Understanding the inhibitory effect of highly potent and selective archazolides binding to the vacuolar atpase

Journal of Chemical Information and Modeling

Volumn 52, Issue 8, 2012, Pages 2265-2272

  Dreisigacker, Sandra ^a,b   Latek, Dorota ^a,f   Bockelmann, Svenja ^c   Huss, Markus ^c   Wieczorek, Helmut ^c   Filipek, Slawomir ^d   Gohlke, Holger ^e   Menche, Dirk ^b,g   Carlomagno, Teresa ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF OSNABRÜCK   (Germany)

^d UNIVERSITY OF WARSAW   (Poland)

^e HEINRICH HEINE UNIVERSITY   (Germany)

^f INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^g UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINDING SITES; DISEASES; LIGANDS;

BIOCHEMICAL EXPERIMENTS; EQUATORIAL REGIONS; INHIBITORY MECHANISM; LIGAND BINDING MODE; MOLECULAR DYNAMICS SIMULATIONS; SELECTIVE INHIBITORS; SITE DIRECTED MUTAGENESIS; THERAPEUTIC TARGETS;

MOLECULAR DYNAMICS;

ARCHAZOLIDE A; ENZYME INHIBITOR; MACROLIDE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; THIAZOLE DERIVATIVE;

ANIMAL; ARTICLE; CELL LINE; CHEMISTRY; DRUG ANTAGONISM; ENZYME SPECIFICITY; ENZYMOLOGY; IC 50; METABOLISM; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOUSE; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; REPRODUCIBILITY; SACCHAROMYCES CEREVISIAE;

ANIMALS; CELL LINE; ENZYME INHIBITORS; INHIBITORY CONCENTRATION 50; MACROLIDES; MICE; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; REPRODUCIBILITY OF RESULTS; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY; THIAZOLES; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84865464829     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci300242d     Document Type: Article

References (40)

1. Sasse, F.; Steinmetz, H.; Höfle, G.; Reichenbach, H. Archazolids, new cytotoxic macrolactones from Archangium gephyra (Myxobacteria). Production, isolation, physico-chemical and biological properties J. Antibiot. (Tokyo) 2003, 56, 520-525 (Pubitemid 36849938)
2. Menche, D.; Hassfeld, J.; Steinmetz, H.; Huss, M.; Wieczorek, H.; Sasse, F. Archazolid-7-O-β-D-glucopyranoside - Isolation, Structural Elucidation and Solution Conformation of a Novel V-ATPase Inhibitor from the Myxobacterium Cystobacter violaceus Eur. J. Org. Chem. 2007, 2007, 1196-1202
3. Menche, D.; Hassfeld, J.; Steinmetz, H.; Huss, M.; Wieczorek, H.; Sasse, F. The first hydroxylated archazolid from the myxobacterium Cystobacter violaceus: isolation, structural elucidation and V-ATPase inhibition J. Antibiot. (Tokyo) 2007, 60, 328-331
4. Horstmann, N.; Essig, S.; Bockelmann, S.; Wieczorek, H.; Huss, M.; Sasse, F.; Menche, D. Archazolid A-15-O-beta-D-glucopyranoside and iso-archazolid B: potent V-ATPase inhibitory polyketides from the myxobacteria Cystobacter violaceus and Archangium gephyra J. Nat. Prod. 2011, 74, 1100-1105
5. Hassfeld, J.; Fares, C.; Steinmetz, H.; Carlomagno, T.; Menche, D. Stereochemical determination of Archazolid A and B, highly potent vacuolar-type ATPase inhibitors from the Myxobacterium Archangium gephyra Org. Lett. 2006, 8, 4751-4754 (Pubitemid 44629451)
6. Fares, C.; Hassfeld, J.; Menche, D.; Carlomagno, T. Simultaneous determination of the conformation and relative configuration of archazolide a by using nuclear overhauser effects, J couplings, and residual dipolar couplings Angew. Chem., Int. Ed. Engl. 2008, 47, 3722-3726
7. Huss, M.; Sasse, F.; Kunze, B.; Jansen, R.; Steinmetz, H.; Ingenhorst, G.; Zeeck, A.; Wieczorek, H. Archazolid and apicularen: novel specific V-ATPase inhibitors BMC Biochem. 2005, 6, 13
8. Menche, D.; Hassfeld, J.; Li, J.; Rudolph, S. Total synthesis of archazolid A J. Am. Chem. Soc. 2007, 129, 6100-6101 (Pubitemid 46786800)
9. Menche, D.; Hassfeld, J.; Li, J.; Mayer, K.; Rudolph, S. Modular total synthesis of archazolid A and B J. Org. Chem. 2009, 74, 7220-7229
10. Menche, D.; Hassfeld, J.; Sasse, F.; Huss, M.; Wieczorek, H. Design, synthesis and biological evaluation of novel analogues of archazolid: a highly potent simplified V-ATPase inhibitor Bioorg. Med. Chem. Lett. 2007, 17, 1732-1735 (Pubitemid 46290630)
11. Bockelmann, S.; Menche, D.; Rudolph, S.; Bender, T.; Grond, S.; von Zezschwitz, P.; Muench, S. P.; Wieczorek, H.; Huss, M. Archazolid A binds to the equatorial region of the c-ring of the vacuolar H+-ATPase J. Biol. Chem. 2010, 285, 38304-38314
12. Beyenbach, K. W.; Wieczorek, H. The V-type H+ ATPase: molecular structure and function, physiological roles and regulation J. Exp. Biol. 2006, 209, 577-589
13. Mandel, M.; Moriyama, Y.; Hulmes, J. D.; Pan, Y. C.; Nelson, H.; Nelson, N. cDNA sequence encoding the 16-kDa proteolipid of chromaffin granules implies gene duplication in the evolution of H+-ATPases Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 5521-5524
14. Hinton, A.; Bond, S.; Forgac, M. V-ATPase functions in normal and disease processes Pflugers Arch. 2009, 457, 589-598
15. Forgac, M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology Nat. Rev. Mol. Cell Biol. 2007, 8, 917-929 (Pubitemid 47622561)
16. Finbow, M. E.; Eliopoulos, E. E.; Jackson, P. J.; Keen, J. N.; Meagher, L.; Thompson, P.; Jones, P.; Findlay, J. B. C. Structure of a 16 kDa integral membrane protein that has identity to the putative proton channel of the vacuolar H+-ATPase Protein Eng. 1992, 5, 7-15
17. Bowman, B. J.; McCall, M. E.; Baertsch, R.; Bowman, E. J. A Model for the Proteolipid Ring and Bafilomycin/Concanamycin-binding Site in the Vacuolar ATPase of Neurospora crassa J. Biol. Chem. 2006, 281, 31885-31893 (Pubitemid 46041451)
18. Baker, N. A.; Sept, D.; Joseph, S.; Holst, M. J.; McCammon, J. A. Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 10037-10041 (Pubitemid 32802969)
19. Erdélyi, M.; Pfeiffer, B.; Hauenstein, K.; Fohrer, J.; Gertsch, J.; Altmann, K.-H.; Carlomagno, T. Conformational Preferences of Natural and C3-Modified Epothilones in Aqueous Solution J. Med. Chem. 2008, 51, 1469-1473 (Pubitemid 351480407)
20. Marraud, M.; Aubry, A. Crystal structures of peptides and modified peptides Biopolymers 1996, 40, 45-83
21. Morris, G. M.; Goodsell, D. S.; Halliday, R. S.; Huey, R.; Hart, W. E.; Belew, R. K.; Olson, A. J. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 1998, 19, 1639-1662 (Pubitemid 128590223)
22. Gohlke, H.; Hendlich, M.; Klebe, G. Knowledge-based scoring function to predict protein-ligand interactions J. Mol. Biol. 2000, 295, 337-356 (Pubitemid 30045364)
23. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M. C.; Xiong, G.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R.; Lee, T.; Caldwell, J.; Wang, J.; Kollman, P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 2003, 24, 1999-2012
24. Krieger, E. (2003, YASARA (www.yasara.org/sd).
25. Murata, T.; Yamato, I.; Kakinuma, Y.; Leslie, A. G. W.; Walker, J. E. Structure of the Rotor of the V-Type Na+-ATPase from Enterococcus hirae Science 2005, 308, 654-659 (Pubitemid 40594379)
26. Pogoryelov, D.; Yildiz, O.; Faraldo-Gomez, J. D.; Meier, T. High-resolution structure of the rotor ring of a proton-dependent ATP synthase Nat. Struct. Mol. Biol. 2009, 16, 1068-1073
27. Meier, T.; Ferguson, S. A.; Cook, G. M.; Dimroth, P.; Vonck, J. Structural Investigations of the Membrane-Embedded Rotor Ring of the F-ATPase from Clostridium paradoxum J. Bacteriol. 2006, 188, 7759-7764 (Pubitemid 44764512)
28. Macromodel, version 9.7; Schrödinger, LLC: New York, NY, 2009.
29. Jorgensen, W. L.; Maxwell, D. S.; Tirado-Rives, J. Development and Testing of the OPLS All-Atom Force Field on Conformational Energetics and Properties of Organic Liquids J. Am. Chem. Soc. 1996, 118, 11225-11236 (Pubitemid 26399746)
30. MacKerell, A. D. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
31. Chemistry at HARvard Macromolecular Mechanics (CHARMM), version 35b2, 2008.
32. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79, 926-935
33. Price, D. J.; Brooks, C. L. Modern protein force fields behave comparably in molecular dynamics simulations J. Comput. Chem. 2002, 23, 1045-1057 (Pubitemid 34781851)
34. Sotriffer, C. A.; Gohlke, H.; Klebe, G. Docking into Knowledge-Based Potential Fields: A Comparative Evaluation of DrugScore J. Med. Chem. 2002, 45, 1967-1970 (Pubitemid 34477710)
35. Lomize, M. A.; Pogozheva, I. D.; Joo, H.; Mosberg, H. I.; Lomize, A. L. OPM database and PPM web server: resources for positioning of proteins in membranes Nucleic Acids Res. 2012, 40 (D1) D370-D376
36. Jakalian, A.; Jack, D. B.; Bayly, C. I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and validation J. Comput. Chem. 2002, 23, 1623-1641 (Pubitemid 35330860)
37. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field J. Comput. Chem. 2004, 25, 1157-1174
38. Brunger, A. T. X-PLOR version 3.1: A System for X-ray Crystallography and NMR; Yale University Press: New Haven, CT, 1993.
39. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual molecular dynamics J. Mol. Graphics Modell. 1996, 14, 33-38 (Pubitemid 26152973)
40. Wieczorek, H.; Cioffi, M.; Klein, U.; Harvey, W. R.; Schweikl, H.; Wolfersberger, M. G. Isolation of goblet cell apical membrane from tobacco hornworm midgut and purification of its vacuolar-type ATPase. In Methods Enzymology; Sidney Fleischer, B. F., Ed.; Academic Press: 1990; Vol. 192, pp 608-616.