Peptide deformylase inhibitors as potent antimycobacterial agents

Antimicrobial Agents and Chemotherapy

Volumn 50, Issue 11, 2006, Pages 3665-3673

  Teo, Jeanette W P ^a,d   Thayalan, Pamela ^a   Beer, David ^a   Yap, Amelia S L ^a   Nanjundappa, Mahesh ^a   Ngew, Xinyi ^a   Duraiswamy, Jeyaraj ^a   Liung, Sarah ^a   Dartois, Veronique ^a   Schreiber, Mark ^a   Hasan, Samiul ^a   Cynamon, Michael ^b   Ryder, Neil S ^c   Yang, Xia ^c   Weidmann, Beat ^c   Bracken, Kathryn ^c   Dick, Thomas ^a   Mukherjee, Kakoli ^a  

^a NOVARTIS INSTITUTE FOR TROPICAL DISEASES   (Singapore)

^b Central New York Research Corporation   (United States)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^d NATIONAL UNIVERSITY HOSPITAL   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINONIN; ANTIMYCOBACTERIAL AGENT; ERYTHROMYCIN; GENOMIC DNA; ISONIAZID; LINEZOLID; N (1 TERT BUTYL 2 DIMETHYLAMINO 2 OXOETHYL) 2 (N FORMYL N HYDROXYAMINOMETHYL)HEXANAMIDE; PDF 611; PDF 709; PEPTIDE DEFORMYLASE INHIBITOR; RIFAMPICIN; STREPTOMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; AREA UNDER THE CURVE; ARTICLE; BACTERIAL GENE; BACTERIUM MUTANT; CONTROLLED STUDY; DEF GENE; DRUG BIOAVAILABILITY; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG HALF LIFE; DRUG STRUCTURE; ESCHERICHIA COLI; FEMALE; IC 50; MINIMUM INHIBITORY CONCENTRATION; MOUSE; MULTIDRUG RESISTANCE; MUTATIONAL ANALYSIS; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SEQUENCE ANALYSIS; SOUTHERN BLOTTING;

EID: 33750578846     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.00555-06     Document Type: Article

References (64)

1. Almassy, R. J., C. A. Janson, C. C. Kan, and Z. Hostomska. 1992. Structures of apo and complexed Escherichia coli glycinamide ribonucleotide transformylase. Proc. Natl. Acad. Sci. USA 89:6114-6118.
2. Apfel, C., D. W. Banner, D. Bur, M. Dietz, T. Hirata, C. Hubschwerlen, H. Locher, M. G. Page, W. Pirson, G. Rosse, and J. L. Specklin. 2000. Hydroxamic acid derivatives as potent peptide deformylase inhibitors and antibacterial agents. J. Med. Chem. 43:2324-2331.
3. Apfel, C. M., H. Locher, S. Even, B. Takacs, C. Hubschwerlen, W. Pirson, M. G. Page, and W. Keck. 2001. Peptide deformylase as an antibacterial drug target: target validation and resistance development. Antimicrob. Agents Chemother. 45:1058-1064.
4. Boularot, A., C. Giglione, I. Artaud, and T. Meinnel. 2004. Structure-activity relationship analysis and therapeutic potential of peptide deformylase inhibitors. Curr. Opin. Investig. Drugs 5:809-822.
5. Bracchi-Ricard, V., K. T. Nguyen, Y. Zhou, P. T. Rajagopalan, D. Chakrabarti, and D. Pei. 2001. Characterization of an eukaryotic peptide deformylase from Plasmodium falciparum. Arch. Biochem. Biophys. 396:162-170.
6. Cavalli, L. R., and B. C. Liang. 1998. Mutagenesis, tumorigenicity, and apoptosis: are the mitochondria involved? Mutat. Res. 398:19-26.
7. Chan, M. K., W. Gong, P. T. Rajagopalan, B. Hao, C. M. Tsai, and D. Pei. 1997. Crystal structure of the Escherichia coli peptide deformylase. Biochemistry 36:13904-13909.
8. fcsK) suitable for gene essentiality and antibacterial mode-of-action studies in Streptococcus pneumoniae. J. Bacteriol. 185:2051-2058.
9. Chen, D., C. Hackbarth, Z. J. Ni, C. Wu, W. Wang, R. Jain, Y. He, K. Bracken, B. Weidmann, D. V. Patel, J. Trias, R. J. White, and Z. Yuan. 2004. Peptide deformylase inhibitors as antibacterial agents: identification of VRC3375, a proline-3-alkylsuccinyl hydroxamate derivative, by using an integrated combinatorial and médicinal chemistry approach. Antimicrob. Agents Chemother. 48:250-261.
10. Chen, D. Z., D. V. Patel, C. J. Hackbarth, W. Wang, G. Dreyer, D. C. Young, P. S. Margolis, C Wu, Z. J. Ni, J. Trias, R. J. White, and Z. Yuan. 2000. Actinonin, a naturally occurring antibacterial agent, is a potent deformylase inhibitor. Biochemistry 39:1256-1262.
11. Clamp, M., J. Cuff, S. M. Searle, and G. J. Barton. 2004. The Jalview Java alignment editor. Bioinformatics 20:426-427.
12. Clements, J. M., R. P. Beckett, A. Brown, G. Catlin, M. Lobell, S. Palan, W. Thomas, M. Whittaker, S. Wood, S. Salama, P. J. Baker, H. F. Rodgers, V. Barynin, D. W. Rice, and M. G. Hunter. 2001. Antibiotic activity and charaterization of BB-3497, a novel peptide deformylase inhibitor. Antimicrob. Agents Chemother. 45:563-570.
13. Cuff, J. A., and G. J. Barton. 1999. Evaluation and improvement of multiple sequence methods for protein secondary structure prediction. Proteins 34:508-519.
14. Cynamon, M. H., E. Alrirez-Freites, and A. E. Yeo. 2004. BB-3497, a peptide deformylase inhibitor, is active against Mycobacterium tuberculosis. J. Antimicrob. Chemother. 53:403-405.
15. Dean, C. R., S. Narayan, D. M. Daigle, J. L. Dzink-Fox, X. Puyang, K. R. Bracken, K. E. Dean, B. Weidmann, Z. Yuan, R. Jain, and N. S. Ryder. 2005. Role of the AcrAB-TolC efflux pump in determining susceptibility of Haemophilus influenzae to the novel peptide deformylase inhibitor LBM415. Antimicrob. Agents Chemother. 49:3129-3135.
16. de Vries, H., A. J. Arendzen, and A. M. Kroon. 1973. The interference of the macrolide antibiotics with mitochondrial protein synthesis. Biochim. Biophys. Acta 331:264-275.
17. Dye, C. 2006. Global epidemiology of tuberculosis. Lancet 367:938-940.
18. Dye, C., C. J. Watt, D. M. Bleed, S. M. Hosseini, and M. C. Raviglione. 2005. Evolution of tuberculosis control and prospects for reducing tuberculosis incidence, prevalence, and deaths globally. JAMA 293:2767-2775.
19. Fantin, V. R., M. J. Berardi, L. Scorrano, S. J. Korsmeyer, and P. Leder. 2002. A novel mitochondriotoxic small molecule that selectively inhibits tumor cell growth. Cancer Cell 2:29-42.
20. Franzblau, S. G., R. S. Witzig, J. C. McLaughlin, P. Torres, G. Madico, A. Hernandez, M. T. Degnan, M. B. Cook, V. K. Quenzer, R. M. Ferguson, and R. H. Gilman. 1998. Rapid, low-technology MIC determination with clinical Mycobacterium tuberculosis isolates by using the microplate Alamar Blue assay. J. Clin. Microbiol. 36:362-366.
21. Giglione, C., and T. Meinnel. 2001. Resistance to anti-peptide deformylase drugs. Expert Opin. Ther. Targets 5:415-418.
22. Giglione, C., A. Serero, M. Pierre, B. Boisson, and T. Meinnel. 2000. Identification of eukaryotic peptide deformylases reveals universality of N-terminal protein processing mechanisms. EMBO J. 19:5916-5929.
23. Gite, S., Y. Li, V. Ramesh, and U. L. RajBhandary. 2000. Escherichia coli methionyl-tRNA formyltransferase: role of amino acids conserved in the linker region and in the C-terminal domain on the specific recognition of the initiator tRNA. Biochemistry 39:2218-2226.
24. Gordon, J. J., B. K. Kelly, and G. A. Miller. 1962. Actinonin: an antibiotic substance produced by an actinomycete. Nature 195:701-702.
25. Groche, D., A. Becker, I. Schlichting, W. Kabsch, S. Schultz, and A. F. Wagner. 1998. Isolation and crystallization of functionally competent Escherichia coli peptide deformylase forms containing either iron or nickel in the active site. Biochem. Biophys. Res. Commun. 246:342-346.
26. Metformyltransferase severely impairs growth of Escherichia coli. J. Bacteriol. 174:4294-4301.
27. Hackbarth, C. J., D. Z. Chen, J. G. Lewis, K. Clark, J. B. Mangold, J. A. Cramer, P. S. Margolis, W. Wang, J. Koehn, C. Wu, S. Lopez, G. Withers III, H. Gn, E. Dunn, R. Kulathila, S.-H. Pan, W. L. Porter, J. Jacobs, J. Trias, D. V. Patel, B. Weldmann, R. J. White, and Z. Yuan. 2002. N-Alkyl urea hydroxamic acids as a new class of peptide deformylase inhibitors with antibacterial activity. Antimicrob. Agents Chemother. 46:2752-2764.
28. Klein, C., P. Chen, J. H. Arevalo, E. A. Stura, A. Marolewski, M. S. Warren, S. J. Benkovic, and I. A. Wilson. 1995. Towards structure-based drug design: crystal structure of a multisubstrate adduct complex of glycinamide ribonucleotide transformylase at 1.96 A resolution. J. Mol. Biol. 249:153-175.
29. Kremer, L. S., and G. S. Besra. 2002. Current status and future development of antitubercular chemotherapy. Expert Opin. Investig. Drugs 11:1033-1049.
30. Kroon, A. M., B. H. Dontfe, M. Holtrop, and C. Van den Bogert. 1984. The mitochondrial genetic system as a target for chemotherapy: tetracyclines as cytostatics. Cancer Lett. 25:33-40.
31. Kroon, A. M., and C. Van den Bogert. 1983. Antibacterial drugs and their interference with the biogenesis of mitochondria in animal and human cells. Pharm. Weekbl. Sci. 5:81-87.
32. Lee, M. D., C. Antczak, Y. Li, F. M. Sirotnak, W. G. Bornmann, and D. A. Scheinberg. 2003. A new human peptide deformylase inhibitable by actinonin. Biochem. Biophys. Res. Commun. 312:309-315.
33. Lee, M. D., Y. She, M. J. Soskis, C. P. Borella, J. R. Gardner, P. A. Hayes, B. M. Dy, M. L. Heaney, M. R. Philips, W. G. Bommann, F. M. Sirotnak, and D. A. Scheinberg. 2004. Human mitochondrial peptide deformylase, a new anticancer target of actinonin-based antibiotics. J. Clin. Investig. 114:1107-1116.
34. Margolis, P., C. Hackbarth, S. Lopez, M. Maniar, W. Wang, Z. Yuan, R. White, and J. Trias. 2001. Resistance of Streptococcus pneumoniae to deformylase inhibitors is due to mutations in defB. Antimicrob. Agents Chemother. 45:2432-2435.
35. Margolis, P. S., C. J. Hackbarth, D. C. Young, W. Wang, D. Chen, Z. Yuan, R. White, and J. Trias. 2000. Peptide deformylase in Staphylococcus aureus: resistance to inhibition is mediated by mutations in the formyltransferase gene. Antimicrob. Agents Chemother. 44:1825-1831.
36. Mazel, D., S. Pochet, and P. Mariiere. 1994. Genetic characterization of polypeptide deformylase, a distinctive enzyme of eubacterial translation. EMBO J. 13:914-923.
37. McKee, E. E., M. Ferguson, A. T. Bentley, and T. A. Marks. 2006. Inhibition of mammalian mitochondrial protein synthesis by oxazolidinones. Antimicrob. Agents Chemother. 50:2042-2049.
38. Meinnel, T., and S. Blanquet. 1995. Enzymatic properties of Escherichia coli peptide deformylase. J. Bacteriol. 177:1883-1887.
39. Meinnel, T., S. Blanquet, and F. Dardel. 1996. A new subclass of the zinc metalloproteases superfamily revealed by the solution structure of peptide deformylase. J. Mol. Biol. 262:375-386.
40. Meinnel, T., C. Lazennec, and S. Blanquet. 1995. Mapping of the active site zinc ligands of peptide deformylase. J. Mol. Biol. 254:175-183.
41. Meinnel, T., C Lazennec, S. Villoing, and S. Blanquet. 1997. Structure-function relationships within the peptide deformylase family. Evidence for a conserved architecture of the active site involving three conserved motifs and a metal ion. J. Mol. Biol. 267:749-761.
42. Meinnel, T., Y. Mechulam, and S. Blanquet. 1993. Methionine as translation start signal: a review of the enzymes of the pathway in Escherichia coli. Biochimie 75:1061-1075.
43. Modica-Napolitano, J. S., K. Koya, E. Weisberg, B. T. Brunelli, Y. Li, and L. B. Chen. 1996. Selective damage to carcinoma mitochondria by the rhodacyanine MKT-077. Cancer Res. 56:544-550.
44. Muri, E. M., M. J. Nieto, R. D. Sindelar, and J. S. Williamson. 2002. Hydroxamic acids as pharmacological agents. Curr. Med. Chem. 9:1631-1653.
45. Nguyen, K. T., X. Hu, C. Cotton, R. Chakrabarti, M. X. Zhu, and D. Pel. 2003. Characterization of a human peptide deformylase: implications for antibacterial drug design. Biochemistry 42:9952-9958.
46. Nunn, P., B. Williams, K. Floyd, C. Dye, G. Elzinga, and M. Raviglione. 2005. Tuberculosis control in the era of HIV. Nat. Rev. Immunol. 5:819-826.
47. Pavelka, M. S., Jr, and W. R. Jacobs, Jr. 1999. Comparison of the construction of unmarked deletion mutations in Mycobacterium smegmatis, Mycobacterium bovis bacillus Calmette-Guérin, and Mycobacterium tuberculosis H37Rv by allelic exchange. J. Bacteriol. 181:47804789.
48. Penta, J. S., F. M. Johnson, J. T. Wachsman, and W. C. Copeland. 2001. Mitochondrial DNA in human malignancy. Mutat. Res. 488:119-133.
49. Ragusa, S., S. Blanquet, and T. Meinnel. 1998. Control of peptide deformylase activity by metal cations. J. Mol. Biol. 280:515-523.
50. Rajagopalan, P. T., A. Datta, and D. Pei. 1997. Purification, characterization, and inhibition of peptide deformylase from Escherichia coli. Biochemistry 36:13910-13918.
51. Rajagopalan, P. T., and D. Pei. 1998. Oxygen-mediated inactivation of peptide deformylase. J. Biol. Chem. 273:22305-22310.
52. Ramanatban-Girish, S. J. McColm, J. M. Clements, P. Taupin, S. Barrowclife, J. Hevizi, S. Safrin, C. Moore, G. Paton, H. Moser, A. Gadd, U. Hoch, V. Jiang, D. Lofland, and K. W. Johnson. 2004. Pharmacokinetics in animals and humans of a first-in-class peptide deformylase inhibitor. Antimicrob. Agents Chemother. 48:4835-4842.
53. Ramesh, V., S. Gite, Y. Li, and U. L. RajBhandary. 1997. Suppressor mutations in Escherichia coli methionyl-tRNA formyltransferase: role of a 16-amino acid insertion module in initiator tRNA recognition. Proc. Natl. Acad. Sci. USA 94:13524-13529.
54. Ramesh, V., S. Gite, and U. L. RajBhandary. 1998. Functional interaction of an arginine conserved in the sixteen amino acid insertion module of Escherichia coli methionyl-tRNA formyltransferase with determinants for formylation in the initiator tRNA. Biochemistry 37:15925-15932.
55. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
56. Sassetti, C. M., D. H. Boyd, and E. J. Rubin. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48:77-84.
57. Saxena, R., and P. K. Chakraborti. 2005. Identification of regions involved in enzymatic stability of peptide deformylase of Mycobacterium tuberculosis. J. Bacteriol. 187:8216-8220.
58. Saxena, R., and P. K. Chakraborti. 2005. The carboxy-terminal end of the peptide deformylase from Mycobacterium tuberculosis is indispensable for its enzymatic activity. Biochem. Biophys. Res. Commun. 332:418-425.
59. Schmitt, E., S. Blanquet, and Y. Mechulam. 1996. Structure of crystalline Escherichia coli methionyl-tRNA(f) Met formyltransferase: comparison with glycinamide ribonucleotide formyltransferase. EMBO J. 15:4749-4758.
60. Serero, A., C. Giglione, A. Sardini, J. Martinez-Sanz, and T. Meinnel. 2003. An unusual peptide deformylase features in the human mitochondrial N-terminal methionine excision pathway. J. Biol. Chem. 278:52953-52963.
61. Solbiati, J., A. Chapman-Smith, J. L. Miller, C. G. Miller, and J. E. Cronan, Jr. 1999. Processing of the N termini of nascent polypeptide chains requires deformylation prior to methionine removal. J. Mol. Biol. 290:607-614.
62. Stover, C. K., V. F. de la Cruz, T. R. Fuerst, J. E. Burlein, L. A. Benson, L. T. Bennett, G. P. Bansal, J. F. Young, M. H. Lee, G. F. Hatfull, et al. 1991. New use of BCG for recombinant vaccines. Nature 351:456-460.
63. Xn, Y., L. T. Lai, J. L. Gabrilove, and D. A. Scheinberg. 1998. Antitumor activity of actinonin in vitro and in vivo. Clin. Cancer Res. 4:171-176.
64. Yuan, Z., J. Trias, and R. J. White. 2001. Deformylase as a novel antibacterial target. Drug Discov. Today 6:954-961.