A novel cofactor-binding mode in bacterial IMP dehydrogenases explains inhibitor selectivity

Journal of Biological Chemistry

Volumn 290, Issue 9, 2015, Pages 5893-5911

  Makowska Grzyska, Magdalena ^a   Kim, Youngchang ^a,b   Maltseva, Natalia ^a   Osipiuk, Jerzy ^a,b   Gu, Minyi ^a   Zhang, Minjia ^c   Mandapati, Kavitha ^c   Gollapalli, Deviprasad R ^c   Gorla, Suresh Kumar ^c   Hedstrom, Lizbeth ^c   Joachimiak, Andrzej ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL AGENTS; BACTERIA; BACTERIOLOGY; BIOCHEMISTRY;

ANTIBIOTIC RESISTANCE; BACILLUS ANTHRACIS; CAMPYLOBACTER JEJUNI; CLOSTRIDIUM PERFRINGENS; CONCOMITANT REDUCTION; GUANINE NUCLEOTIDES; INHIBITOR SELECTIVITY; PHYSIOLOGICAL ROLES;

BINDING ENERGY;

ADENOSINE; INOSINATE DEHYDROGENASE INHIBITOR; INOSINE PHOSPHATE; NICOTINAMIDE ADENINE DINUCLEOTIDE; OXIDOREDUCTASE; RIBONUCLEOTIDE; UNCLASSIFIED DRUG; XANTHOSINE 5' MONOPHOSPHATE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; ENZYME INHIBITOR; INOSINATE DEHYDROGENASE; PROTEIN BINDING;

ARTICLE; BACILLUS ANTHRACIS; BINDING AFFINITY; BINDING SITE; CAMPYLOBACTER JEJUNI; CLOSTRIDIUM PERFRINGENS; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME INHIBITION; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; VIBRIO CHOLERAE; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; CLOSTRIDIUM PERFRINGENS; EUKARYOTA; PROKARYOTA; VIBRIO CHOLERAE;

AMINO ACID SEQUENCE; ANTI-INFECTIVE AGENTS; BACILLUS ANTHRACIS; BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; CLOSTRIDIUM PERFRINGENS; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; IMP DEHYDROGENASE; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84923791158     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.619767     Document Type: Article

References (54)

1. Fischbach, M. A., and Walsh, C. T. (2009) Antibiotics for emerging pathogens. Science 325, 1089-1093
2. Kim, Y., Tesar, C., Mire, J., Jedrzejczak, R., Binkowski, A., Babnigg, G., Sacchettini, J., and Joachimiak, A. (2011) Structure of apo- and mono-metalated forms of NDM-1, a highly potent carbapenem-hydrolyzing metallo-B-lactamase. PLoS ONE 6, e24621
3. World Health Organization (2013) Global Tuberculosis Report, pp. 45-5.8
4. Hedstrom, L., Liechti, G., Goldberg, J. B., and Gollapalli, D. R. (2011) The antibiotic potential of prokaryotic IMP dehydrogenase inhibitors. Curr. Med. Chem. 18, 1909-1918
5. Gollapalli, D. R., Macpherson, I. S., Liechti, G., Gorla, S. K., Goldberg, J. B., and Hedstrom, L. (2010) Structural determinants of inhibitor selectivity in prokaryotic IMP dehydrogenases. Chem. Biol. 17, 1084-1091
6. Chen, L., Wilson, D. J., Xu, Y., Aldrich, C. C., Felczak, K., Sham, Y. Y., and Pankiewicz, K. W. (2010) Triazole-linked inhibitors of inosine monophosphate dehydrogenase from human and Mycobacterium tuberculosis. J. Med. Chem. 53, 4768-4778
7. Usha, V., Hobrath, J. V., Gurcha, S. S., Reynolds, R. C., and Besra, G. S. (2012) Identification of novel Mt-Guab2 inhibitor series active against M. tuberculosis. PLoS ONE 10.1371/journal.pone.0033886
8. Rao, V. A., Shepherd, S. M., Owen, R., and Hunter, W. N. (2013) Structure of Pseudomonas aeruginosa inosine 5′-monophosphate dehydrogenase. Acta Crystallogr. Sect. F Struct. Biol. Crystalliz. Commun. 69, 243-247
9. Mandapati, K., Gorla, S. K., House, A. L., McKenney, E. S., Zhang, M., Rao, S. N., Gollapalli, D. R., Mann, B. J., Goldberg, J. B., Cuny, G. D., Glomski, I. J., and Hedstrom, L. (2014) Repurposing Cryptosporidium inosine 5′-monophosphate dehydrogenase inhibitors as potential antibacterial agents. ACS Med. Chem. Lett. 5, 846-850
10. Hedstrom, L. (2009) IMP dehydrogenase: structure, mechanism, and inhibition. Chem. Rev. 109, 2903-2928
11. Makowska-Grzyska, M., Kim, Y., Wu, R., Wilton, R., Gollapalli, D. R., Wang, X. K., Zhang, R., Jedrzejczak, R., Mack, J. C., Maltseva, N., Mulligan, R., Binkowski, T. A., Gornicki, P., Kuhn, M. L., Anderson, W. F., Hedstrom, L., and Joachimiak, A. (2012) Bacillus anthracis inosine 5′-monophosphate dehydrogenase in action: the first bacterial series of structures of phosphate ion-, substrate-, and product-bound complexes. Biochemistry 51, 6148-6163
12. Wierenga, R. K. (2001) The TIM-barrel fold: a versatile framework for efficient enzymes. FEBS Lett. 492, 193-198
13. Bateman, A. (1997) The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem. Sci. 22, 12-13
14. Zhang, R., Evans, G., Rotella, F. J., Westbrook, E. M., Beno, D., Huberman, E., Joachimiak, A., and Collart, F. R. (1999) Characteristics and crystal structure of bacterial inosine 5′-monophosphate dehydrogenase. Biochemistry 38, 4691-4700
15. Gan, L., Seyedsayamdost, M. R., Shuto, S., Matsuda, A., Petsko, G. A., and Hedstrom, L. (2003) The immunosuppressive agent mizoribine monophosphate forms a transition state analogue complex with inosine monophosphate dehydrogenase. Biochemistry 42, 857-863
16. Nimmesgern, E., Black, J., Futer, O., Fulghum, J. R., Chambers, S. P., Brummel, C. L., Raybuck, S. A., and Sintchak, M. D. (1999) Biochemical analysis of the modular enzyme inosine 5′-monophosphate dehydrogenase. Protein Expr. Purif. 17, 282-289
17. Pimkin, M., and Markham, G. D. (2008) The CBS subdomain of inosine 5′-monophosphate dehydrogenase regulates purine nucleotide turnover. Mol. Microbiol. 68, 342-359
18. Colby, T. D., Vanderveen, K., Strickler, M. D., Markham, G. D., and Goldstein, B. M. (1999) Crystal structure of human type II inosine monophosphate dehydrogenase: implications for ligand binding and drug design. Proc. Natl. Acad. Sci. U.S.A. 96, 3531-3536
19. Prosise, G. L., and Luecke, H. (2003) Crystal structures of Tritrichomonas foetus inosine monophosphate dehydrogenase in complex with substrate, cofactor and analogs: a structural basis for the random-in ordered-out kinetic mechanism. J. Mol. Biol. 326, 517-527
20. + orients the active site loop for catalysis. Biochemistry 41, 13309-13317
21. Felczak, K., Chen, L., Wilson, D., Williams, J., Vince, R., Petrelli, R., Jayaram, H. N., Kusumanchi, P., Kumar, M., and Pankiewicz, K. W. (2011) Cofactor-type inhibitors of inosine monophosphate dehydrogenase via modular approach: targeting the pyrophosphate binding sub-domain. Bioorg. Med. Chem. 19, 1594-1605
22. Zhang, R., Evans, G., Rotella, F., Westbrook, E., Huberman, E., Joachimiak, A., and Collart, F. R. (1999) Differential signatures of bacterial and mammalian IMP dehydrogenase enzymes. Curr. Med. Chem. 6, 537-543
23. Pankiewicz, K. W., and Goldstein, B. M. (2003) in Inosine Monophosphate Dehydrogenase: A Major Therapeutic Target (Pankiewicz, K. W., and Goldstein, B. M., eds) pp. 1-17, American Chemical Society, Washington, D. C.
24. Umejiego, N. N., Gollapalli, D., Sharling, L., Volftsun, A., Lu, J., Benjamin, N. N., Stroupe, A. H., Riera, T. V., Striepen, B., and Hedstrom, L. (2008) Targeting a prokaryotic protein in a eukaryotic pathogen: identification of lead compounds against cryptosporidiosis. Chem. Biol. 15, 70-77
25. Sharling, L., Liu, X., Gollapalli, D. R., Maurya, S. K., Hedstrom, L., and Striepen, B. (2010) A screening pipeline for antiparasitic agents targeting Cryptosporidium inosine monophosphate dehydrogenase. PLoS Negl. Trop. Dis. 4, e794
26. Maurya, S. K., Gollapalli, D. R., Kirubakaran, S., Zhang, M., Johnson, C. R., Benjamin, N. N., Hedstrom, L., and Cuny, G. D. (2009) Triazole inhibitors of Cryptosporidium parvum inosine 5′-monophosphate dehydrogenase. J. Med. Chem. 52, 4623-4630
27. Kirubakaran, S., Gorla, S. K., Sharling, L., Zhang, M., Liu, X., Ray, S. S., Macpherson, I. S., Striepen, B., Hedstrom, L., and Cuny, G. D. (2012) Structure-activity relationship study of selective benzimidazole-based inhibitors of Cryptosporidium parvum IMPDH. Bioorg. Med. Chem. Lett. 22, 1985-1988
28. Gorla, S. K., Kavitha, M., Zhang, M., Chin, J. E., Liu, X., Striepen, B., Makowska-Grzyska, M., Kim, Y., Joachimiak, A., Hedstrom, L., and Cuny, G. D. (2013) Optimization of benzoxazole-based inhibitors of Cryptosporidium parvum inosine 5′-monophosphate dehydrogenase. J. Med. Chem. 56, 4028-4043
29. Johnson, C. R., Gorla, S. K., Kavitha, M., Zhang, M., Liu, X., Striepen, B., Mead, J. R., Cuny, G. D., and Hedstrom, L. (2013) Phthalazinone inhibitors of inosine-5′-monophosphate dehydrogenase from Cryptosporidium parvum. Bioorg. Med. Chem. Lett. 23, 1004-1007
30. Gorla, S. K., Kavitha, M., Zhang, M., Liu, X., Sharling, L., Gollapalli, D. R., Striepen, B., Hedstrom, L., and Cuny, G. D. (2012) Selective and potent urea inhibitors of Cryptosporidium parvum inosine 5′-monophosphate dehydrogenase. J. Med. Chem. 55, 7759-7771
31. Macpherson, I. S., Kirubakaran, S., Gorla, S. K., Riera, T. V., D'Aquino, J. A., Zhang, M., Cuny, G. D., and Hedstrom, L. (2010) The structural basis of Cryptosporidium-specific IMP dehydrogenase inhibitor selectivity. J. Am. Chem. Soc. 132, 1230-1231
32. Geiser, M., Cèbe, R., Drewello, D., and Schmitz, R. (2001) Integration of PCR fragments at any specific site within cloning vectors without the use of restriction enzymes and DNA ligase. BioTechniques 31, 88-90
33. Kim, Y., Babnigg, G., Jedrzejczak, R., Eschenfeldt, W. H., Li, H., Maltseva, N., Hatzos-Skintges, C., Gu, M., Makowska-Grzyska, M., Wu, R., An, H., Chhor, G., and Joachimiak, A. (2011) High-throughput protein purification and quality assessment for crystallization. Methods 55, 12-28
34. Rosenbaum, G., Alkire, R. W., Evans, G., Rotella, F. J., Lazarski, K., Zhang, R. G., Ginell, S. L., Duke, N., Naday, I., Lazarz, J., Molitsky, M. J., Keefe, L., Gonczy, J., Rock, L., Sanishvili, R., Walsh, M. A., Westbrook, E., and Joachimiak, A. (2006) The structural biology center 19ID undulator beamline: facility specifications and protein crystallographic results. J. Synchrotron Radiat. 13, 30-45
35. Minor, W., Cymborowski, M., Otwinowski, Z., and 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, 859-866
36. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
37. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
38. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
39. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
40. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57, 122-133
41. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
42. Kerr, K. M., Digits, J. A., Kuperwasser, N., and Hedstrom, L. (2000) Asp338 controls hydride transfer in Escherichia coli IMP dehydrogenase. Biochemistry 39, 9804-9810
43. Albini, A., and Alpegiani, M. (1984) The photochemistry of the N-oxide function. Chem. Rev. 84, 43-71
44. Brown, G. B., Levin, G., and Murphy, S. (1964) Purine N-oxides. XII. Photochemical changes induced by ultraviolet radiation. Biochemistry 3, 880-883
45. Riera, T. V., Zheng, L., Josephine, H. R., Min, D., Yang, W., and Hedstrom, L. (2011) Allosteric activation via kinetic control: potassium accelerates a conformational change in IMP dehydrogenase. Biochemistry 50, 8508-8518
46. Sintchak, M. D., Fleming, M. A., Futer, O., Raybuck, S. A., Chambers, S. P., Caron, P. R., Murcko, M. A., and Wilson, K. P. (1996) Structure and mechanism of inosine monophosphate dehydrogenase in complex with the immunosuppressant mycophenolic acid. Cell 85, 921-930
47. Trzhtsinskaya, B. V., and Abramova, N. D. (1991) Imidazole-2-thiones: synthesis, structure, properties. Sulfur Rep. 10, 389-430
48. Rossman, M. G., Liljas, A., Branden, C.-I., Banaszak, L. J., and Paul, D. B. (1975) in The Enzymes (Boyer, P. D., ed) pp. 61-102 Academic Press, New York
49. Bell, C. E., Yeates, T. O., and Eisenberg, D. (1997) Unusual conformation of nicotinamide adenine dinucleotide (NAD) bound to diphtheria toxin:A comparison with NAD bound to the oxidoreductase enzymes. Protein Sci. 6, 2084-2096
50. Kuppuraj, G., Sargsyan, K., Hua, Y.-H., Merrill, A. R., and Lim, C. (2011) Linking distinct conformations of nicotinamide adenine dinucleotide with protein fold/function. J. Phys. Chem. B 115, 7932-7939
51. 8 barrel enzymes. Nat. Chem. Biol. 7, 950-958
52. Giangreco, I., and Packer, M. J. (2013) Pharmacophore binding motifs for nicotinamide adenine dinucleotide analogues across multiple protein families: a detailed contact-based analysis of the interaction between proteins and NAD(P) cofactors. J. Med. Chem. 56, 6175-6189
53. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890
54. Robert, X., and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320-W324