Experimental evidence for a metallohydrolase mechanism in which the nucleophile is not delivered by a metal ion: EPR spectrokinetic and structural studies of aminopeptidase from Vibrio proteolyticus

Biochemical Journal

Volumn 403, Issue 3, 2007, Pages 527-536

  Kumar, Amit ^a   Periyannan, Gopal Raj ^a   Narayanan, Beena ^a   Kittell, Aaron W ^a   Kim, Jung Ja ^a   Bennett, Brian ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Aminopeptidase; Cobalt; EPR; Metallohydrolase; Vibrio proteolyticus; Zinc

Indexed keywords

AMINOPEPTIDASE; METALLOHYDROLASE; VIBRIO PROTEOLYTICUS;

COBALT; NUCLEOPHILES; PARAMAGNETIC RESONANCE; PROTEOLYSIS; X RAYS; ZINC;

ENZYME INHIBITION;

AMINOPEPTIDASE; ASPARTIC PROTEINASE; BESTATIN; GLUTAMIC ACID; HYDROLASE; HYDROXYL GROUP; LEUCYLLEUCYLLEUCINE; METAL ION; METALLO BETA LACTAMASE; METALLOHYDROLASE; PEPTIDE DERIVATIVE; UNCLASSIFIED DRUG; WATER; BACTERIAL LEUCYL AMINOPEPTIDASE; BACTERIAL PROTEIN; OLIGOPEPTIDE;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; ENZYME MECHANISM; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PROTEOMICS; STRUCTURE ANALYSIS; VIBRIO; VIBRIO PROTEOLYTICUS; CHEMISTRY; CRYSTALLIZATION; KINETICS; METABOLISM; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS); VIBRIO PROTEOLYTICUS;

AMINOPEPTIDASES; BACTERIAL PROTEINS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ELECTRON SPIN RESONANCE SPECTROSCOPY; KINETICS; OLIGOPEPTIDES;

EID: 34247871295     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061591     Document Type: Article

References (57)

1. Bennett, B. (2002) EPR of Co(II) as a structural and mechanistic probe of metalloprotein active sites: characterisation of an aminopeptidase. Curr. Top. Biophys. 26, 49-57
2. Barrett, A. J. and Rawlings, N. D. (eds) (1998) Handbook of Proteolytic Enzymes, Elsevier Academic Press, London
3. Arfin, S. M. and Bradshaw, R. A. (1988) Cotranslational processing and protein turnover in eukaryotic cells. Biochemistry 27, 7979-7984
4. Bradshaw, R. A. (1988) Protein translocation and turnover in eukaryotic cells. Trends Biochem. Sci. 14, 276
5. Arechaga, G., Martinez, J. M., Prieto, I., Ramirez, M. J., Alba, F. and Ramirez, M. (1999) Changes in membrane-bound leucine aminopeptidase activity during maturation and ageing of brain. Biochem. Mol. Biol. Int. 47, 861-868
6. Taylor, A., Daims, M., Lee, J. and Surgenor, T. (1982) Identification and quantification of leucine aminopeptidase in aged normal and cataractous human lenses and ability of bovine lens LAP to cleave bovine crystallins. Curr. Eye Res. 2, 47-56
7. Pulido-Cejudo, G., Conway, B., Proulx, P., Brown, R. and Izaguirre, C. A. (1997) Bestatin-mediated inhibition of leucine aminopeptidase may hinder HIV infection. Antivir. Res. 36, 167-177
8. Scoglio, M. E., DiPietro, A., Picerno, I., Delia, S., Mauro, A. and Lagana, P. (2001) Virulence factors in Vibrios and Aeromonads isolated from seafood. New Microbiol. 24, 273-280
9. Hashida, H., Takabayashi, A., Kanai, M., Adachi, M., Kondo, K., Kohno, N., Yamaoka, Y. and Miyake, M. (2002) Aminopeptidase N is involved in cell motility and angiogenesis: its clinical significance in human colon cancer. Gastroenterology 122, 376-386
10. Zhang, P., Nicholson, D. E., Bujnicki, J. M., Su, X., Brendle, J. J., Ferdig, M., Kyle, D. E., Milhous, W. K. and Chiang, P. K. (2002) Angiogenesis inhibitors specific for methionine aminopeptidase 2 as drugs for malaria and leishmaniasis. J. Biomed. Sci. 9, 34-40
11. Ishii, K., Usui, S., Sugimura, Y., Yoshida, S., Hioki, T., Tatematsu, M., Yamamoto, H. and Hirano, K. (2001) Aminopeptidase N regulated by zinc in human prostate participates in tumor cell invasion. Int. J. Cancer 92, 49-54
12. Kaznowski, A. and Wlodarczak, K. (1991) Enzymatic characterization of Vibrionaceae strains isolated from environment and cold-blooded animals. Acta Microbiol. Pol. 40, 71-76
13. Maras, B., Greenblatt, H. M., Shoham, G., Spungin-Bialik, A., Blumberg, S. and Barra, D. (1997) Aminopeptidase from Streptomyces griseus: primary structure and comparison with other zinc-containing aminopeptidases. Eur. J. Biochem. 236, 843-846
14. Centers for Disease Control (CDC) (1990) Aeromonas wound infections associated with outdoor octivities: California. MMWR Morb. Mortal. Wkly. Rep. 39, 334-335
15. Centers for Disease Control, Prevention (CDC) (1998) Outbreak of Vibrio parahaemolyticus infections associated with eating raw oysters: Pacific Northwest, 1997. MMWR Morb. Mortal. Wkly. Rep. 47, 457-462
16. Centres for Disease Control, Prevention (CDC) (1999) Outbreak of Vibrio parahaemolyticus infection associated with eating raw oysters and clams harvested from Long Island Sound: Connecticut, New Jersey and New York, 1998. MMWR Morb. Mortal. Wkly. Rep. 48, 48-51
17. Yadav, A. S. and Kumar, A. (2000) Prevalence of enterotoxigenic motile aeromonads in children, fish, milk and ice-cream and their public health significance. Southeast Asian J. Trop. Med. Public Health 31, (Suppl. 1), 153-156
18. Benassi, F. O., Vergara, M., von Specht, M. H., Garcia, M. A., Quiroga, M. I., Pucciarelli, A. B., Zubreski, E., Laczeski, M., Martin, B. M., Leardini, N. and Gutkind, G. (2001) β-Lactam antibiotic sensitivity in Aeromonas spp. of clinical, animal and environmental origin. Rev. Argent. Microbiol. 33, 47-51
19. Hansen, L. T., Austin, J. W. and Gill, T. A. (2001) Antibacterial effect of protamine in combination with EDTA and refrigeration. Int. J. Food Microbiol. 66, 149-161
20. Fujii, H., Nakajima, M., Aoyagi, T. and Tsuruo, T. (1996) Inhibition of tumor cell invasion and matrix degradation by aminopeptidase inhibitor. Biol. Pharm. Bull. 19, 6-10
21. Jones, D. T. (1999) GenTHREADER: An efficient and reliable protein fold recognition method for genomic sequences. J. Mol. Biol. 287, 797-815
22. Davis, M. I., Bennett, M. J., Thomas, L. M. and Bjorkman, P. J. (2005) Crystal structure of prostate-specific membrane antigen, a tumor marker and peptidase. Proc. Natl. Acad. Sci. U.S.A. 102, 5981-5986
23. Chevrier, B., Schalk, C., D'Orchymont, H., Rondeau, J.-M., Moras, D. and Tarnus, C. (1994) Crystal structure of Aeromonas proteolytica aminopeptidase: a prototypical member of the co-catalytic zinc enzyme family. Structure 2, 283-291
24. Bennett, B. and Holz, R. C. (1997) EPR studies on the mono- and dicobalt(II)-substituted forms of the aminopeptidase from Aeromonas proteolytica: insight into the catalytic mechanism of dinuclear hydrolases. J. Am. Chem. Soc. 119, 1923-1933
25. Bennett, B. and Holz, R. C. (1997) Spectroscopically distinct cobalt(II) sites in heterodimetallic forms of the aminopeptidase from Aeromonas proteolytica: characterization of substrate binding. Biochemistry 36, 9837-9846
26. Prescott, J. M., Wagner, F. W., Holmquist, B. and Vallee, B. L. (1985) Spectral and kinetic studies of metal-substituted Aeromonas aminopeptidase: nonidentical, interacting metal-binding sites. Biochemistry 24, 5350-5356
27. Bennett, B. and Holz, R. C. (1998) Inhibition of the aminopeptidase from Aeromonas proteolytica by L-leucinephosphonic acid, a transition state analogue of peptide hydrolysis. J. Am. Chem. Soc. 120, 12139-12140
28. 151 and two zinc ions of the cocatalytic unit. Eur. J. Biochem. 237, 393-398
29. DePaola, C., Bennett, B., Holz, R. C., Ringe, D. and Petsko, G. (1999) L-Butaneboronic acid binding to Aeromonas proteolytica aminopeptidase: a case of arrested development. Biochemistry 38, 9048-9053
30. Stamper, C., Bennett, B., Edwards, T., Holz, R. C., Ringe, D. and Petsko, G. (2001) inhibition of the aminopeptidase from Aeromonas proteolytica by L-leucinephosphonic acid: spectroscopic and crystallographic characterization of the transition state of peptide hydrolysis. Biochemistry 40, 7035-7036
31. Stamper, C. C., Bienvenue, D. L., Bennett, B., Ringe, D., Petsko, G. and Holz, R. C. (2004) Spectroscopic and X-ray crystallographic characterization of bestatin bound to the aminopeptidase from Aeromonas (Vibrio) proteolytica. Biochemistry 43, 9620-9628
32. Bzymek, K. P. and Holz, R. C. (2004) The catalytic role of glutamate 151 in the leucine aminopeptidase from Aeromonas proteolytica. J. Biol. Chem. 279, 31018-31025
33. Bayliss, M. E. and Prescott, J. M. (1986) Modified activity of Aeromonas aminopeptidase: metal ion substitution and role of substrates. Biochemistry 25, 8113-8117
34. Bayliss, M. E., Wilkes, S. H. and Prescott, J. M. (1980) Aeromonas neutral protease: specificity toward extended substrates. Arch. Biochem. Biophys. 204, 214-219
35. Izawa, T., Ishikawa, S., Tanokura, T., Ohta, K. and Hayashi, K. (1997) Purification and characterization of Aeromonas caviae aminopeptidase possessing debittering activity. J. Agric. Food Chem. 45, 4897-4902
36. Wagner, F. W., Wilkes, S. H. and Prescott, J. M. (1972) Specificity of Aeromonas aminopeptidase towards amino acid amides and dipeptides. J. Biol. Chem. 247, 1208-1210
37. Wilkes, S. H., Bayliss, M. E. and Prescott, J. M. (1973) Specificity of Aeromonas aminopeptidase towards oligopeptides and polypeptides. Eur. J. Biochem. 34, 159-166
38. Prescott, J. M., Wagner, F. W., Holmquist, B. and Vallee, B. L. (1983) One hundred fold increased activity of Aeromonas aminopeptidase by sequential substitutions with Ni(II) or Cu(II) followed by zinc. Biochem. Biophys. Res. Commun. 114, 646-652
39. Xu, D., Xie, D. and Guo, H. (2006) Catalytic mechanism of class B2 metallo-β-lactamase. J. Biol. Chem. 281, 8740-8747
40. Gill, S. C. and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326
41. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
42. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
43. Bzymek, K. P., D'Souza, V. M., Chen, G., Campbell, H., Mitchell, A. and Holz, R. C. (2004) Function of the signal peptide and N- and C-terminal propeptides in the leucine aminopeptidase from Aeromonas proteolytica. Protein Expression Purif. 37, 294-305
44. Marangoni, A. G. (2003) Characterization of enzyme activity. Enzyme Kinetics: A Modern Approach, pp. 44-60, John Wiley & Sons, Hoboken
45. Garrity, J. D., Bennett, B. and Crowder, M. W. (2005) Direct evidence that the reaction intermediate of metallo-β-lactamase L1 is metal bound. Biochemistry 44, 1078-1087
46. Hanson, G. R., Gates, K. E., Noble, C. J., Mitchell, A., Benson, S., Griffin, M. and Burrage, K. (2003) XSophe-Sophe-XeprView: a computer simulation software suite for the analysis of continuous wave EPR spectra. In EPR of Free Radicals in Solids: Trends in Methods and Applications (Shiotani, M. and Lund, A., eds.), pp. 197-237, Kluwer Press, Dordrecht
47. Desmarais, W., Bienvenue, D. L., Bzymek, K., Holz, R. C., Petsko, G. and Ringe, D. (2002) The 1.20 Å resolution crystal structure of the aminopeptidase from Aeromonas proteolytica complexed with Tris: a tale of buffer inhibition. Structure 10, 1063-1072
48. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
49. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760-763
50. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 54, 905-921
51. Laskowski, R. A., MacArthur, M. W., Moss, D. S. and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
52. Schechter, I. and Berger, A. (1967) On the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162
53. Copik, A. J., Waterson, S., Swierczek, S. I., Bennett, B. and Holz, R. C. (2005) Both nucleophile and substrate bind to the catalytic Fe(II)-center in the type-II methionyl aminopeptidase from Pyrococcus turiosus. Inorg. Chem. 44, 1160-1162
54. Horecker, B. L., Tsolas, O. and Lai, C. Y. (1972) Aldolases. In The Enzymes (Boyer, P. D., ed.), pp. 213-258, Academic Press, New York
55. Baker, J. O. and Prescott, J. M. (1983) Aeromonas aminopeptidase: pH dependence and a transition-state-analogue inhibitor. Biochemistry 22, 5322-5331
56. Lipscomb, W. N. and Sträter, N. (1996) Recent advances in zinc enzymology. Chem. Rev. 96, 2375-2433
57. Bennett, B., Antholine, W. E., D'souza, V. M., Chen, G., Ustinyuk, L. and Holz, R. C. (2002) Structurally distinct active sites in the copper(II)-substituted aminopeptidase from Aeromonas proteolytica. J. Am. Chem. Soc. 124, 13025-13034