Structural relationship between the active sites of β-Lactam- recognizing and amidase signature enzymes: Convergent evolution?

Biochemistry

Volumn 49, Issue 45, 2010, Pages 9688-9697

  Pratt, R F ^a   McLeish, Michael J ^b  

^a WESLEYAN UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; AMIDASE; AMIDOHYDROLASE SUPERFAMILY; BACTERIAL CELLS; BACTERIAL PROTEIN; BACTERIAL RESISTANCE; CONVERGENT EVOLUTION; LACTAMASES; NH GROUPS; OXYANION HOLE; SPATIAL OVERLAP; STRUCTURAL RELATIONSHIP;

AMIDES; AMINO ACIDS; ANTIBIOTICS; BACTERIOLOGY; BIOCHEMISTRY; CELL MEMBRANES; ENZYMES; POSITIVE IONS;

CATALYSTS;

AMIDASE; AMIDASE SIGNATURE ENZYME; BACTERIAL PROTEIN; BETA LACTAM; BETA LACTAM RECOGNIZING ENZYME; NUCLEOPHILE; PEPTIDASE; SERINE DEHYDRATASE; UNCLASSIFIED DRUG;

ACTINOMADURA; BIOSYNTHESIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME MECHANISM; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; STREPTOCOCCUS; STREPTOCOCCUS PNEUMONIAE;

AMIDOHYDROLASES; AMINO ACID SEQUENCE; BACTERIA; BETA-LACTAMS; CATALYTIC DOMAIN; CHYMOTRYPSIN; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; PEPTIDE HYDROLASES; PROTEIN FOLDING; SERINE; SERINE PROTEASES; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; STREPTOMYCES; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS);

EID: 78149418550     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1012222     Document Type: Review

References (63)

1. Orengo, C. A. and Thornton, J. M. (2005) Protein families and their evolution: A structural perspective Annu. Rev. Biochem. 74, 867-900
2. Murzin, A. G., Brenner, S. E., Hubbard, T., and Chothia, C. (1995) SCOP: A structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247, 536-540
3. Orengo, C. A., Pearl, F. M., Bray, J. E., Todd, A. E., Martin, A. C., Lo, C. L., and Thornton, J. M. (1999) The CATH database provides insights into protein structure/function relationships Nucleic Acids Res. 27, 275-279
4. Hanson, K. R. and Rose, I. A. (1975) Interpretation of enzyme stereospecificity Acc. Chem. Res. 8, 1-10
5. Polgár, L. (2005) The catalytic triad of serine peptidases Cell. Mol. Life Sci. 62, 2161-2172
6. Botos, I. and Wlodawer, A. (2007) The expanding diversity of serine hydrolases Curr. Opin. Struct. Biol. 17, 683-690
7. Ekici, O. D., Paetzel, M., and Dalbey, R. E. (2008) Unconventional serine proteases: Variations on the catalytic Ser/His/Asp triad configuration Protein Sci. 17, 2023-2037
8. Gherardini, P. F., Wass, M. N., Helmer-Citterich, M., and Sternberg, M. J. E. (2007) Convergent evolution of enzyme active sites is not a rare phenomenon J. Mol. Biol. 372, 817-845
9. Alva, V., Remmert, M., Biegert, A., Lupas, A. N., and Söding, J. (2010) A galaxy of folds Protein Sci. 19, 124-130
10. Rawlings, N. D., Barrett, A. J., and Bateman, A. (2010) MEROPS: The peptidase database Nucleic Acids Res. 38, D227-D233
11. Kraut, J. (1977) Serine proteases: Structure and mechanism of catalysis Annu. Rev. Biochem. 46, 331-358
12. Menard, R. and Storer, A. C. (1992) Oxyanion hole interactions in serine and cysteine proteases Biol. Chem. Hoppe-Seyler 373, 393-400
13. Ghuysen, J.-M. (1990) Serine β-lactamases and penicillin-binding proteins Annu. Rev. Microbiol. 45, 37-67
14. Goffin, C. and Ghuysen, J.-M. (1998) Multimodular penicillin-binding proteins: An enigmatic family of orthologs and paralogs Microbiol. Mol. Biol. Rev. 62, 1079-1093
15. Goffin, C. and Ghuysen, J.-M. (2002) Biochemistry and comparative genomics of SXXK superfamily acyltransferases offer a clue to the mycobacterial paradox: Presence of penicillin-susceptible target proteins versus lack of efficiency of penicillin as therapeutic agent Microbiol. Mol. Biol. Rev. 66, 702-738
16. Popham, D. L. and Young, K. D. (2003) Role of penicillin-binding proteins in bacterial cell morphogenesis Curr. Opin. Microbiol. 57, 594-599
17. Stewart, G. C. (2005) Taking shape: Control of bacterial cell wall biosynthesis Mol. Microbiol. 57, 1171-1181
18. Macheboeuf, P., Contreras-Martel, C., Job, V., Dideberg, O., and Dessen, A. (2006) Penicillin-binding proteins: Key players in bacterial cell cycle and drug resistance processes FEMS Microbiol. Rev. 30, 673-691
19. Sauvage, E., Kerff, F., Terrak, M., Ayala, J. A., and Charlier, P. (2008) The penicillin-binding proteins: Structure and role in peptidoglycan biosynthesis FEMS Microbiol. Rev. 32, 234-258
20. Lovering, A. L., Gretes, M., and Strynadka, N. C. J. (2008) Structural details of the glycosyltransferase step of peptidoglycan assembly Curr. Opin. Struct. Biol. 18, 534-543
21. Dzhekieva, L., Rocaboy, M., Kerff, F., Charlier, P., Sauvage, E., and Pratt, R. F. (2010) Crystal structure of a complex between the Actinomadura R39 dd -peptidase and a peptidoglycan-mimetic boronate inhibitor: Interpretation of a transition state analogue in terms of catalytic mechanism Biochemistry 49, 6411-6419
22. Sauvage, E., Powell, A. J., Heilemann, J., Josephine, H. R., Charlier, P., Davies, C., and Pratt, R. F. (2008) Crystal structures of complexes of bacterial dd -peptidases with peptidoglycan-mimetic ligands: The substrate specificity puzzle J. Mol. Biol. 381, 383-393
23. Pratt, R. F. (2008) Substrate specificity of bacterial dd -peptidases (penicillin-binding proteins) Cell. Mol. Life Sci. 65, 2138-2155
24. Pratt, R. F. (2002) Functional evolution of the β-lactamase active site J. Chem. Soc., Perkin Trans. 2, 851-861
25. Bompard-Gilles, C., Remaut, H., Villeret, V., Prangé, T., Fanuel, L., Delmarcelle, M., Joris, B., Frère, J.-M., and Van Beeumen, J. (2000) Crystal structure of a d -aminopeptidase from Ochrobactrum anthropi, a new member of the "penicillin-recognizing" family Structure 8, 971-980
26. Okazaki, S., Suzuki, A., Komeda, H., Yamaguchi, S., Asano, Y., and Yamane, T. (2007) Crystal structure and functional characterization of a d -stereospecific amino acid amidase from Ochrobactrum anthropi SV3, a new member of the penicillin-recognizing enzymes J. Mol. Biol. 368, 79-91
27. Kelly, J. A. and Kuzin, A. P. (1995) The refined crystallographic structure of a dd -peptidase penicillin-target enzyme at 1.6 Å resolution J. Mol. Biol. 254, 223-236
28. Wagner, U. G., Petersen, E. I., Schwab, H., and Kratky, C. (2002) Est B from Burkholderia gladioli: A novel esterase with a β-lactamase fold reveals steric factors to discriminate between esterolytic and β-lactam cleaving activity Protein Sci. 11, 467-478
29. Schütte, M. and Fetzner, S. (2007) Est A from Arthrobacter nitroguajacolicus Rübia, a thermo- and solvent-tolerant carboxylesterase related to class C β-lactamases Curr. Microbiol. 54, 230-236
30. Kawashima, Y., Ohki, T., Shibata, N., Higuchi, Y., Wakitani, Y., Matsuura, Y., Nakata, Y., Takeo, M., Kaito, D., and Negoro, S. (2009) Molecular design of a nylon-6 byproduct-degrading enzyme from a carboxylesterase with a β-lactamase fold FEBS J. 276, 2547-2556
31. Yoshimune, K., Shirakihara, Y., Shiratori, A., Wakayama, M., Chantawannakul, P., and Moriguchi, M. (2006) Crystal structure of a major fragment of the salt-tolerant glutaminase from Micrococcus luteus K-3 Biochem. Biophys. Res. Commun. 346, 1118-1124
32. Brown, G., Singer, A., Proudfoot, C. F., Skarinaa, T., Kim, Y., Chang, C., Dementieva, I., Kuznetsova, E., Gonzalez, C. F., Joachimiak, A., Savchenko, A., and Yakunin, A. F. (2008) Functional and structural characterization of four glutaminases from Escherichia coli and Bacillus subtilis Biochemistry 47, 5724-5735
33. Peitsaro, N., Polianskyte, Z., Tuimala, J., Pörn-Ares, I., Liobikas, J., Speer, O., Lindholm, D., Thompson, J., and Eriksson, O. (2008) Evolution of a family of metazoan active-site serine enzymes from penicillin-binding proteins: A novel facet of the bacterial legacy BMC Evol. Biol. 8, 26
34. Smith, T. S., Southern, C., Ellington, K., Campbell, D., Tew, D. G., and Debouck, D. (2001) Identification, genomic organization and mRNA expression of LACTB, encoding a serine β-lactamase-like protein with an amino-terminal transmembrane domain Genomics 78, 12-14
35. Polianskyte, Z., Peitsaro, N., Dapkunas, A., Liobikas, J., Soliymani, R., Lalowski, M., Speer, O., Seitsonen, J., Butcher, S., Cereghetti, G. M., Linder, M. O., Merckel, M., Thompson, J., and Ericksson, O. (2009) LACTB is a filament-forming protein localized in mitochondria Proc. Natl. Acad. Sci. U.S.A. 106, 18960-18965
36. Mayaux, J. F., Cerbelaud, E., Soubrier, F., Yeh, P., Blanche, F., and Petre, D. (1991) Purification, cloning, and primary structure of a new enantiomer-selective amidase from a Rhodococcus strain: Structural evidence for a conserved genetic coupling with nitrile hydratase J. Bacteriol. 173, 6694-6704
37. Chebrou, H., Bigey, F., Arnaud, A., and Galzy, P. (1996) Study of the amidase signature group Biochim. Biophys. Acta 1298, 285-293
38. Cravatt, B. F., Giang, D. K., Mayfield, S. P., Boger, D. L., Lerner, R. A., and Gilula, N. B. (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides Nature 384, 83-87
39. Shin, S., Lee, T. H., Ha, N. C., Koo, H. M., Kim, S. Y., Lee, H. S., Kim, Y. S., and Oh, B.-H. (2002) Structure of malonamidase E2 reveals a novel Ser-cisSer-Lys catalytic triad in a new serine hydrolase fold that is prevalent in nature EMBO J. 21, 2509-2516
40. Hashimoto, Y., Nishiyama, M., Ikehata, O., Horinouchi, S., and Beppu, T. (1991) Cloning and characterization of an amidase gene from Rhodococcus species N-774 and its expression in Escherichia coli Biochim. Biophys. Acta 1088, 225-233
41. Gomi, K., Kitamoto, K., and Kumagai, C. (1991) Cloning and molecular characterization of the acetamidase-encoding gene (amd S) from Aspergillus oryzae Gene 108, 91-98
42. Gaffney, T. D., da Costa e Silva, O., Yamada, T., and Kosuge, T. (1990) Indoleacetic acid operon of Pseudomonas syringae subsp. savastanoi: Transcription analysis and promoter identification J. Bacteriol. 172, 5593-5601
43. Shapir, N., Sadowsky, M. J., and Wackett, L. P. (2005) Purification and characterization of allophanate hydrolase (AtzF) from Pseudomonas sp. strain ADP J. Bacteriol. 187, 3731-3738
44. Curnow, A. W., Hong, K., Yuan, R., Kim, S., Martins, O., Winkler, W., Henkin, T. M., and Soll, D. (1997) Glu-tRNAGln amidotransferase: A novel heterotrimeric enzyme required for correct decoding of glutamine codons during translation Proc. Natl. Acad. Sci. U.S.A. 94, 11819-11826
45. Schon, A., Kannangara, C. G., Gough, S., and Soll, D. (1988) Protein biosynthesis in organelles requires misaminoacylation of tRNA Nature 331, 187-190
46. Bracey, M. H., Hanson, M. A., Mesuda, K. R., Stevens, R. C., and Cravatt, B. F. (2002) Structural adaptations in a membrane enzyme that terminates endocannabinoid signaling Science 298, 1793-1796
47. Labahn, J., Neumann, S., Buldt, G., Kula, M. R., and Granzin, J. (2002) An alternative mechanism for amidase signature enzymes J. Mol. Biol. 322, 1053-1064
48. Nakamura, A., Yao, M., Chimnaronk, S., Sakai, N., and Tanaka, I. (2006) Ammonia channel couples glutaminase with transamidase reactions in GatCAB Science 312, 1954-1958
49. PDB ID: 2GI3; coordinates deposited by the Joint Center For Structural Genomics, 2006.
50. Yasuhira, K., Shibata, N., Mongami, G., Vedo, Y., Atsumi, Y., Kawashimi, Y., Hibino, A., Tanaka, Y., Lee, Y.-H., Kato, D., Takeo, M., Higuchi, Y., and Negoro, S. (2010) X-ray crystallographic analysis of the 6-aminohexanoate cyclic dimer hydrolase J. Biol. Chem. 285, 1239-1248
51. Shin, S., Yun, Y. S., Koo, H. M., Kim, Y. S., Choi, K. Y., and Oh, B.-H. (2003) Characterization of a novel Ser-cisSer-Lys catalytic triad in comparison with the classical Ser-His-Asp triad J. Biol. Chem. 278, 24937-24943
52. McKinney, M. K. and Cravatt, B. F. (2003) Evidence for distinct roles in catalysis for residues of the serine-serine-lysine catalytic triad of fatty acid amide hydrolase J. Biol. Chem. 278, 37393-37399
53. Valina, A. L. B., Mazumder-Shivakumar, D., and Bruice, T. C. (2004) Probing the Ser-Ser-Lys catalytic triad mechanism of peptide amidase: Computational studies of the ground state, transition state and intermediate Biochemistry 43, 15657-15672
54. Tubert-Brohman, I., Acevedo, O., and Jorgenson, W. L. (2006) Elucidation of hydrolysis mechanisms for fatty acid amide hydrolase and its Lys 142 Ala variant via QM/MM simulations J. Am. Chem. Soc. 128, 16904-16913
55. Lodola, A., Mor, M., Sirivak, J., and Mulholland, A. J. (2009) Insights into the mechanism and inhibition of fatty acid amide hydrolase from quantum mechanics/molecular mechanics (QM/MM) modelling Biochem. Soc. Trans. 37, 363-367
56. Sauvage, E., Powell, A. J., Heilemann, J., Charlier, P., Davies, C., and Pratt, R. F. (2008) Crystal structures of complexes of bacterial dd -peptidases with peptidoglycan-mimetic ligands: The substrate specificity puzzle J. Mol. Biol. 381, 383-393
57. Navratna, V., Nadig, S., Sood, V., Prasad, K., Arakere, G., and Gopal, B. (2010) Molecular basis for the role of Staphylococcus aureus penicillin-binding protein 4 in antimicrobial resistance J. Bacteriol. 192, 134-144
58. Lim, D. and Strynadka, N. C. J. (2002) Structural basis for the β-lactam resistance of PBP2a from methicillin-resistant Staphylococcus aureus Nat. Struct. Biol. 9, 870-876
59. Tulinsky, A. and Blevins, R. A. (1987) Structure of a tetrahedral transition state complex of α-chymotrypsin dimer at 1.8 Å resolution J. Biol. Chem. 262, 7737-7743
60. Jeffrey, G. A. and Saenger, W. (1991) in Hydrogen bonding in biological structures, Chapter 12, Springer-Verlag, Berlin.
61. Kortemme, T., Morozov, A. V., and Baker, D. (2003) An orientation-dependent hydrogen bonding potential improves prediction of specificity and structure for proteins and protein-protein complexes J. Mol. Biol. 326, 1239-1259
62. Paetzel, M., Dalbey, R. E., and Strynadka, N. C. J. (2002) Crystal structure of a bacterial signal peptidase apoenzyme. Implications for signal peptide binding and the SerLys dyad mechanism J. Biol. Chem. 277, 9512-9519
63. Kobayashi, M., Fujiwara, Y., Goda, M., Komeda, H., and Shimizu, S. (1997) Identification of active sites in amidase: Evolutionary relationship between amide bond- and peptide bond-cleaving enzymes Proc. Natl. Acad. Sci. U.S.A. 94, 11986-11991