Structural interactions dictate the kinetics of macrophage migration inhibitory factor inhibition by different cancer-preventive isothiocyanates

Biochemistry

Volumn 51, Issue 38, 2012, Pages 7506-7514

  Crichlow, Gregg V ^a,c   Fan, Chengpeng ^a   Keeler, Camille ^a   Hodsdon, Michael ^a   Lolis, Elias J ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE CANCER CENTER   (United States)

^c Innovimmune Biotherapeutics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIAPOPTOTIC PROPERTIES; BINDING MODES; BIOLOGICAL INTERACTIONS; CANCER DEVELOPMENT; CELLULAR PROCESS; CRYSTALLOGRAPHIC STRUCTURE; HETERONUCLEAR SINGLE-QUANTUM COHERENCES; ISOTHIOCYANATES; MIGRATION INHIBITORY FACTORS; SECOND-ORDER RATE CONSTANTS; STRUCTURAL FEATURE; STRUCTURAL INTERACTIONS; STRUCTURE ACTIVITY RELATIONSHIPS; SUBUNIT INTERFACES;

BINDING ENERGY; MACROPHAGES; NUTRIENTS; QUANTUM THEORY; RATE CONSTANTS;

DISEASES;

MACROPHAGE MIGRATION INHIBITION FACTOR; PHENETHYL ISOTHIOCYANATE; RECOMBINANT PROTEIN; SULFORAPHANE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PREVENTION; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG PROTEIN BINDING; DRUG STRUCTURE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

CRYSTALLIZATION; HUMANS; ISOTHIOCYANATES; KINETICS; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MODELS, MOLECULAR; NEOPLASMS; PROTEIN CONFORMATION;

BRASSICA OLERACEA VAR. ITALICA; NASTURTIUM OFFICINALE;

EID: 84866720451     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3005494     Document Type: Article

References (42)

1. de Jong, Y. P., Abadia-Molina, A. C., Satoskar, A. R., Clarke, K., Rietdijk, S. T., Faubion, W. A., Mizoguchi, E., Metz, C. N., Alsahli, M., ten Hove, T., Keates, A. C., Lubetsky, J. B., Farrell, R. J., Michetti, P., van Deventer, S. J., Lolis, E., David, J. R., Bhan, A. K., Terhorst, C., and Sahli, M. A. (2001) Development of chronic colitis is dependent on the cytokine MIF Nat. Immunol. 2, 1061-1066
2. Schrader, J., Deuster, O., Rinn, B., Schulz, M., Kautz, A., Dodel, R., Meyer, B., Al-Abed, Y., Balakrishnan, K., Reese, J., and Bacher, M. (2009) Restoration of contact inhibition in human glioblastoma cell lines after MIF knockdown BMC Cancer 9, 464
3. Zhang, Y., Zeng, X., Chen, S., Zhang, Z., Li, P., Yi, W., Huang, H., Yao, J., Li, S., and Hu, C. (2011) Characterization, epitope identification and mechanisms of the anti-septic capacity of monoclonal antibodies against macrophage migration inhibitory factor Int. Immunopharmacol. 11, 1333-1340
4. Crichlow, G. V., Cheng, K. F., Dabideen, D., Ochani, M., Aljabari, B., Pavlov, V. A., Miller, E. J., Lolis, E., and Al-Abed, Y. (2007) Alternative chemical modifications reverse the binding orientation of a pharmacophore scaffold in the active site of macrophage migration inhibitory factor J. Biol. Chem. 282, 23089-23095
5. Winner, M., Meier, J., Zierow, S., Rendon, B. E., Crichlow, G. V., Riggs, R., Bucala, R., Leng, L., Smith, N., Lolis, E., Trent, J. O., and Mitchell, R. A. (2008) A Novel, Macrophage Migration Inhibitory Factor Suicide Substrate Inhibits Motility and Growth of Lung Cancer Cells Cancer Res. 68, 7253-7257
6. Fingerle-Rowson, G., Kaleswarapu, D. R., Schlander, C., Kabgani, N., Brocks, T., Reinart, N., Busch, R., Schutz, A., Lue, H., Du, X., Liu, A., Xiong, H., Chen, Y., Nemajerova, A., Hallek, M., Bernhagen, J., Leng, L., and Bucala, R. (2009) A Tautomerase-null MIF Gene Knock-in Mouse Reveals that Protein Interactions and not Enzymatic Activity Mediate MIF-dependent Growth Regulation Mol. Cell. Biol. 29, 1922-1932
7. Ouertatani-Sakouhi, H., El-Turk, F., Fauvet, B., Cho, M.-K., Pinar Karpinar, D., Le Roy, D., Dewor, M., Roger, T., Bernhagen, J., Calandra, T., Zweckstetter, M., and Lashuel, H. A. (2010) Identification and Characterization of Novel Classes of Macrophage Migration Inhibitory Factor (MIF) Inhibitors with Distinct Mechanisms of Action J. Biol. Chem. 285, 26581-26598
8. Brown, K. K., Blaikie, F. H., Smith, R. A., Tyndall, J. D., Lue, H., Bernhagen, J., Winterbourn, C. C., and Hampton, M. B. (2009) Direct modification of the proinflammatory cytokine macrophage migration inhibitory factor by dietary isothiocyanates J. Biol. Chem. 284, 32425-32433
9. Cross, J. V., Rady, J. M., Foss, F. W., Lyons, C. E., Macdonald, T. L., and Templeton, D. J. (2009) Nutrient isothiocyanates covalently modify and inhibit the inflammatory cytokine macrophage migration inhibitory factor (MIF) Biochem. J. 423, 315-321
10. Ouertatani-Sakouhi, H., El-Turk, F., Fauvet, B., Roger, T., Le Roy, D., Karpinar, D. P., Leng, L., Bucala, R., Zweckstetter, M., Calandra, T., and Lashuel, H. A. (2009) A new class of isothiocyanate-based irreversible inhibitors of macrophage migration inhibitory factor Biochemistry 48, 9858-9870
11. Wattenberg, L. W. (1981) Inhibition of carcinogen-induced neoplasia by sodium cyanate, tert-butyl isocyanate, and benzyl isothiocyanate administered subsequent to carcinogen exposure Cancer Res. 41, 2991-2994
12. Yang, M. D., Lai, K. C., Lai, T. Y., Hsu, S. C., Kuo, C. L., Yu, C. S., Lin, M. L., Yang, J. S., Kuo, H. M., Wu, S. H., and Chung, J. G. (2010) Phenethyl isothiocyanate inhibits migration and invasion of human gastric cancer AGS cells through suppressing MAPK and NF-κB signal pathways Anticancer Res. 30, 2135-2143
13. Dey, M., Kuhn, P., Ribnicky, D., Premkumar, V., Reuhl, K., and Raskin, I. (2010) Dietary phenethylisothiocyanate attenuates bowel inflammation in mice BMC Chem. Biol. 10, 4
14. Higdon, J. V., Delage, B., Williams, D. E., and Dashwood, R. H. (2007) Cruciferous vegetables and human cancer risk: Epidemiologic evidence and mechanistic basis Pharmacol. Res. 55, 224-236
15. Tang, L., Zirpoli, G. R., Guru, K., Moysich, K. B., Zhang, Y., Ambrosone, C. B., and McCann, S. E. (2010) Intake of cruciferous vegetables modifies bladder cancer survival Cancer Epidemiol., Biomarkers Prev. 19, 1806-1811
16. Tang, L., Zirpoli, G. R., Jayaprakash, V., Reid, M. E., McCann, S. E., Nwogu, C. E., Zhang, Y., Ambrosone, C. B., and Moysich, K. B. (2010) Cruciferous vegetable intake is inversely associated with lung cancer risk among smokers: A case-control study BMC Cancer 10, 162
17. Jakubikova, J., Cervi, D., Ooi, M., Kim, K., Nahar, S., Klippel, S., Cholujova, D., Leiba, M., Daley, J. F., Delmore, J., Negri, J., Blotta, S., McMillin, D. W., Hideshima, T., Richardson, P. G., Sedlak, J., Anderson, K. C., and Mitsiades, C. S. (2011) Anti-tumor activity and signaling events triggered by the isothiocyanates, sulforaphane and phenethyl isothiocyanate, in multiple myeloma Haematologica 96, 1170-1179
18. Musk, S. R., Astley, S. B., Edwards, S. M., Stephenson, P., Hubert, R. B., and Johnson, I. T. (1995) Cytotoxic and clastogenic effects of benzyl isothiocyanate towards cultured mammalian cells Food Chem. Toxicol. 33, 31-37
19. Dinkova-Kostova, A. T., Fahey, J. W., Wade, K. L., Jenkins, S. N., Shapiro, T. A., Fuchs, E. J., Kerns, M. L., and Talalay, P. (2007) Induction of the phase 2 response in mouse and human skin by sulforaphane-containing broccoli sprout extracts Cancer Epidemiol., Biomarkers Prev. 16, 847-851
20. Guo, Z., Smith, T. J., Wang, E., Sadrieh, N., Ma, Q., Thomas, P. E., and Yang, C. S. (1992) Effects of phenethyl isothiocyanate, a carcinogenesis inhibitor, on xenobiotic-metabolizing enzymes and nitrosamine metabolism in rats Carcinogenesis 13, 2205-2210
21. Trachootham, D., Zhang, H., Zhang, W., Feng, L., Du, M., Zhou, Y., Chen, Z., Pelicano, H., Plunkett, W., Wierda, W. G., Keating, M. J., and Huang, P. (2008) Effective elimination of fludarabine-resistant CLL cells by PEITC through a redox-mediated mechanism Blood 112, 1912-1922
22. Okazaki, K., Umemura, T., Imazawa, T., Nishikawa, A., Masegi, T., and Hirose, M. (2003) Enhancement of urinary bladder carcinogenesis by combined treatment with benzyl isothiocyanate and N-butyl-N-(4-hydroxybutyl)nitrosamine in rats after initiation Cancer Sci. 94, 948-952
23. Okazaki, K., Yamagishi, M., Son, H. Y., Imazawa, T., Furukawa, F., Nakamura, H., Nishikawa, A., Masegi, T., and Hirose, M. (2002) Simultaneous treatment with benzyl isothiocyanate, a strong bladder promoter, inhibits rat urinary bladder carcinogenesis by N-butyl-N-(4-hydroxybutyl)nitrosamine Nutr. Cancer 42, 211-216
24. Zanichelli, F., Capasso, S., Cipollaro, M., Pagnotta, E., Carteni, M., Casale, F., Iori, R., and Galderisi, U. (2012) Dose-dependent effects of R-sulforaphane isothiocyanate on the biology of human mesenchymal stem cells, at dietary amounts, it promotes cell proliferation and reduces senescence and apoptosis, while at anti-cancer drug doses, it has a cytotoxic effect Age (Dordrecht, Neth.) 34, 281-293
25. Crichlow, G. V., Lubetsky, J. B., Leng, L., Bucala, R., and Lolis, E. J. (2009) Structural and kinetic analyses of macrophage migration inhibitory factor active site interactions Biochemistry 48, 132-139
26. 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., and Lolis, E. J. (2010) Allosteric inhibition of macrophage migration inhibitory factor revealed by ibudilast Proc. Natl. Acad. Sci. U.S.A. 107, 11313-11318
27. Otwinowski, Z. and Minor, W. (1997) Processing of X-Ray Diffraction Data Collected in Oscillation Mode Methods Enzymol. 276, 307-325
28. Collaborative Computational, Project Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
29. Navaza, J. (2001) Implementation of molecular replacement in AMoRe Acta Crystallogr. D57, 1367-1372
30. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D54, 905-921
31. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66, 486-501
32. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
33. Goddard, T. D. and Kneller, D. F. (2008) Sparky 3, University of California, San Francisco.
34. Edman, P. (1949) A method for the determination of amino acid sequence in peptides Arch. Biochem. 22, 475
35. Le, Z. G., Chen, Z. C., Hu, Y., and Zheng, Q. G. (2005) Organic reactions in ionic liquids: Ionic liquid-promoted efficient synthesis of disubstituted and trisubstituted thioureas derivatives Chin. Chem. Lett. 16, 201-204
36. Swope, M., Sun, H. W., Blake, P. R., and Lolis, E. (1998) Direct link between cytokine activity and a catalytic site for macrophage migration inhibitory factor EMBO J. 17, 3534-3541
37. Jorgensen, W. L., Gandavadi, S., Du, X., Hare, A. A., Trofimov, A., Leng, L., and Bucala, R. (2010) Receptor agonists of macrophage migration inhibitory factor Bioorg. Med. Chem. Lett. 20, 7033-7036
38. Cho, Y., Jones, B. F., Vermeire, J. J., Leng, L., DiFedele, L., Harrison, L. M., Xiong, H., Kwong, Y. K., Chen, Y., Bucala, R., Lolis, E., and Cappello, M. (2007) Structural and functional characterization of a secreted hookworm Macrophage Migration Inhibitory Factor (MIF) that interacts with the human MIF receptor CD74 J. Biol. Chem. 282, 23447-23456
39. Cho, Y., Vermeire, J. J., Merkel, J. S., Leng, L., Du, X., Bucala, R., Cappello, M., and Lolis, E. (2011) Drug repositioning and pharmacophore identification in the discovery of hookworm MIF inhibitors Chem. Biol. 18, 1089-1101
40. Bernhagen, J., Krohn, R., Lue, H., Gregory, J. L., Zernecke, A., Koenen, R. R., Dewor, M., Georgiev, I., Schober, A., Leng, L., Kooistra, T., Fingerle-Rowson, G., Ghezzi, P., Kleemann, R., McColl, S. R., Bucala, R., Hickey, M. J., and Weber, C. (2007) MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment Nat. Med. 13, 587-596
41. Merk, M., Baugh, J., Zierow, S., Leng, L., Pal, U., Lee, S. J., Ebert, A. D., Mizue, Y., Trent, J. O., Mitchell, R., Nickel, W., Kavathas, P. B., Bernhagen, J., and Bucala, R. (2009) The Golgi-Associated Protein p115 Mediates the Secretion of Macrophage Migration Inhibitory Factor J. Immunol. 182, 6896-6906
42. Engh, R. A. and Huber, R. (1991) Accurate bond and angle parameters for X-ray protein structure refinement Acta Crystallogr. A47, 392-400