Identification of the proteasome inhibitor MG262 as a potent ATP-dependent inhibitor of the Salmonella enterica serovar typhimurium Lon protease

Biochemistry

Volumn 45, Issue 27, 2006, Pages 8264-8274

  Frase, Hilary ^a   Hudak, Jason ^a   Lee, Irene ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINETRIPHOSPHATE; ANTIBIOTICS; BACTERIA; DEGRADATION; HYDROLYSIS; LEAD; MATHEMATICAL MODELS; PARAMETER ESTIMATION; PROTEINS;

HOMO-OLIGOMERIC ATP; KINETIC PARAMETERS; LON-SPECIFIC INHIBITOR; REGULATORY PROTEINS;

ENZYMES;

ADENOSINE TRIPHOSPHATE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORONIC ACID DERIVATIVE; ENDOPEPTIDASE LA; EPOXOMICIN; ETHYLBORONIC ACID; ISOPROPYLBORONIC ACID; MG 262; PROTEASOME INHIBITOR; SULFONE; UNCLASSIFIED DRUG; VINYL SULFONE;

ARTICLE; BACTERIAL VIRULENCE; CROSS REACTION; ENZYME INHIBITION; ENZYME PURIFICATION; ENZYME SPECIFICITY; HYDROLYSIS; IC 50; MICHAELIS MENTEN KINETICS; MOLECULAR CLONING; NONHUMAN; PEPTIDE SYNTHESIS; PLASMID; PRIORITY JOURNAL; PROTEIN DEGRADATION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; STEADY STATE;

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; BORONIC ACIDS; CLONING, MOLECULAR; CYSTEINE PROTEINASE INHIBITORS; DRUG DESIGN; HUMANS; INHIBITORY CONCENTRATION 50; PROTEASE LA; PROTEASOME ENDOPEPTIDASE COMPLEX; RECOMBINANT PROTEINS; SALMONELLA ENTERICA;

BACTERIA (MICROORGANISMS); SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 33745850131     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060542e     Document Type: Article

References (60)

1. Monaghan, R. L., and Barrett, J. F. (2006) Antibacterial drug discovery-then, now and the genomics future, Biochem. Pharmacol. 71, 901-909.
2. Robertson, G. T., Kovach, M. E., Allen, C. A., Ficht, T. A., and Roop, R. M., II (2000) The Brucella abortus Lon functions as a generalized stress response protease and is required for wild-type virulence in BALB/c mice, Mol. Microbiol. 35, 577-588.
3. Takaya, A., Suzuki, M., Matsui, H., Tomoyasu, T., Sashinami, H., Nakane, A., and Yamamoto, T. (2003) Lon, a stress-induced ATP-dependent protease, is critically important for systemic Salmonella enterica serovar typhimurium infection of mice, Infect. Immun. 71, 690-696.
4. Matsui, H., Suzuki, M., Isshiki, Y., Kodama, C., Eguchi, M., Kikuchi, Y., Motokawa, K., Takaya, A., Tomoyasu, T., and Yamamoto, T. (2003) Oral immunization with ATP-dependent protease-deficient mutants protects mice against subsequent oral challenge with virulent Salmonella enterica serovar typhimurium, Infect. Immun. 71, 30-39.
5. Charette, M. F., Henderson, G. W., Doane, L. L., and Markovitz, A. (1984) DNA-stimulated ATPase activity on the lon (CapR) protein, J. Bacteriol. 158, 195-201.
6. Chung, C. H., and Goldberg, A. L. (1981) The product of the lon (capR) gene in Escherichia coli is the ATP-dependent protease, protease La, Proc. Natl. Acad. Sci. U.S.A. 78, 4931-4935.
7. Goff, S. A., and Goldberg, A. L. (1985) Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes, Cell 41, 587-595.
8. Goldberg, A. L., Moerschell, R. P., Chung, C. H., and Maurizi, M. R. (1994) ATP-dependent protease La (lon) from Escherichia coli, Methods Enzymol. 244, 350-375.
9. Goldberg, A. L., and Waxman, L. (1985) The role of ATP hydrolysis in the breakdown of proteins and peptides by protease La from Escherichia coli, J. Biol. Chem. 260, 12029-12034.
10. Gottesman, S. (1996) Proteases and their targets in Escherichia coli, Annu. Rev. Genet. 30, 465-506.
11. Gottesman, S., Gottesman, M., Shaw, J. E., and Pearson, M. L. (1981) Protein degradation in E. coli: the lon mutation and bacteriophage lambda N and ell protein stability, Cell 24, 225-233.
12. Gottesman, S., and Maurizi, M. R. (1992) Regulation by proteolysis: energy-dependent proteases and their targets, Microbiol. Rev. 56, 592-621.
13. Maurizi, M. R. (1992) Proteases and protein degradation in Escherichia coli, Experientia 48, 178-201.
14. Schoemaker, J. M., Gayda, R. C., and Markovitz, A. (1984) Regulation of cell division in Escherichia coli: SOS induction and cellular location of the sulA protein, a key to lon-associated filamentation and death, J. Bacteriol. 158, 551-561.
15. Suzuki, C. K., Kutejova, E., and Suda, K. (1995) Analysis and purification of ATP-dependent mitochondrial lon protease of Saccharomyces cerevisiae, Methods Enzymol. 260, 486-494.
16. Wang, N., Maurizi, M. R., Emmert-Buck, L., and Gottesman, M. M. (1994) Synthesis, processing, and localization of human Lon protease, J. Biol. Chem. 269, 29308-29313.
17. Huang, X., and Miller, W. (1991) A time-efficient, linear-space local similarity algorithm, Adv. Appl. Math. 12, 337-357.
18. Apte, B. N., Rhodes, H., and Zipser, D. (1975) Mutation blocking the specific degradation of reinitiation polypeptides in E. coli, Nature 257, 329-331.
19. Downs, D., Waxman, L., Goldberg, A. L., and Roth, J. (1986) Isolation and characterization of lon mutants in Salmonella typhimurium, J. Bacteriol. 165, 193-197.
20. Gottesman, S., and Zipser, D. (1978) Deg phenotype of Escherichia coli lon mutants, J. Bacteriol. 133, 844-851.
21. Grossman, A. D., Burgess, R. R., Walter, W., and Gross, C. A. (1983) Mutations in the lon gene of E. coli K12 phenotypically suppress a mutation in the sigma subunit of RNA polymerase, Cell 32, 151-159.
22. Howard-Flanders, P., Simson, E., and Theriot, L. (1964) A locus that controls filament formation and sensitivity to radiation in Escherichia coli K-12, Genetics 49, 237-246.
23. Mizusawa, S., and Gottesman, S. (1983) Protein degradation in Escherichia coli: the lon gene controls the stability of sulA protein, Proc. Natl. Acad. Sci. U.S.A. 80, 358-362.
24. + proteins and substrate recognition, it all depends on their partner in crime, FEBS Lett. 529, 6-10.
25. Patel, S., and Latterich, M. (1998) The AAA team: related ATPases with diverse functions, Trends Cell Biol. 8, 65-71.
26. Patterson, J., Vineyard, D., Thomas-Wohlever, J., Behshad, R., Burke, M., and Lee, I. (2004) Correlation of an adenine-specific conformational change with the ATP-dependent peptidase activity of Escherichia coli Lon, Biochemistry 43, 7432-7442.
27. Wang, J., Song, J. J., Seong, I. S., Franklin, M. C., Kamtekar, S., Eom, S. H., and Chung, C. H. (2001) Nucleotide-dependent conformational changes in a protease-associated ATPase HsIU, Structure (Cambridge, MA, U.S.) 9, 1107-1116.
28. + alpha domain of E. coli Lon protease at 1.9 Å resolution, J. Struct. Biol. 146, 113-122.
29. Lowe, J., Stock, D., Jap, B., Zwickl, P., Baumeister, W., and Huber, R. (1995) Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution, Science 268, 533-539.
30. Bota, D. A., and Davies, K. J. (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism, Nat. Cell Biol. 4, 674-680.
31. Waxman, L., and Goldberg, A. L. (1982) Protease La from Escherichia coli hydrolyzes ATP and proteins in a linked fashion, Proc. Natl. Acad. Sci. U.S.A. 79, 4883-4887.
32. Waxman, L., and Goldberg, A. L. (1985) Protease La, the lon gene product, cleaves specific fluorogenic peptides in an ATP-dependent reaction, J. Biol. Chem. 260, 12022-12028.
33. Kisselev, A. F., and Goldberg, A. L. (2001) Proteasome inhibitors: from research tools to drug candidates, Chem. Biol. 8, 739-758.
34. Fu, G. K., and Markovitz, D. M. (1998) The human LON protease binds to mitochondrial promoters in a single-stranded, site-specific, strand-specific manner, Biochemistry 37, 1905-1909.
35. Thomas-Wohlever, J., and Lee, I. (2002) Kinetic characterization of the peptidase activity of Escherichia coli Lon reveals the mechanistic similarities in ATP-dependent hydrolysis of peptide and protein substrates, Biochemistry 41, 9418-9425.
36. Liu, T., Lu, B., Lee, I., Ondrovicova, G., Kutejova, E., and Suzuki, C. K. (2004) DNA and RNA binding by the mitochondrial lon protease is regulated by nucleotide and protein substrate, J. Biol. Chem. 279, 13902-13910.
37. Gilbert, S. P., and Mackey, A. T. (2000) Kinetics: a tool to study molecular motors, Methods 22, 337-354.
38. Copeland, R. A. (2000) Enzymes: A Practical Introduction to Structure, Mechanism, and Data Analysis, 2nd ed., John Wiley & Sons, Inc., New York.
39. Copeland, R. A. (2005) Evaluation of Enzyme Inhibitors in Drug Discovery: A Guide for Medicinal Chemists and Pharmacologists, John Wiley & Sons, Inc., Hoboken, NJ.
40. Lee, I., and Berdis, A. J. (2001) Adenosine triphosphate-dependent degradation of a fluorescent lambda N substrate mimic by Lon protease, Anal. Biochem. 291, 74-83.
41. Waxman, L., and Goldberg, A. L. (1986) Selectivity of intracellular proteolysis: protein substrates activate the ATP-dependent protease (La), Science 232, 500-503.
42. Botos, I., Melnikov, E. E., Cherry, S., Tropea, J. E., Khalatova, A. G., Rasulova, F., Dauter, Z., Maurizi, M. R., Rotanova, T. V., Wlodawer, A., and Gustchina, A. (2004) The catalytic domain of Escherichia coli Lon protease has a unique fold and a Ser-Lys dyad in the active site, J. Biol. Chem. 279, 8140-8148.
43. Adams, J., Behnke, M., Chen, S., Cruickshank, A. A., Dick, L. R., Grenier, L., Klunder, J. M., Ma, Y. T., Plamondon, L., and Stein, R. L. (1998) Potent and selective inhibitors of the proteasome: dipeptidyl boronic acids, Bioorg. Med. Chem. Lett. 8, 333-338.
44. Palmer, J. T., Rasnick, D., Klaus, J. L., and Bromme, D. (1995) Vinyl sulfones as mechanism-based cysteine protease inhibitors, J. Med. Chem. 38, 3193-3196.
45. Bogyo, M., McMaster, J. S., Gaczynska, M., Tortorella, D., Goldberg, A. L., and Ploegh, H. (1997) Covalent modification of the active site threonine of proteasomal beta subunits and the Escherichia coli homolog HslV by a new class of inhibitors, Proc. Natl. Acad. Sci. U.S.A. 94, 6629-6634.
46. Sousa, M. C., Kassler, B. M., Overkleeft, H. S., and McKay, D. B. (2002) Crystal structure of HslUV complexed with a vinyl sulfone inhibitor: corroboration of a proposed mechanism of allosteric activation of HslV by HslU, J. Mol. Biol. 318, 779-785.
47. Joyeau, R., Maoulida, C., Guillet, C., Frappier, F., Teixeira, A. R., Schrevel, J., Santana, J., and Grellier, P. (2000) Synthesis and activity of pyrrolidinyl- and thiazolidinyl-dipeptide derivatives as inhibitors of the Tc80 prolyl oligopeptidase from Trypanosoma cruzi, Eur. J. Med. Chem. 35, 257-266.
48. Bogyo, M., Shin, S., McMaster, J. S., and Ploegh, H. L. (1998) Substrate binding and sequence preference of the proteasome revealed by active-site-directed affinity probes, Chem. Biol. 5, 307-320.
49. Meng, L., Mohan, R., Kwok, B. H., Elofsson, M., Sin, N., and Crews, C. M. (1999) Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity, Proc. Natl. Acad. Sci. U.S.A. 96, 10403-10408.
50. Hanada, M., Sugawara, K., Kaneta, K., Toda, S., Nishiyama, Y., Tomita, K., Yamamoto, H., Konishi, M., and Oki, T. (1992) Epoxomicin, a new antitumor agent of microbial origin, J. Antibiot. (Tokyo) 45, 1746-1752.
51. Groll, M., Kim, K. B., Kairies, N., Huber, R., and Crews, C. M. (2000) Crystal structure of epoxomicin: 20S proteasome reveals a molecular basis for selectivity of α′,β′-epoxyketone proteasome inhibitors, J. Am. Chem. Soc. 122, 1237-1238.
52. Koehler, K. A., and Lienhard, G. E. (1971) 2-Phenylethaneboronic acid, a possible transition-state analog for chymotrypsin, Biochemistry 10, 2477-2483.
53. Thompson, R. C. (1973) Use of peptide aldehydes to generate transition-state analogs of elastase, Biochemistry 12, 47-51.
54. Westerik, J. O., and Wolfenden, R. (1972) Aldehydes as inhibitors of papain, J. Biol. Chem. 247, 8195-8197.
55. Vinitsky, A., Michaud, C., Powers, J. C., and Orlowski, M. (1992) Inhibition of the chymotrypsin-like activity of the pituitary multicatalytic proteinase complex, Biochemistry 31, 9421-9428.
56. Yoo, S. J., Kim, H. H., Shin, D. H., Lee, C. S., Seong, I. S., Seol, J. H., Shimbara, N., Tanaka, K., and Chung, C. H. (1998) Effects of the cys mutations on structure and function of the ATP-dependent HslVU protease in Escherichia coli. The Cys287 to Val mutation in HslU uncouples the ATP-dependent proteolysis by HslvU from ATP hydrolysis, J. Biol. Chem. 273, 22929-22935.
57. Granot, Z., Geiss-Friedlander, R., Melamed-Book, N., Eimerl, S., Timberg, R., Weiss, A. M., Hales, K. H., Hales, D. B., Stocco, D. M., and Orly, J. (2003) Proteolysis of normal and mutated steroidogenic acute regulatory proteins in the mitochondria: the fate of unwanted proteins, Mol. Endocrinol. 17, 2461-2476.
58. Ondrovicova, G., Liu, T., Singh, K., Tian, B., Li, H., Gakh, O., Perecko, D., Janata, J., Granot, Z., Orly, J., Kutejova, E., and Suzuki, C. K. (2005) Cleavage site selection within a folded substrate by the ATP-dependent lon protease, J. Biol. Chem. 280, 25103-25110.
59. Ling, Y. H., Liebes, L., Zou, Y., and Perez-Soler, R. (2003) Reactive oxygen species generation and mitochondrial dysfunction in the apoptotic response to Bortezomib, a novel proteasome inhibitor, in human H460 non-small cell lung cancer cells, J. Biol. Chem. 278, 33714-33723.
60. Pei, X. Y., Dai, Y., and Grant, S. (2003) The proteasome inhibitor bortezomib promotes mitochondrial injury and apoptosis induced by the small molecule Bcl-2 inhibitor HA14-1 in multiple myeloma cells, Leukemia 17, 2036-2045.