Solvent-assisted slow conversion of a dithiazole derivative produces a competitive inhibitor of peptide deformylase

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 4, 2010, Pages 704-713

  Berg, Alexander K ^a   Yu, Qingfeng ^a   Qian, Steven Y ^a   Haldar, Manas K ^a   Srivastava, D K ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

Inhibitor; Peptide deformylase; Slow inhibition; Thiadiazole

Indexed keywords

2 AMINO 5 MERCAPTO 1,3,4 THIADIAZOLE; ANTIBIOTIC AGENT; HYDROGEN PEROXIDE; N,N DIMETHYLFORMAMIDE; PEPTIDE DEFORMYLASE; PEPTIDE DEFORMYLASE INHIBITOR; THIADIAZOLE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; COMPETITIVE INHIBITION; DIMERIZATION; DISULFIDE BOND; DRUG BINDING; DRUG SYNTHESIS; ENZYME INHIBITION; HUMAN; OXIDATION; PRIORITY JOURNAL;

AMIDOHYDROLASES; CATALYTIC DOMAIN; DIMETHYLFORMAMIDE; DRUG DESIGN; ENZYME INHIBITORS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, MOLECULAR; RECOMBINANT PROTEINS; SOLVENTS; THIADIAZOLES;

EID: 76849101051     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2009.11.006     Document Type: Article

References (61)

1. Marcker K., and Sanger F. N-formyl-methionyl-S-RNA. J. Mol. Biol. 8 (1964) 835-840
2. Meinnel T., Mechulam Y., and Blanquet S. Methionine as translation start signal: a review of the enzymes of the pathway in Escherichia coli. Biochimie 75 (1993) 1061-1075
3. Giglione C., and Meinnel T. Organellar peptide deformylases: universality of the N-terminal methionine cleavage mechanism. Trends Plant Sci. 6 (2001) 566-572
4. Giglione C., Vallon O., and Meinnel T. Control of protein life-span by N-terminal methionine excision. EMBO J. 22 (2003) 13-23
5. Bingel-Erlenmeyer R., Kohler R., Kramer G., Sandikci A., Antolić S., Maier T., Schaffitzel C., Wiedmann B., Bukau B., and Ban N. A peptide deformylase-ribosome complex reveals mechanism of nascent chain processing. Nature 452 (2008) 108-111
6. Giglione C., Fieulaine S., and Meinnel T. Cotranslational processing mechanisms: towards a dynamic 3D model. Trends Biochem. Sci. 34 (2009) 417-426
7. Giglione C., Boularot A., and Meinnel T. Protein N-terminal methionine excision. Cell. Mol. Life Sci. 61 (2004) 1455-1474
8. Giglione C., and Meinnel T. Peptide deformylase as an emerging target for antiparasitic agents. Expert Opin. Ther. Targets 5 (2001) 41-57
9. Serero A., Giglione C., Sardini A., Martinez-Sanz J., and Meinnel T. An unusual peptide deformylase features in the human mitochondrial N-terminal methionine excision pathway. J. Biol. Chem. 278 (2003) 52953-52963
10. Lee M.D., Antczak C., Li Y., Sirotnak F.M., Bornmann W.G., and Scheinberg D.A. A new human peptide deformylase inhibitable by actinonin. Biochem. Biophys. Res. Commun. 312 (2003) 309-315
11. Lee M.D., She Y., Soskis M.J., Borella C.P., Gardner J.R., Hayes P.A., Dy B.M., Heaney M.L., Philips M.R., Bornmann W.G., Sirotnak F.M., and Scheinberg D.A. Human mitochondrial peptide deformylase, a new anticancer target of actinonin-based antibiotics. J. Clin. Invest. 114 (2004) 1107-1116
12. Von Jagow G., Schägger H., Engel W.D., Machleidt W., Machleidt I., and Kolb H.J. Beef heart complex III: isolation and characterization of cytochrome B. FEBS Lett. 91 (1978) 121-125
13. Tanaka M., Yasunobu K.T., Wei Y.H., and King T.E. The complete amino acid sequence of bovine heart cytochrome oxidase subunit VI. J. Biol. Chem. 256 (1981) 4832-4837
14. Nguyen K.T., Hu X., Colton C., Chakrabarti R., Zhu M.X., and Pei D. Characterization of a human peptide deformylase: implications for antibacterial drug design. Biochemistry 42 (2003) 9952-9958
15. Adams J.M. On the release of the formyl group from nascent protein. J. Mol. Biol. 33 (1968) 571-589
16. Yuan Z., and White R.J. The evolution of peptide deformylase as a target: contribution of biochemistry, genetics and genomics. Biochem. Pharmacol. 71 (2006) 1042-1047
17. Giglione C., Pierre M., and Meinnel T. Peptide deformylase as a target for new generation, broad spectrum antimicrobial agents. Mol. Microbiol. 36 (2000) 1197-1205
18. Meinnel T., and Blanquet S. Characterization of the Thermus thermophilus locus encoding peptide deformylase and methionyl-tRNA(fMet) formyltransferase. J. Bacteriol. 176 (1994) 7387-7390
19. Mazel D., Pochet S., and Marlière P. Genetic characterization of polypeptide deformylase, a distinctive enzyme of eubacterial translation. EMBO J. 13 (1994) 914-923
20. Bandow J.E., Becher D., Büttner K., Hochgräfe F., Freiberg C., Brötz H., and Hecker M. The role of peptide deformylase in protein biosynthesis: a proteomic study. Proteomics 3 (2003) 299-306
21. Wang W., White R., and Yuan Z. Proteomic study of peptide deformylase inhibition in Streptococcus pneumoniae and Staphylococcus aureus. Antimicrob Agents Chemother. 50 (2006) 1656-1663
22. Guay D.R.P. Drug forecast-the peptide deformylase inhibitors as antibacterial agents. Ther. Clin. Risk Manag. 3 (2007) 513-525
23. Chen D.Z., Patel D.V., Hackbarth C.J., Wang W., Dreyer G., Young D.C., Margolis P.S., Wu C., Ni Z.J., Trias J., White R.J., and Yuan Z. Actinonin, a naturally occurring antibacterial agent, is a potent deformylase inhibitor. Biochemistry 39 (2000) 1256-1262
24. Broughton B.J., Chaplen P., Freeman W.A., Warren P.J., Wooldridge K.R., and Wright D.E. Studies concerning the antibiotic actinonin. Part VIII. Structure-activity relationships in the actinonin series. J. Chem. Soc. Perkin 1 (1975) 857-860
25. Jain R., Chen D., White R.J., Patel D.V., and Yuan Z. Bacterial peptide deformylase inhibitors: a new class of antibacterial agents. Curr. Med. Chem. 12 (2005) 1607-1621
26. Kola I., and Landis J. Can the pharmaceutical industry reduce attrition rates?. Nat. Rev. Drug Discov. 3 (2004) 711-715
27. Caldwell J., Gardner I., and Swales N. An introduction to drug disposition: the basic principles of absorption, distribution, metabolism, and excretion. Toxicol. Pathol. 23 (1995) 102-114
28. Clements J.M., Beckett R.P., Brown A., Catlin G., Lobell M., Palan S., Thomas W., Whittaker M., Wood S., Salama S., Baker P.J., Rodgers H.F., Barynin V., Rice D.W., and Hunter M.G. Antibiotic activity and characterization of BB-3497, a novel peptide deformylase inhibitor. Antimicrob. Agents Chemother. 45 (2001) 563-570
29. Becker A., Schlichting I., Kabsch W., Groche D., Schultz S., and Wagner A.F. Iron center, substrate recognition and mechanism of peptide deformylase. Nat. Struct. Biol. 5 (1998) 1053-1058
30. Hao B., Gong W., Rajagopalan P.T., Zhou Y., Pei D., and Chan M.K. Structural basis for the design of antibiotics targeting peptide deformylase. Biochemistry 38 (1999) 4712-4719
31. Ragusa S., Mouchet P., Lazennec C., Dive V., and Meinnel T. Substrate recognition and selectivity of peptide deformylase. Similarities and differences with metzincins and thermolysin. J. Mol. Biol. 289 (1999) 1445-1457
32. Guilloteau J., Mathieu M., Giglione C., Blanc V., Dupuy A., Chevrier M., Gil P., Famechon A., Meinnel T., and Mikol V. The crystal structures of four peptide deformylases bound to the antibiotic actinonin reveal two distinct types: a platform for the structure-based design of antibacterial agents. J. Mol. Biol. 320 (2002) 951-962
33. Van Aller G.S., Nandigama R., Petit C.M., DeWolf W.E.J., Quinn C.J., Aubart K.M., Zalacain M., Christensen S.B., Copeland R.A., and Lai Z. Mechanism of time-dependent inhibition of polypeptide deformylase by actinonin. Biochemistry 44 (2005) 253-260
34. Berg A.K., and Srivastava D.K. Delineation of alternative conformational states in Escherichia coli peptide deformylase via thermodynamic studies for the binding of actinonin. Biochemistry 48 (2009) 1584-1594
35. Malkhasian A.Y.S., Finch M.E., Nikolovski B., Menon A., Kucera B.E., and Chavez F.A. N,N′-dimethylformamide-derived products from catalytic oxidation of 3-hydroxyflavone. Inorg. Chem. 46 (2007) 2950-2952
36. Vilsmeier A., and Haack A. Über die einwirkung von halogenphosphor auf alkyl-formanilide. Eine neue methode zur darstellung sekundärer und tertiärer p-alkylamino-benzaldehyde. Chem. Ber. 60 (1927) 119-122
37. Freeman F., and Keindl M. A facile synthesis of s-(1-chloroalkyl) alkanesulfonothioates. Synthesis 6 (1984) 500-502
38. Berg A.K., Manokaran S., Eiler D., Kooren J., Mallik S., and Srivastava D.K. Energetic rationale for an unexpected and abrupt reversal of guanidinium chloride-induced unfolding of peptide deformylase. Protein Sci. 17 (2008) 11-15
39. Ragusa S., Blanquet S., and Meinnel T. Control of peptide deformylase activity by metal cations. J. Mol. Biol. 280 (1998) 515-523
40. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem 72 (1976) 248-254
41. Rajagopalan P.T., Datta A., and Pei D. Purification, characterization, and inhibition of peptide deformylase from Escherichia coli. Biochemistry 36 (1997) 13910-13918
42. Wei Y., and Pei D. Continuous spectrophotometric assay of peptide deformylase. Anal. Biochem. 250 (1997) 29-34
43. Sculley M.J., Morrison J.F., and Cleland W.W. Slow-binding inhibition: the general case. Biochim. Biophys. Acta 1298 (1996) 78-86
44. Tian W.X., and Tsou C.L. Determination of the rate constant of enzyme modification by measuring the substrate reaction in the presence of the modifier. Biochemistry 21 (1982) 1028-1032
45. Mathes R.A., and Beber A.J. A synthesis of 2-thiazolethiol and its disulfide. J. Amer. Chem. Soc. 70 (1948) 1451-1452
46. Morris G., Goodsell D., Halliday R., Huey R., Hart W., Belew A., and Olson A. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. Comp. Chem. 19 (1998) 1639-1662
47. Huey R., Morris G.M., Olson A.J., and Goodsell D.S. A semiempirical free energy force field with charge-based desolvation. J. Comput. Chem. 28 (2007) 1145-1152
48. Musiani F., Arnofi E., Casadio R., and Ciurli S. Structure-based computational study of the catalytic and inhibition mechanisms of urease. J. Biol. Inorg. Chem. 6 (2001) 300-314
49. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
50. Chu M., Mierzwa R., He L., Xu L., Gentile G., Terracciano J., Patel M., Miesel L., Bohanon S., Kravec C., Cramer C., Fischman T.O., Hruza A., Ramanathan L., Shipkova P., and Chan T.M. Isolation and structure elucidation of two novel deformylase inhibitors produced by Streptomyces sp. Tetrahed. Lett. 42 (2001) 3549-3551
51. Grant S.K., Green B.G., and Kozarich J.W. Inhibition and structure-activity studies of methionine hydroxamic acid derivatives with bacterial peptide deformylase. Bioorg. Chem. 29 (2001) 211-222
52. Madison V., Duca J., Bennett F., Bohanon S., Cooper A., Chu M., Desai J., Girijavallabhan V., Hare R., Hruza A., Hendrata S., Huang Y., Kravec C., Malcolm B., McCormick J., Miesel L., Ramanathan L., Reichert P., Saksena A., Wang J., Weber P.C., Zhu H., and Fischmann T. Binding affinities and geometries of various metal ligands in peptide deformylase inhibitors. Biophys. Chem. 101-102 (2002) 239-247
53. Nguyen K.T., Hu X., and Pei D. Slow-binding inhibition of peptide deformylase by cyclic peptidomimetics as revealed by a new spectrophotometric assay. Bioorg. Chem. 32 (2004) 178-191
54. Hu X., Nguyen K.T., Jiang V.C., Lofland D., Moser H.E., and Pei D. Macrocyclic inhibitors for peptide deformylase: a structure-activity relationship study of the ring size. J. Med. Chem. 47 (2004) 4941-4949
55. Boularot A., Giglione C., Petit S., Duroc Y., Alves de Sousa R., Larue V., Cresteil T., Dardel F., Artaud I., and Meinnel T. Discovery and refinement of a new structural class of potent peptide deformylase inhibitors. J. Med. Chem. 50 (2007) 10-20
56. Shen G., Zhu J., Simpson A.M., and Pei D. Design and synthesis of macrocyclic peptidyl hydroxamates as peptide deformylase inhibitors. Bioorg. Med. Chem. Lett. 18 (2008) 3060-3063
57. Segel I.H. Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems (1975), John Wiley and Sons, Inc., New York
58. Bernhard S.A. The coupling of conformational changes to function in proteins. Stud. Org. Chem. 10 (1982) 237-252
59. Johnson J.K., Wang Z.X., and Srivastava D.K. Mechanistic investigation of medium-chain fatty acyl-CoA dehydrogenase utilizing 3-indolepropionyl/acryloyl-CoA as chromophoric substrate analogues. Biochemistry 31 (1992) 10564-10575
60. Johnson J.K., and Srivastava D.K. Detection and identification of a chromophoric intermediate during the medium-chain fatty acyl-CoA dehydrogenase-catalyzed reaction via rapid-scanning UV/visible spectroscopy. Biochemistry 32 (1993) 8004-8013
61. Rajagopalan P.T., Grimme S., and Pei D. Characterization of cobalt(II)-substituted peptide deformylase: function of the metal ion and the catalytic residue Glu-133. Biochemistry 39 (2000) 779-790