Kinetic and spectroscopic analysis of the catalytic role of h79 in the methionine aminopeptidase from Escherichia coli

Biochemistry

Volumn 47, Issue 45, 2008, Pages 11885-11893

  Watterson, Sarah J ^b   Mitra, Sanghamitra ^b   Swierczek, Sabina I ^b   Bennett, Brian ^a,c   Holz, Richard C ^a,b  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b UTAH STATE UNIVERSITY   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; BINDING SITES; ENZYMES; ESCHERICHIA COLI; HYDROGEN; HYDROGEN BONDS; MANGANESE; ORGANIC COMPOUNDS; PROTON TRANSFER; PROTONS; SPECTROSCOPIC ANALYSIS;

ACTIVE SITES; AMINE GROUPS; BACKBONE CARBONYLS; CATALYTIC MECHANISMS; CATALYTIC ROLES; CRYSTALLOGRAPHIC DATUMS; GAIN INSIGHTS; HISTIDINE RESIDUES; HYDROGEN BONDINGS; KINETIC ISOTOPES; METAL BINDINGS; METHIONINE AMINOPEPTIDASE; MUTATED ENZYMES; PEPTIDE LINKAGES; REACTION MECHANISMS; SPECIFIC ACTIVITIES; TRANSITION STATES;

MANGANESE COMPOUNDS;

AMINE; CARBONYL DERIVATIVE; COBALT; HISTIDINE; MANGANESE; METHIONYL AMINOPEPTIDASE;

ARTICLE; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SPECIFICITY; ESCHERICHIA COLI; HYDROGEN BOND; METAL BINDING; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; SPECTROSCOPY; ULTRAVIOLET SPECTROSCOPY; WILD TYPE; X RAY CRYSTALLOGRAPHY;

AMINOPEPTIDASES; BINDING SITES; CATALYSIS; COBALT; CRYSTALLOGRAPHY, X-RAY; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HISTIDINE; IRON; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED;

ESCHERICHIA COLI;

EID: 55849098590     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801499g     Document Type: Article

References (47)

1. Copik, A. J., Swierczek, S. I., Lowther, W. T., D'souza, V., Matthews, B. W., and Holz, R. C. (2003) Kinetic and Spectroscopic Characterization of the H178A Mutant of the Methionyl Aminopeptidase from Escherichia coli. Biochemistry 42, 6283-6292.
2. Bradshaw, R. A. (1989) Protein translocation and turnover in eukaryotic cells. Trends Biochem. Sci. 14, 276-279.
3. Meinnel, T., Mechulam, Y., and Blanquet, S. (1993) Methionine as Translation Start Signal: A Review of the Enzymes of the Pathway in Escherichia coli. Biochimie 75, 1061-1075.
4. α-acetyl transferase families. Trends Biochem. Sci. 23, 263-267.
5. Arfin, S. M., and Bradshaw, R. A. (1988) Corranslational processing and protein turnover in eukaryotic cells. Biochemistry 27 (21), 7979-7984.
6. Lowther, W. T., and Matthews, B. W. (2002) Metalloaminopeptidases: Common Functional Themes in Disparate Structural Suroundings. Chem. Rev. 102, 4581-4607.
7. Lowther, W. T., and Matthews, B. W. (2000) Structure and function of the methionine aminopeptidases. Biochim. Biophys. Acta 1477, 157-167.
8. Chang, S.-Y. P., McGary, E. C., and Chang, S. (1989) Methionine Aminopeptidase gene of Escherichia coli is essential for cell growth. J. Bacteriol. 171 (7), 4071-4072.
9. Chang, Y.-H., Teichert, U., and Smith, J. A. (1992) Molecular cloning, sequencing, deletion, and overexpression of a methionine aminopeptidase gene from Saccharomyces cerevisiae. J. Biol. Chem. 267, 8007-8011.
10. Li, X., and Chang, Y.-H. (1995) Amino terminal protein processing in Saccharomyces cerevisiae is an essential function that requires two distinct methionine aminopeptidases. Proc. Natl. Acad. Sci. U.S.A. 92, 12357-12361.
11. Miller, C. G., Kukral, A. M., Miller, J. L., and Movva, N. R. (1989) pepM is an essential gene in Salmonella typhimurium. J. Bacteriol. 171, 5215-5217.
12. Taunton, J. (1997) How to starve a tumor. Chem. Biol. 4, 493-496.
13. Griffith, E. C., Su, Z., Turk, B. E., Chen, S., Chang, Y. H., Wu, Z., Biemann, K., and Liu, J. O. (1997) Methionine aminopeptidase (type 2) is the common target for angiogenesis inhibitors AGM-1470 and ovalicin. Chem. Biol. 4, 461-471.
14. Sin, N., Meng, L., Wang, M. Q., Wen, J. J., Bornmann, W. G., and Crews, C. M. (1997) The anti-angiogenic agent fumagillin covalently binds and inhibits the mathionine aminopeptidase, MetAP-2. Proc. Natl. Acad. Sci. U.S.A. 94, 6099-6103.
15. Liu, S., Widom, J., Kemp, C. W., Crews, C. M., and Clardy, J. (1998) Structure of the human methionine aminopeptidase-2 complexed with fumagillin. Science 282, 1324-1327.
16. Lowther, W. T., McMillen, D. A., Orville, A. M., and Matthews, B. W. (1998) The anti-angiogenic agent fumagillin covalently modifies a conserved active site histidine in the Escherichia coli methionine aminopeptidase. Proc. Natl. Acad. Sci. U.S.A. 95, 12153-12157.
17. Douangamath, A., Dale, G. E., D'Arcy, A., Almstetter, M., Eckl, R., Frutos-Hoener, A., Henkel, B., Illgen, K., Nerdinger, S., Schulz, H., MacSweeney, A., Thormann, M., Treml, A., Pierau, S., Wadman, S., and Oefner, C. (2004) J. Med. Chem. 47, 1325-1328.
18. Tahirov, T. H., Oki, H., Tsukihara, T., Ogasahara, K., Yutani, K., Ogata, K., Izu, Y., Tsunasawa, S., and Kato, I. (1998) Crystal structure of the methionine aminopeptidase from the hyperthermophile Pyrococcus furiosus. J. Mol. Biol. 284, 101-124.
19. Lowther, W. T., Orville, A. M., Madden, D. T., Lim, S., Rich, D. H., and Matthews, B. W. (1999) Escherichia coli Methionine Aminopeptidase: Implications of crystallographic analyses of the native, mutant and inhibited enzymes for the mechanism of catalysis. Biochemistry 38, 7678-7688.
20. Roderick, L. S., and Matthews, B. W. (1993) Structure of the Cobalt-Dependent Methionine Aminopeptidase from Escherichia coli: A new type of proteolytic enzyme. Biochemistry 32, 3907-3912.
21. Spraggon, G., Schwarzenbacher, R., Kreusch, A., McMullan, D., Brinen, L. S., Canaves, J. M., Dai, X., Deacon, A. M., Elsliger, M. A., Eshagi, S., Floyd, R., Godzik, A., Grittini, C., Grzechnik, S. K., Jaroszewski, L., Karlak, C., Klock, H. E., Koesema, E., Kovarik, J. S., Kuhn, P., McPhillips, T. M., Miller, M. D., Morse, A., Moy, K., Ouyang, J., Page, R., Quijano, K., Rezezadeh, F., Robb, A., Sims, E., Stevens, R. C., van den Bedem, H., Velasquez, J., Vincent, J., von Delft, F., Wang, X., West, B., Wolf, G., Xu, Q., Hodgson, K. O., Wooley, J., Lesley, S. A., and Wilson, I. A. (2004) Proteins 56, 396-400.
22. Addlagatta, A., Hu, X., Liu, J. O., and Matthews, B. W. (2005) Structural basis for the finctonal differences between type I and type H human methionine aminopeptidases. Biochemistry 44, 14741-14749.
23. D'souza, V. M., Bennett, B., Copik, A. J., and Holz, R. C. (2000) Characterization of the Divalent Metal Binding Properties of the Methionyl Aminopeptidase from Escherichia coli. Biochemistry 39, 3817-3826.
24. Cosper, N. J., D'souza, V., Scott, R., and Holz, R. C. (2001) Structural Evidence that the Methionyl Aminopeptidase from Escherichia coli is a Mononuclear Metalloprotease. Biochemistry 40, 13302-13309.
25. Ye, Q. Z., Xie, S. X., Ma, Z. Q., Huang, M., and Hanzlik, R. P. (2006) Structural Basis of Catalysis by Monometalated Methionine Aminopeptidase. Proc. Natl. Acad. Sci. U.S.A. 103, 9470-9475.
26. Lowther, T. W., Zhang, Y., Sampson, P. B., Honek, J. F., and Matthews, B. W. (1999) Insights into the mechanism of E. coli methionine aminopeptidase from the structural analysis of reaction products and phosphorous-based transition state analogs. Biochemistry 38, 14810-14819.
27. Huang, M., Xie, S. X., Ma, Z. Q., Hanzlik, R. P., and Ye, Q. Z. (2006) Metal mediated inhibition of methionine aminopeptidase by quinolinyl sulfonamides. Biochem. Biophys. Res. Commun. 339, 506-513.
28. Li, J.-Y., Cui, Y.-M., Chen, L.-L., Gu, M., Li, J., Nan, F. J., and Ye, Q. Z. (2004) Mutations at the S1 Sites of Methionine Aminopeptidases from Escherichia coli and Homo sapiens Reveal the Residues Critical for Substrate Specificity. J. Biol. Chem. 279, 21128-21134.
29. D'souza, V. M., and Holz, R. C. (1999) The Methionyl Aminopeptidase from Escherichia coli is an Iron(II) Containing Enzyme. Biochemistry 38, 11079-11085.
30. D'souza, V. M., Bennett, B., and Holz, R. C. (2000) Characterization of the Divalent Metal Binding Properties of the Methionyl Aminopeptidase from Escherichia coli. Biochemistry 39, 3817-3826.
31. Salomaa, P., Schaleger, L. L., and Long, F. A. (1964) Solvent Deuterium Isotope Effects on Acid-Base Equilibria. J. Am. Chem. Soc. 86, 1-7.
32. Albery, W. J. (1975) Proton Transfer Reactions, Chapman & Hall, London.
33. Venkatasubban, K. S., and Schowen, R. L. (1984) The proton inventory technique. CRC Crit. Rev. Biochem. 17, 1-44.
34. Elrod, J. P., Hogg, J. L., Quinn, D. M., Venkatasubban, K. S., and Schowen, R. L. (1980) Protionic reorganization and substrate structure in catalysis by serine proteases. J. Am. Chem. Soc. 102, 3917-3922.
35. Izatt, R. M., and Christensen, J. J. (1976) Heats of proton ionization, pK, and related thermodynamic quantities, 3rd ed., Vol. 1, CRC Press, Cleveland, OH.
36. Winzor, D. J., and Sawyer, W. H. (1995) Quantitative Characterization of Ligand Binding, Wiley-Liss, New York.
37. Griffith, E. C., Su, Z., Niwayama, S., Ramsay, C. A., Chang, Y.-H., and Liu, J. O. (1998) Molecular recognition of angiogenesis inhibitors fumagillin and ovalicin by methionine aminopeptidase 2. Proc. Natl. Acad. Sci. U.S.A. 95, 15183-15188.
38. Larrabee, J. A., Leung, C. H., Moore, R., Thamrong.nawasawat, T., and Wessler, B. H. (2004) Magnetic Circular Dichroism and Cobalt(II) Binding Equilibrium Studies of Escherichia coli Methionyl Aminopeptidase. J. Am. Chem. Soc. 126, 12316-12324.
39. Hu, X. V., Chen, X., Han, K. C., Mildvan, A. S., and Liu, J. O. (2007) Kinetic and Mutational Studies of the Number of Interacting Divalent Cations Required by Bacterial and Human Methionine Aminopeptidases. Biochemistry 46, 12833-12843.
40. Wang, J., Sheppard, G. S., Lou, P., Kawai, M., Park, C., Egan, D. A., Schneider, A., Bouska, J., Lesniewski, R., and Henkin, J. (2003) Physiologically relevant metal cofactor for methionine aminopeptidase-2 is manganese. Biochemistry 42, 5035-5042.
41. Chai, S. C., Wang, W.-L., and Ye, Q.-Z. (2008) Fe(II) is the native cofactor for Escherichia coli methionine aminopeptidase. J. Biol. Chem. 283, 26879-26885.
42. Whiting, A. K., Boldt, Y. R., Hendrich, M. P., Wackett, L. P., and Que, L. (1996) Manganese(II)-dependent extradiol-cleaving chatechol dioxygenase from Arthrobacter globiformis CM-2. Biochemistry 35, 160-170.
43. Cleland, W. W. (1982) Use of isotope effects to elucidate enzyme mechanisms. Crit. Rev. Biochem. 13, 385-427.
44. Kaiser, E. T., and Kaiser, B. L. (1972) Carboxypeptidase A. Mechanistic analysis. Acc. Chem. Res. 5, 219-224.
45. 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.
46. Wang, Z., Fast, W., Valentine, A. M., and Benkovic, S. J. (1999) Metallo-β-lactamase: Structure and mechanism. Curr. Opin. Chem. Biol. 3, 614-622.
47. Chen, G., Edwards, T., D'souza, V. M., and Holz, R. C. (1997) Mechanistic studies on the aminopeptidase from Aeromonas proteolytica: A two-metal ion mechanism for peptide hydrolysis. Biochemistry 36, 4278-4286.