Binding ensemble profiling with photoaffinity labeling (BEProFL) approach: Mapping the binding poses of HDAC8 inhibitors

Journal of Medicinal Chemistry

Volumn 52, Issue 22, 2009, Pages 7003-7013

  He, Bai ^a   Velaparthi, Subash ^a   Pieffet, Gilles ^a   Pennington, Chris ^a,b   Mahesh, Aruna ^a   Holzle, Denise L ^a   Brunsteiner, Michael ^a   Van Breemen, Richard ^a   Blond, Sylvie Y ^a,c   Petukhov, Pavel A ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b ABBOTT LABORATORIES   (United States)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

7 (4 BENZYLOXYPHENYLCARBAMOYL)HEPTANOIC ACID METHYL ESTER; 7 (4 HYDROXYPHENYLCARBAMOYL)HEPTANOIC ACID METHYL ESTER; 7 [4 (3 AZIDO 5 AZIDOMETHYLBENZYLOXY)PHENYLCARBAMOYL]HEPTANOIC ACID METHYL ESTER; 7 [4 (3 AZIDOPHENYL)THIAZOL 2 YLCARBAMOYL]HEPTANOIC ACID METHYL ESTER; AMINO ACID; AZIDE; HISTONE DEACETYLASE 8; HISTONE DEACETYLASE INHIBITOR; OCTANEDIOIC ACID [4 (3 AZIDO 5 AZIDOMETHYLBENZYLOXY)PHENYL]AMIDE HYDROXYAMIDE; OCTANEDIOIC ACID [4 (3 AZIDOPHENYL)THIAZOL 2 YL]AMIDE HYDROXYAMIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; DRUG PROTEIN BINDING; DRUG STRUCTURE; DRUG SYNTHESIS; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR DYNAMICS; PHOTOAFFINITY LABELING; TANDEM MASS SPECTROMETRY; ULTRAVIOLET RADIATION;

AMINO ACID SEQUENCE; AZIDES; CHROMATOGRAPHY, LIQUID; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHOTOAFFINITY LABELS; PROTEIN BINDING; PROTEIN CONFORMATION; REPRESSOR PROTEINS; TANDEM MASS SPECTROMETRY;

EID: 70949103451     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm9005077     Document Type: Article

References (56)

1. Korner, M.; Tibes, U. Histone deacetylase inhibitors: a novel class of anti-cancer agents on its way to the market. Prog. Med. Chem. 2008, 46, 205-280.
2. Marks, P. A.; Richon, V. M.; Rifkind, R. A. Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J. Natl. Cancer Inst. 2000, 92, 1210-1216.
3. de Ruijter, A. J.; van Gennip, A. H.; Caron, H. N.; Kemp, S.; van Kuilenburg, A. B.Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J. 2003, 370, 737-749.
4. Hahnen, E.; Hauke, J.; Trankle, C.; Eyupoglu, I. Y.; Wirth, B.; Blumcke, I. Histone deacetylase inhibitors: possible implications for neurodegenerative disorders. Expert Opin. Invest. Drugs 2008, 17, 169-184.
5. Wang, D. F.; Helquist, P.; Wiech, N. L.; Wiest, O. Toward selective histone deacetylase inhibitor design: homology modeling, docking studies, and molecular dynamics simulations of human class I histone deacetylases. J. Med. Chem. 2005, 48, 6936-6947.
6. Nielsen, P. E. Photochemical Probes in Biochemistry; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1989; Vol.272.
7. Rajagopalan, K.; Watt, D. S.; Haley, B. E. Orientation of GTP and ADP within their respective binding sites in glutamate dehydrogenase. Eur. J. Biochem. 1999, 265, 564-571.
8. Olcott, M.C.; Bradley, M. L.; Haley, B. E. Photoaffinity labeling of creatine kinase with 2-azido- and 8-azidoadenosine triphosphate: identification of two peptides from the ATP-binding domain. Biochemistry 1994, 33, 11935-11941.
9. Speers, A. E.; Adam, G. C.; Cravatt, B. F. Activity-based protein profiling in vivo using a copper(I)-catalyzed azide-alkyne [3 + 2] cycloaddition. J. Am. Chem. Soc. 2003, 125, 4686-4687.
10. Adam, G. C.; Burbaum, J.; Kozarich, J. W.; Patricelli, M. P.; Cravatt, B. F. Mapping enzyme active sites in complex proteomes. J. Am. Chem. Soc. 2004, 126, 1363-1368.
11. Sieber, S. A.; Mondala, T. S.; Head, S. R.; Cravatt, B. F. Microarray platform for profiling enzyme activities in complex proteomes. J. Am. Chem. Soc. 2004, 126, 15640-15641.
12. Speers, A. E.; Cravatt, B. F. A tandem orthogonal proteolysis strategy for high-content chemical proteomics. J. Am. Chem. Soc. 2005, 127, 10018-10019.
13. Hanson, S. R.; Hsu, T. L.; Weerapana, E.; Kishikawa, K.; Simon, G. M.; Cravatt, B. F.; Wong, C. H. Tailored glycoproteomics and glycan site mapping using saccharide-selective bioorthogonal probes. J. Am. Chem. Soc. 2007, 129, 7266-7267.
14. Li, W.; Blankman, J. L.; Cravatt, B. F. A functional proteomic strategy to discover inhibitors for uncharacterized hydrolases. J. Am. Chem. Soc. 2007, 129, 9594-9595.
15. Salisbury, C. M.; Cravatt, B. F. Activity-based probes for proteomic profiling of histone deacetylase complexes. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 1171-1176.
16. Hosoya, T.; Hiramatsu, T.; Ikemoto, T.; Nakanishi, M.; Aoyama, H.; Hosoya, A.; Iwata, T.; Maruyama, K.; Endo, M.; Suzuki, M. Novel bifunctional probe for radioisotope-free photoaffinity labeling: compact structure comprised of photospecific ligand ligation and detectable tag anchoring units. Org. Biomol. Chem. 2004, 2, 637-641.
17. Sun, P.; Wang, G. X.; Furuta, K.; Suzuki, M. Synthesis of a bisazido analogue of acromelic acid for radioisotope-free photoaffinity labeling and biochemical studies. Bioorg. Med. Chem. Lett. 2006, 16, 2433-2436.
18. 2+ release from sarcoplasmic reticulum of skeletal muscle. Bioorg. Med. Chem. Lett. 2005, 15, 1289-1294.
19. Saxon, E.; Armstrong, J. I.; Bertozzi, C. R. A "traceless" Staudinger ligation for the chemoselective synthesis of amide bonds. Org. Lett. 2000, 2, 2141-2143.
20. Saxon, E.; Bertozzi, C. R. Cell surface engineering by a modified Staudinger reaction. Science 2000, 287, 2007-2010.
21. Kiick, K. L.; Saxon, E.; Tirrell, D. A.; Bertozzi, C. R. Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation. Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (1), 19-24.
22. Saxon, E.; Luchansky, S. J.; Hang, H. C.; Yu, C.; Lee, S. C.; Bertozzi, C. R. Investigating cellular metabolism of synthetic azidosugars with the Staudinger ligation. J. Am. Chem. Soc. 2002, 124, 14893-14902.
23. Vocadlo, D. J.; Hang, H. C.; Kim, E. J.; Hanover, J. A.; Bertozzi, C. R. A chemical approach for identifying O-GlcNAc-modified proteins in cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 9116-9121.
24. Vocadlo, D. J.; Bertozzi, C. R. A strategy for functional proteomic analysis of glycosidase activity from cell lysates. Angew. Chem., Int. Ed. 2004, 43, 5338-5342.
25. Al-Mawsawi, L. Q.; Fikkert, V.; Dayam, R.; Witvrouw, M.; Burke, T. R., Jr.; Borchers, C. H.; Neamati, N. Discovery of a small-molecule HIV-1 integrase inhibitor-binding site. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 10080-10085.
26. Kozikowski, A. P.; Chen, Y.; Gaysin, A.; Chen, B.; D'Annibale, M. A.; Suto, C. M.; Langley, B. C. Functional differences in epigenetic modulators-superiority of mercaptoacetamide based-HDAC inhibitors relative to hydroxamates in cortical neuron neuroprotection studies. J. Med. Chem. 2007, 50, 3054-3061.
27. 2+ release from sarcoplasmic reticulum of skeletal muscle. Bioorg. Med. Chem. Lett. 2005, 15, 1289-1294.
28. Lin, P. C.; Ueng, S. H.; Yu, S. C.; Jan, M. D.; Adak, A. K.; Yu, C. C.; Lin, C. C. Surface modification of magnetic nanoparticle via Cu(I)-catalyzed alkyne-azide [2 + 3] cycloaddition. Org. Lett. 2007, 9, 2131-2134.
29. Berendsen, H. J. C.; van der Spoel, D.; van Drunen, R. GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 1995, 91, 43-56.
30. Lindal, E.; Hess, B.; van der Spoel, D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 2001, 7, 306-317.
31. Van Der Spoel, D.; Van Buuren, A. R.; Apol, E.; Meulenhoff, P. J.; Tieleman, D. P.; Sijbers, A. L. T. M.; Hess, B.; Feenstra, K. A.; Lindahl, E.; Drunen, R. v.; Berendsen, H. J. C. GROMACS User Manual, version 3.0; Nijenborgh 4, 9747 AG: Groningen, The Netherlands, 2001; http://www.gromacs.org.
32. Van Der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E. GROMACS: fast, flexible and free. J. Comput. Chem. 2005, 26, 1701-1718.
33. Cornell, W. D.; Cieplak, P.; Barly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 1995, 117, 5179-5197.
34. Sorin, E. J.; Rhee, Y. M.; Pande, V. S. Does waterplay a structural role in the folding of small nucleic acids? Biophys. J. 2005, 88, 2516-2524.
35. 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.
36. Wang, J.; Wang, W.; Kollman, P. A.; Case, D. A. Automatic atom type and bond type perception in molecular mechanical calculations. J. Mol. Graph. Modell. 2006, 25, 247-260.
37. Pieffet, G.; Petukhov, P. A. Parameterization of aromatic azido groups: application as photoaffinity probes in molecular dynamics studies. J. Mol. Model. 2009, 15, 1291-1297.
38. Jakalian, A.; Bush, B. L.; Jack, D. B.; Bayly, C. I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I: Method. J. Comput. Chem. 2000, 21, 132-146.
39. 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.
40. Jones, G.; Willett, P.; Glen, R. C.; Leach, A. R.; Taylor, R. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 1997, 267, 727-748.
41. Suzuki, T.; Kouketsu, A.; Matsuura, A.; Kohara, A.; Ninomiya, S.; Kohda, K.; Miyata, N. Thiol-based SAHA analogues as potent histone deacetylase inhibitors. Bioorg. Med. Chem. Lett. 2004, 14, 3313-3317.
42. Chen, Y.; Lopez-Sanchez, M.; Savoy, D. N.; Billadeau, D. D.; Dow, G. S.; Kozikowski, A. P. A series of potent and selective, triazolylphenyl-based histone deacetylases inhibitors with activity against pancreatic cancer cells and Plasmodium falciparum. J. Med. Chem. 2008, 51, 3437-3448.
43. Somoza, J. R.; Skene, R. J.; Katz, B. A.; Mol, C.; Ho, J. D.; Jennings, A. J.; Luong, C.; Arvai, A.; Buggy, J. J.; Chi, E.; Tang, J.; Sang, B. C.; Verner, E.; Wynands, R.; Leahy, E. M.; Dougan, D. R.; Snell, G.; Navre, M.; Knuth, M. W.; Swanson, R. V.; McRee, D. E.; Tari, L. W. Structural snapshots of human HDAC8 provide insights into the class I histone deacetylases. Structure (Cambridge, MA, U. S.) 2004, 12, 1325-1334.
44. Vannini, A.; Volpari, C.; Gallinari, P.; Jones, P.; Mattu, M.; Carfi, A.; De Francesco, R.; Steinkuhler, C.; Di Marco, S. Substrate binding to histone deacetylases as shown by the crystal structure of the HDAC8-substrate complex. EMBO Rep. 2007, 8, 879-884.
45. Dowling, D. P.; Gantt, S. L.; Gattis, S. G.; Fierke, C. A.; Christianson, D. W. Structural studies of human histone deacetylase 8 and its site-specific variants complexed with substrate and inhibitors. Biochemistry 2008, 47, 13554-13563.
46. 50) of an enzymatic reaction. Biochem. Pharmacol. 1973, 22, 3099-3108.
47. Girish, V.; Vijayalakshmi, A. Affordable image analysis using NIH Image/ImageJ. Indian J. Cancer 2004, 41, 47.
48. Eliceiri, K. W.; Rueden, C. Tools for visualizing multidimensional images from living specimens. Photochem. Photobiol. 2005, 81, 1116-1122.
49. Vida, version 3.0; Openeye Scientific Software LLC: Santa Fe, NM, 2008.
50. Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.; Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. UCSF Chimera, a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25, 1605-1612.
51. 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.
52. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 1997, 18, 1463-1472.
53. Miyamoto, S.; Kollman, P. A. SETTLE: an analytical version of the SHAKE and RATTLE algorithms for rigid water models. J. Comput. Chem. 1992, 13, 952-962.
54. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 1984, 81, 3684-3690.
55. Molecular-Dynamics Simulations of Statistical-Mechanical Systems; Hoover, W. G., Ed.; North-Holland: Amsterdam, 1986.
56. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: an N-log(N) method for Ewald sums in large systems. J. Chem. Phys. 1993, 98, 10089-10092.