Journal of Medicinal Chemistry
Article
(10) Dobson, S. E.; Augustijn, K. D.; Brannigan, J. A.; Schnick, C.;
Janse, C. J.; Dodson, E. J.; Waters, A. P.; Wilkinson, A. J. The crystal
structures of macrophage migration inhibitory factor from Plasmodium
falciparum and Plasmodium berghei. Protein Sci. 2009, 18, 2578−2591.
(11) Cournia, Z.; Leng, L.; Gandavadi, S.; Du, X.; Bucala, R.;
Jorgensen, W. L. Discovery of human macrophage migration inhibitory
factor (MIF)-CD74 antagonists via virtual screening. J. Med. Chem.
2009, 52, 416−424.
(12) Cho, Y.; Vermeire, J. J.; Merkel, J. S.; Leng, L.; Du, X.; Bucala,
R.; Cappello, M.; Lolis, E. Drug repositioning and pharmacophore
identification in the discovery of hookworm MIF inhibitors. Chem.
Biol. 2011, 18, 1089−1101.
(13) Senter, P. D.; Al-Abed, Y.; Metz, C. N.; Benigni, F.; Mitchell, R.
A.; Chesney, J.; Han, J.; Gartner, C. G.; Nelson, S. D.; Todaro, G. J.;
Bucala, R. Inhibition of macrophage migration inhibitory factor (MIF)
tautomerase and biological activities by acetaminophen metabolites.
Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 144−149.
(14) Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.;
Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. UCSF Chimeraa
visualization system for exploratory research and analysis. J. Comput.
Chem. 2004, 25, 1605−1612.
(29) Bernhagen, J.; Mitchell, R. A.; Calandra, T.; Voelter, W.;
Cerami, A.; Bucala, R. Purification, bioactivity, and secondary structure
analysis of mouse and human macrophage migration inhibitory factor
(MIF). Biochemistry 1994, 33, 14144−14155.
(30) Taylor, A. B.; Johnson, W. H., Jr.; Czerwinski, R. M.; Li, H. S.;
Marvin, L.; Hackert, M. L.; Whitman, C. P. Crystal structure of
macrophage migration inhibitory factor complexed with (E)-2-fluoro-
p-hydroxycinnamate at 1.8 Å resolution: implications for enzymatic
catalysis and inhibition. Biochemistry 1999, 38, 7444−7452.
(31) Baell, J. B.; G. A. Holloway, G. A. New substructure filters for
removal of pan assay interference compounds (PAINS) from
screening libraries and for their exclusion in bioassays. J. Med. Chem.
2010, 53, 2719−2740.
(32) Michel, J.; Tirado-Rives, J.; Jorgensen, W. L. Energetics of
displacing water molecules from protein binding sites: consequences
for ligand optimization. J. Am. Chem. Soc. 2009, 131, 15403−15411.
(33) Leung, C. S.; Leung, S. S. F.; Tirado-Rives, J.; Jorgensen, W. L.
Methyl effects on protein−ligand binding. J. Med. Chem. 2012, 55,
4489−4500.
(34) Cho, Y.; Crichlow, G. V.; Vermeire, J. J.; Leng, L.; Du, X.;
Hodsdon, M. E.; Bucala, R.; Cappello, M.; Gross., M.; Gaeta, F.;
Johnson, K.; Lolis, E. J. Allosteric inhibition of macrophage migration
inhibitory factor revealed by ibudilast. Proc. Natl. Acad. Sci. U.S.A.
2010, 107, 11313−11318.
(35) Hare, A. A.; Leng, L.; Gandavadi, S.; Du, X.; Cournia, Z.; Bucala,
R.; Jorgensen, W. L. Optimization of N-benzyl-benzoxazol-2-ones as
inhibitors of macrophage migration inhibitory factor (MIF). Bioorg.
Med. Chem. Lett. 2010, 20, 5811−5814.
(36) Jorgensen, W. L.; Gandavadi, S.; Du, X.; Hare, A. A.; Trofimov,
A.; Leng, L.; Bucala, R. Receptor agonists of macrophage migration
inhibitory factor. Bioorg. Med. Chem. Lett. 2010, 20, 7033−7036.
(37) Alam, A.; Haldar, S.; Thulasiram, H. V.; Kumar, R.; Goyal, M.;
Iqbal, M.; Pal, C.; Dey, S.; Bindu, S.; Sarkar, S.; Pal, U.; Maiti, N. C.;
Bandyopadhyay, U. Novel anti-inflammatory activity of epoxyazadir-
adione against macrophage migration inhibitory factor. J. Biol. Chem.
2012, 287, 24844−24861.
(15) 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.
(16) Schrodinger Suite 2009 Protein Preparation Wizard; Schrodinger,
̈
̈
LLC: New York, NY, 2009.
(17) LigPrep, version 2.5; Schrodinger, LLC: New York, NY, 2011.
̈
(18) Lipinski, C. A.; Lombardo, F.; Dominy, B. W.; Feeney, P. J.
Experimental and computational approaches to estimate solubility and
permeability in drug discovery and development settings. Adv. Drug
Delivery Rev. 2001, 46, 3−26.
(19) Jorgensen, W. L. QikProp, version 3.0; Schrodinger, LLC: New
York, 2006.
(20) Irwin, J. J.; Shoichet, B. K. ZINCa free database of
commercially available compounds for virtual screening. J. Chem. Inf.
Model. 2005, 45, 177−182.
(21) Friesner, R. A.; Banks, J. L.; Murphy, R. B.; Halgren, T. A.;
Klicic, J. J.; Mainz, D. T.; Repasky, M. P.; Knoll, E. H.; Shelley, M.;
Perry, J. K.; Shaw, D. E.; Francis, P.; Shenkin, P. S. Glide: a new
approach for rapid, accurate docking and scoring. 1. Method and
assessment of docking accuracy. J. Med. Chem. 2004, 47, 1739−1749.
(22) Friesner, R. A.; Murphy, R. B.; Repasky, M. P.; Frye, L. L.;
Greenwood, J. R.; Halgren, T. A.; Sanschagrin, P. C.; Mainz, D. T.
Extra precision Glide: docking and scoring incorporating a model of
hydrophobic enclosure for protein−ligand complexes. J. Med. Chem.
2006, 49, 6177−6196.
(23) Maestro, version 9.2; Schrodinger, LLC: New York, NY, 2011.
̈
(24) Terhorst, J. P.; Jorgensen, W. L. E/Z energetics for molecular
modeling and design. J. Chem. Theory Comput. 2010, 6, 2762−2769.
(25) 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.
(26) MacroModel, version 9.8; Schrodinger, LLC: New York, NY,
̈
2010.
(27) (a) Evans, D. A.; Katz, J. L.; West, T. R. Synthesis of diaryl
ethers through the copper-promoted arylation of phenols with
arylboronic acids. An expedient synthesis of thyroxine. Tetrahedron
Lett. 1998, 39, 2937−2940. (b) Tzschucke, C. C.; Murphy, J. M.;
Hartwig, J. F. Arenes to anilines and aryl ethers by sequential iridium-
catalyzed borylation and copper-catalyzed coupling. Org. Lett. 2007, 9,
761−764.
(28) Kamir, D.; Zierow, S.; Leng, L.; Cho, Y.; Diaz, Y.; Griffith, J.;
McDonald, C.; Merk, M.; Mitchell, R. A.; Trent, J.; Chen, Y.; Kwong,
Y.-K. A.; Xiong, H.; Vermeire, J.; Cappello, M.; McMahon-Pratt, D.;
Walker, J.; Bernhagen, J.; Lolis, E.; Bucala, R. A Leishmania ortholog of
macrophage migration inhibitory factor modulates host macrophage
responses. J. Immunol. 2008, 180, 8250−8261.
10159
dx.doi.org/10.1021/jm301269s | J. Med. Chem. 2012, 55, 10148−10159