Bacterial Zinc Proteases as Orphan Targets

Drug Design of Zinc-Enzyme Inhibitors: Functional, Structural, and Disease Applications

Volumn , Issue , 2009, Pages 673-703

  Supuran, Claudiu T ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Bacterial zinc protease inhibitor drug design; Bacterial zinc proteases as orphan targets; Metalloproteases of M9 family (Vibrio and Clostridium collagenases)

Indexed keywords

EID: 84889354586     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470508169.ch28     Document Type: Chapter

References (91)

1. Barrett, A. J.; Rawlings, N. D.;Woessner, J. F., Jr., Eds. Handbook of Proteolytic Enzymes (CD-ROM); Academic Press: London, 1998; Chapters 1-569.
2. Supuran, C. T.; Scozzafava, A.; Mastrolorenzo, A. Bacterial proteases: current therapeutic use and future prospects for the development of new antibiotics. Expert Opin. Ther. Pat. 2001, 11, 221-259.
3. Supuran, C. T.; Scozzafava, A.; Clare, B. W. Bacterial protease inhibitors. Med. Res. Rev. 2002, 22, 329-372.
4. Mastrolorenzo, A.; Rusconi, S.; Scozzafava, A.; Barbaro, G.; Supuran, C. T. Inhibitors of HIV-1 protease: current state of the art 10 years after their introduction. From antiretroviral drugs to antifungal, antibacterial and antitumor agents based on aspartic protease inhibitors. Curr. Med. Chem. 2007, 14, 2734-2748.
5. Barbaro, G.; Scozzafava, A.; Mastrolorenzo, A.; Supuran, C. T. Highly active antiretroviral therapy: current state of the art, newagents and their pharmacological interactions useful for improving therapeutic outcome. Curr. Pharm. Des. 2005, 11, 1805-1843.
6. Wlodawer, A.; Gustchina, A. Structural and biochemical studies of retroviral proteases. Biochim. Biophys. Acta 2000, 1477, 16-34.
7. Travis, J.; Potempa, J. Bacterial proteinases as targets for the development of second generation antibiotics. Biochim. Biophys. Acta 2000, 1477, 35-50.
8. Miyoshi, S. I.; Shinoda, S. Bacterial metalloproteases as the toxic factor in infection. J. Toxicol. Toxin. Rev. 1997, 16, 177-194.
9. Maeda, H. Role of microbial proteases in pathogenesis. Microbiol. Immunol. 1996, 40, 685-699.
10. Rice, S. A.; Givskov, M.; Steinberg, P.; Kjelleberg, S. Bacterial signals and antagonists: the interaction between bacteria and higher organisms. J. Mol. Microbiol. Biotechnol. 1999, 1, 23-31.
11. Wright, G. D. Resisting resistance: newstrategies for battling superbugs. Chem. Biol. 2000, 7, R127-R132.
12. Rawlings, N. D.; Barrett, A. J. Evolutionary families of peptidases. Biochem. J. 1993, 290, 205-218.
13. Berger, A.; Schechter, I. Mapping the active site of papain with the aid of peptide substrates and inhibitors. Philos. Trans. R. Soc. Lond. 1970, 257, 249-264.
14. Coleman, J. E. Zinc enzymes. Curr. Opin. Chem. Biol. 1998, 2, 222-234.
15. Shinoda, S.; Miyoshi, S. I.;Wakae, H.; Rahman, M.; Tomochika, K. I. Bacterial proteases as pathogenic factors, with special emphasis on vibrio proteases. J. Toxicol. Toxin. Rev. 1996, 15, 327-339.
16. Vollmer, P.; Walev, I.; Rose-John, S.; Bhakdi, S. Novel pathogenic mechanism of microbial metalloproteinase: liberation of membrane-anchored molecules in biologically active form exemplified by studies with the human interleukin-6 receptor. Infect. Immun. 1996, 64, 3646-3651.
17. Påhlman, L. I.; Marx, P. F.; Mörgelin, M.; Lukomski, S.; Meijers, J. C.; Herwald, H. Thrombin-activatable fibrinolysis inhibitor binds to Streptococcus pyogenes by interacting with collagen-like proteins A and B. J. Biol. Chem. 2007, 282, 24873-24881.
18. Schiavo, G.; Matteoli, M.; Montecucco, C. Neurotoxins affecting neuroexocytosis. Physiol. Rev. 2000, 80, 717-766.
19. Humeau,Y.; Doussau, F.; Grant, N. J.; Poulain, B. Howbotulinum and tetanus neurotoxins block neurotransmitter release. Biochimie 2000, 82, 427-446.
20. Beynon,R. J.;Beaumont,A.Thermolysin. InHandbookofProteolyticEnzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 351.
21. Coffey, A.; van den Burg, B.; Veltman, R.; Abee, T. Characteristics of the biologically active 35-kDa metalloprotease virulence factor from Listeria monocytogenes. J. Appl. Microbiol. 2000, 88, 132-141.
22. Makinen, P. L.; Makinen, K. K. The Enterococcus faecalis extracellular metalloendopeptidase (EC 3.4.24.30; coccolysin) inactivates human endothelin at bonds involving hydrophobic amino acid residues. Biochem. Biophys. Res. Commun. 1994, 200, 981-985.
23. Del Papa, M. F.; Hancock, L. E.; Thomas, V. C.; Perego, M. Full activation of Enterococcus faecalis gelatinase by a C-terminal proteolytic cleavage. J. Bacteriol. 2007, 189, 8835-8843.
24. Nagamune, K.;Yamamoto, K.; Naka, A.; Matsuyama, J.; Miwatani, T.; Honda, T. In vitro proteolytic processing and activation of the recombinant precursor of El Tor cytolysin/hemolysin (pro-HlyA) of Vibrio cholerae by soluble hemagglutinin/protease of V. cholerae, trypsin, and other proteases. Infect. Immun. 1996, 64, 4655-4658.
25. Benitez, J. A.; Garcia, L.; Silva, A.; Garcia, H.; Fando, R.; Cedre, B. Preliminary assessment of the safety and immunogenicity of a new CTXPhi-negative, hemagglutinin/protease-defective El Tor strain as a cholera vaccine candidate. Infect. Immun. 1999, 67, 539-545.
26. Lutfullah, G.; Amin, F.; Khan, Z.; Azhar, N.; Azim, M. K.; Noor, S.; Shoukat, K. Homology modeling of hemagglutinin/protease [HA/P (vibriolysin)] from Vibrio cholerae: sequence comparison, residue interactions and molecular mechanism. Protein J. 2008, 27, 105-114.
27. Kon, Y.; Tsukada, H.; Hasegawa, T.; Igarashi, K.;Wada, K.; Suzuki, E.; Arakawa, M.; Gejyo, F. The role of Pseudomonas aeruginosa elastase as a potent inflammatory factor in a rat air pouch inflammation model. FEMS Immunol. Med. Microbiol. 1999, 25, 313-321.
28. Pesci, E. C.; Milbank, J. B.; Pearson, J. P.; McKnight, S.; Kende, A. S.; Greenberg, E. P.; Iglewski, B. H. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 1999, 96, 11229-11234.
29. Kessler, E.; Ohman, D. E. Pseudolysin. In Handbook of Proteolytic Enzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 357.
30. Adekoya, O. A.; Willassen, N. P.; Sylte, I. Molecular insight into pseudolysin inhibition using the MM-PBSA and LIE methods. J. Struct. Biol. 2006, 153, 129-144.
31. Woessner, J. F. Legionella metalloendopeptidase. In Handbook of Proteolytic Enzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 358.
32. Moffat, J. F.; Edelstein, P. H.; Regula, D. P.; Cirillo, J. D.; Tompkins, L. S. Effects of an isogenic Zn-metalloprotease-deficient mutant of Legionella pneumophila in a guinea-pig pneumonia model. Mol. Microbiol. 1994, 12, 693-705.
33. Grass, G.; Schierhorn, A.; Sorkau, E.;Müller, H.; Rücknagel, P.; Nies, D. H.; Fricke, B. Camelysin is a novel surface metalloproteinase from Bacillus cereus. Infect. Immun. 2004, 72, 219-228.
34. Karbalaei-Heidari, H. R.; Ziaee, A. A.; Amoozegar, M. A.; Cheburkin, Y.; Budisa, N. Molecular cloning and sequence analysis of a novel zinc-metalloprotease gene from the Salinivibrio sp. strain AF-2004 and its extracellular expression in E. coli. Gene 2008, 408, 196-203.
35. Sokol, P. A.; Malott, R. J.; Riedel, K.; Eberl, L. Communication systems in the genus Burkholderia: global regulators and targets for novel antipathogenic drugs. Future Microbiol. 2007, 2, 555-563.
36. Kooi, C.; Corbett, C. R.; Sokol, P. A. Functional analysis of the Burkholderia cenocepacia ZmpA metalloprotease. J. Bacteriol. 2005, 187, 4421-4429.
37. Kooi, C.; Subsin, B.; Chen, R.; Pohorelic, B.; Sokol, P. A. Burkholderia cenocepacia ZmpB is a broad-specificity zinc metalloprotease involved in virulence. Infect. Immun. 2006, 74, 4083-4093.
38. Jung, C. M.; Matsushita, O.; Katayama, S.; Minami, J.; Sakurai, J.; Okabe, A. Identification of metal ligands in the Clostridium histolyticum ColH collagenase. J. Bacteriol. 1999, 181, 2816-2822.
39. Matsushita, O.; Jung, C. M.; Minami, J.; Katayama, S.; Nishi, N.; Okabe, A. Astudy of the collagen-binding domain of a 116-kDa Clostridium histolyticum collagenase. J. Biol. Chem. 1998, 273, 3643-3648.
40. Fukushima, J.; Okuda, K. Vibrio collagenase. In Handbook of Proteolytic Enzymes (CDROM); Barrett, A. J.; Rawlings, N. D.;Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 367.
41. Miyoshi, S. Vibrio vulnificus infection and metalloprotease. J. Dermatol. 2006, 33, 589-595.
42. Chang, A. K.; Park, J. W.; Lee, E. H.; Lee, J. S. The N-terminal propeptide of Vibrio vulnificus extracellular metalloprotease is both an inhibitor of and a substrate for the enzyme. J. Bacteriol. 2007, 189, 6832-6838.
43. Varina, M.; Denkin, S. M.; Staroscik, A. M.; Nelson, D. R. Identification and characterization of Epp, the secreted processing protease for the Vibrio anguillarum EmpA metalloprotease. J. Bacteriol. 2008, 190, 6589-6597.
44. Matson, J. S.; DiRita, V. J. Degradation of themembrane-localized virulence activator TcpP by theYaeLprotease inVibrio cholerae.Proc.Natl. Acad. Sci.USA2005, 102, 16403-16408.
45. Van Wart, H. E. Clostridium collagenase. In Handbook of Proteolytic Enzymes (CDROM); Barrett, A. J.; Rawlings, N. D.;Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 368.
46. Bond, M. D.; Van Wart, H. E. Purification and separation of individual collagenases of Clostridium histolyticum using red dye ligand chromatography. Biochemistry 1984, 23, 3077-3085.
47. Bond, M. D.; Van Wart, H. E. Characterization of the individual collagenases from Clostridium histolyticum. Biochemistry 1984, 23, 3085-3091.
48. Jung, W.; Winter, H. Considerations for the use of clostridial collagenase in clinical practice. Clin. Drug Invest. 1998, 15, 245-252.
49. Scozzafava, A.; Supuran, C. T. Protease inhibitors: synthesis of potent bacterial collagenase and matrix metalloproteinase inhibitors incorporating N-4-nitrobenzylsulfonylglycine hydroxamate moieties. J. Med. Chem. 2000, 43, 1858-1865.
50. Valee, B. L.; Auld, D. S. Zinc coordination, function and structure of zinc enzymes and other proteins. Biochemistry 1990, 29, 5647-5659.
51. Larsen, K. S.; Zhang, K.; Auld, D. S. D-Phe complexes of zinc and cobalt carboxypeptidase A. J. Inorg. Biochem. 1996, 64, 149-162.
52. Lund, T.; Granum, P. E. The 105-kDa protein component of Bacillus cereus non-hemolytic enterotoxin is a metalloprotease with gelatinolytic and collagenolytic activity. FEMS Microbiol. Lett. 1999, 178, 355-361.
53. Louis, D.; Bernillon, J.; Paisse, J. O.;Wallach, J. M. Use of liquid chromatography-mass spectrometry coupling for monitoring the serralysin-catalyzed hydrolysis of a peptide library. J. Chromatogr. B. Biomed. Sci. Appl. 1999, 732, 271-276.
54. Baumann, U. Serralysin. In Handbook of Proteolytic Enzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 386.
55. Basu, B.; Apte, S. K. A novel serralysin metalloprotease from Deinococcus radiodurans. Biochim. Biophys. Acta 2008, 1784, 1256-1264.
56. Kwak, J.; Lee, K.; Shin, D. H.; Maeng, J. S.; Park, D. S.; Oh, H.W.; Son, K. H.; Bae, K. S.; Park, H. Y. Biochemical and genetic characterization of arazyme, an extracellular metalloprotease produced from Serratia proteamaculans HY-3. J. Microbiol. Biotechnol. 2007, 17, 761-768.
57. Morihara, K. Aeruginolysin. In Handbook of Proteolytic Enzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 387.
58. Belas, R. Mirabilysin. In Handbook of Proteolytic Enzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 388.
59. Franco, A. A.; Cheng, R. K.; Chung, G. T.; Wu, S.; Oh, H. B.; Sears, C. L. Molecular evolution of the pathogenicity island of enterotoxigenic Bacteroides fragilis strains. J. Bacteriol. 1999, 181, 6623-6633.
60. Obiso, R. J.; Bevan, D. R.; Wilkins, T. D. Molecular modeling and analysis of the Bacteroides fragilis toxin. Clin. Infect. Dis. 1997, 25, S153-S155.
61. Moncrief, J. S.; Duncan, A. J.; Wright, R. L.; Barroso, L. A.; Wilkins, T. D. Molecular characterization of the fragilysin pathogenicity islet of enterotoxigenic Bacteroides fragilis. Infect. Immun. 1998, 66, 1735-1739.
62. Moncrief, J. S.; Obiso, R. J.; Barroso, L. A.; Kling, J. J.; Wright, R. L.;Van Tassell, R. L.; Lyerly, D. M.;Wilkins, T. D. The enterotoxin of Bacteroides fragilis is a metalloprotease. Infect. Immun. 1995, 63, 175-181.
63. Teplyakov, A.; Polyakov, K.; Obmolova, G. Crystal structure of carboxypeptidase T from Thermoactinomyces vulgaris. Eur. J. Biochem. 1992, 208, 281-288.
64. Strater, N.; Sherratt, D. J.; Colloms, S. D. X-ray structure of aminopeptidase A from Escherichia coli and a model for the nucleoprotein complex in Xer site-specific recombination. EMBO J. 1999, 18, 4513-4522.
65. Strater, N.; Sun, L.; Kantrowitz, E. R.; Lipscomb, W. N. A bicarbonate ion as a general base in the mechanism of peptide hydrolysis by dizinc leucine aminopeptidase. Proc. Natl. Acad. Sci. USA 1999, 96, 11151-11155.
66. Mathew, Z.; Knox, T. M.; Miller,C.G. Salmonella enterica serovar typhimurium peptidase B is a leucyl aminopeptidase with specificity for acidic amino acids. J. Bacteriol. 2000, 182, 3383-3393.
67. Mahadevan, D.; Saldanha, J. W. The extracellular regions of PSMA and the transferrin receptor contain an aminopeptidase domain: implications for drug design. Protein Sci. 1999, 8, 2546-2549.
68. Huntington, K. M.; Bienvenue, D. L.; Wei, Y.; Bennett, B.; Holz, R. C.; Pei, D. Slowbinding inhibition of the aminopeptidase from Aeromonas proteolytica by peptide thiols: synthesis and spectroscopic characterization. Biochemistry 1999, 38, 15587-15596.
69. Sherwood, R. F.; Melton, R. G. Glutamate carboxypeptidase. In Handbook of Proteolytic Enzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 483.
70. Galivan, J.; Ryan, T. J.; Chave, K.; Rhee, M.; Yao, R.; Yin, D. Glutamyl hydrolase: pharmacological role and enzymatic characterization. Pharmacol. Ther. 2000, 85, 207-215.
71. Rowsell, S.; Pauptit, R. A.; Tucker, A. D.; Melton, R. G.; Blow, D. M.; Brick, P. Crystal structure of carboxypeptidase G2, a bacterial enzyme with applications in cancer therapy. Structure 1997, 5, 337-347.
72. Melton, R. G.; Sherwood, R. F. Antibody-enzyme conjugates for cancer therapy. J. Natl. Cancer Inst. 1996, 88, 153-165.
73. Boger, D. L. Vancomycin, teicoplanin and ramoplanin: synthetic and mechanistic studies. Med. Res. Rev. 2001, 21, 356-381.
74. Lessard, I. A.; Walsh, C. T. VanX, a bacterial D-alanyl-D-alanine dipeptidase: resistance, immunity, or survival function? Proc. Natl. Acad. Sci. USA 1999, 96, 11028-11032.
75. Wu, Z.; Walsh, C. T. Dithiol compounds: potent, time-dependent inhibitors of VanX, a zinc-dependent D,D-dipeptidase required for vancomycin resistance in Enterococcus faecium. J. Am. Chem. Soc. 1996, 118, 1785-1786.
76. Bussiere, D. E.; Pratt, S. D.; Katz, L.; Severin, J. M.; Holzman, T.; Park, C. The structure of VanX reveals a novel amino-dipeptidase involved in mediating transposon-based vancomycin resistance. Mol. Cell 1998, 2, 75-84.
77. Mellors, A. O-sialoglycoprotein endopeptidase. In Handbook of Proteolytic Enzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 505.
78. Kessler, E. b-Lytic metalloendopeptidase. In Handbook of Proteolytic Enzymes (CDROM); Barrett, A. J.; Rawlings, N. D.;Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 506.
79. Kessler, E.; Ohman, D. E. Staphylolysin. In Handbook of Proteolytic Enzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter k507.
80. Ryding, U.; Renneberg, J.; Rollof, J.; Christensson, B. Antibody response to Staphylococcus aureus whole cell, lipase and staphylolysin in patients with S. aureus infections. FEMS Microbiol. Immunol. 1992, 4, 105-110.
81. Odintsov, S. G.; Sabala, I.; Marcyjaniak, M.; Bochtler,M. Latent LytM at 1.3Åresolution. J. Mol. Biol. 2004, 335, 775-785.
82. Bochtler, M.; Odintsov, S. G.; Marcyjaniak, M.; Sabala, I. Similar active sites in lysostaphins and D-Ala-D-Ala metallopeptidases. Protein Sci. 2004, 13, 854-861.
83. Plaut, A. G. IgA-specific metalloendopeptidase. In Handbook of Proteolytic Enzymes (CD-ROM); Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Jr., Eds.; Academic Press: London, 1998; Chapter 508.
84. Poulsen, K.; Reinholdt, J.; Jespersgaard, C.; Boye, K.; Brown, T. A.; Hauge, M.; Kilian, M. A comprehensive genetic study of streptococcal immunoglobulin A1 proteases: evidence for recombination within and between species. Infect. Immun. 1998, 66, 181-190.
85. Langer, T. AAA proteases: cellular machines for degrading membrane proteins. Trends Biol. Sci. 2000, 25, 247-251.
86. Schumann, W. FtsH: a single chain chaperonin? FEMS Microbiol. Rev. 1999, 23, 1-11.
87. Makino, S.; Makino, T.; Abe, K.; Hashimoto, J.; Tatsuta, T.; Kitagawa, M.; Mori, H.; Ogura, T.; Fujii, T.; Fushinobu, S.; Wakagi, T.; Matsuzawa, H. Second transmembrane segment of FtsH plays a role in its proteolytic activity and homo-oligomerization. FEBS Lett. 1999, 460, 554-558.
88. Asahara, Y.; Atsuta, K.; Motohashi, K.; Taguchi, H.; Yohda, M.; Yoshida, M. FtsH recognizes proteins with unfolded structure and hydrolyzes the carboxyl side of hydrophobic residues. J. Biochem. (Tokyo) 2000, 127, 931-937.
89. Srinivasan, R.; Anilkumar, G.; Rajeswari, H.; Ajitkumar, P. FEMS Microbiol. Lett. 2006, 259, 97-105.
90. Ito, K.; Akiyama, Y. Cellular functions, mechanism of action, and regulation of FtsH protease. Annu. Rev. Microbiol. 2005, 59, 211-231.
91. Sakoh, M.; Ito, K.; Akiyama, Y. Proteolytic activity of HtpX, a membrane-bound and stress-controlled protease from Escherichia coli. J. Biol. Chem. 2005, 280, 33305-33310.