et al. (2014) Celastrol from 'Thunder God Vine' protects SH-SY5Y cells through the preservation of mitochondrial function and inhibition of p38 MAPK in a rotenone model of Parkinson's disease. Neurochem Res 39(1):84-96.
48. Sreeramulu S, Gande SL, Göbel M, Schwalbe H (2009) Molecular mechanism of inhibition of the human protein complex Hsp90-Cdc37, a kinome chaperone-cochaperone, by triterpene celastrol. Angew Chem Int Ed Engl 48(32):5853-5855.
49. Klaić L, Morimoto RI, Silverman RB (2012) Celastrol analogues as inducers of the heat shock response. Design and synthesis of affinity probes for the identification of protein targets. ACS Chem Biol 7(5):928-937.
50. Klaić L, Trippier PC, Mishra RK, Morimoto RI, Silverman RB (2011) Remarkable stereospecific conjugate additions to the Hsp90 inhibitor celastrol. J Am Chem Soc 133(49):19634-19637.
51. Hanson RL, Lardy HA, Kupchan SM (1970) Inhibition of phosphofructokinase by quinone methide and alpha-methylene lactone tumor inhibitors. Science 168(3929):378-380.
52. Yang Z, et al. (2001) Synthesis of variously oxidized abietane diterpenes and their antibacterial activities against MRSA and VRE. Bioorg Med Chem 9(2):347-356. (Pubitemid 32244033)
53. Case DA, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26(16):1668-1688. (Pubitemid 43076180)
54. Hornak V, et al. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65(3):712-725. (Pubitemid 44583220)
55. Lindorff-Larsen K, et al. (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78(8):1950-1958.
56. Ryckaert J-P, Ciccotti G, Berendsen HJC (1977) Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J Comput Phys 23(3):327-341.
57. Grant BJ, Rodrigues AP, ElSawy KM, McCammon JA, Caves LS (2006) Bio3d: An R package for the comparative analysis of protein structures. Bioinformatics 22(21):2695-2696. (Pubitemid 44642612)
58. Abseher R, Nilges M (1998) Are there non-trivial dynamic cross-correlations in proteins? J Mol Biol 279(4):911-920. (Pubitemid 28284705)
59. VanAalten DMF, DeGroot BL, Findlay JBC, Berendsen HJC, Amadei A (1997) A comparison of techniques for calculating protein essential dynamics. J Comput Chem 18(2):169-181. (Pubitemid 127598563)
60. Mao J, et al. (2006) Solid-state NMR, crystallographic, and computational investigation of bisphosphonates and farnesyl diphosphate synthase- bisphosphonate complexes. J Am Chem Soc 128(45):14485-14497. (Pubitemid 44749848)
61. Mao J, et al. (2004) Crystallization and preliminary X-ray diffraction study of the farnesyl diphosphate synthase from Trypanosoma brucei. Acta Crystallogr D Biol Crystallogr 60(Pt 10):1863-1866. (Pubitemid 41079709)
62. Zhang Y, et al. (2013) Chemo-immunotherapeutic antimalarials targeting isoprenoid biosynthesis. ACS Med Chem Lett 4(4):423-427.
63. Minor W, Cymborowski M, Otwinowski Z, Chruszcz M (2006) HKL-3000: The integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr 62(Pt 8):859-866. (Pubitemid 44125661)
64. Winn MD, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67(Pt 4):235-242.
65. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
66. Laskowski RA, Swindells MB (2011) LigPlot+: Multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model 51(10):2778-2786.
67. Laskowski RA, et al. (1997) PDBsum: A Web-based database of summaries and analyses of all PDB structures. Trends Biochem Sci 22(12):488-490. (Pubitemid 27515917)
68. Schrödinger LLC (2013) The PyMOL molecular graphics system (Schrödinger, LLC, New York), Version 1.3.
69. Rieger CE, Lee J, Turnbull JL (1997) A continuous spectrophotometric assay for aspartate transcarbamylase and ATPases. Anal Biochem 246(1):86-95. (Pubitemid 27100511)
70. Zhang Y, et al. (2006) Activity of nitrogen-containing and non-nitrogen-containing bisphosphonates on tumor cell lines. J Med Chem 49(19):5804-5814. (Pubitemid 44423717)
71. PerkinElmer (2013) ChemDraw (PerkinElmer Informatics), Version 13.0.2.3020. Available at www.cambridgesoft.com/Ensemble-for-Chemistry/ChemDraw/ . Accessed May 27, 2014.