Autoproteolytic and catalytic mechanisms for the β-aminopeptidase BapA - A member of the Ntn hydrolase family

Structure

Volumn 20, Issue 11, 2012, Pages 1850-1860

  Merz, Tobias ^a   Heck, Tobias ^b   Geueke, Birgit ^b   Mittl, Peer R E ^a   Briand, Christophe ^a   Seebach, Dieter ^c   Kohler, Hans Peter E ^b   Grütter, Markus G ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^c ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPEPTIDASE B; ASPARAGINE; B AMINOPEPTIDASE BAPA; GLUTAMIC ACID; LYSINE; PROLINE; SERINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CATALYSIS; CHEMICAL BOND; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; MUTATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STRUCTURE;

AMIDOHYDROLASES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; GLUTAMYL AMINOPEPTIDASE; MODELS, MOLECULAR; PROTEOLYSIS;

SPHINGOSINICELLA;

EID: 84868552501     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.07.017     Document Type: Article

References (44)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.-W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. M.-I. Aguilar, A.W. Purcell, R. Devi, R. Lew, J. Rossjohn, A.I. Smith, and P. Perlmutter β-amino acid-containing hybrid peptides - new opportunities in peptidomimetics Org. Biomol. Chem. 5 2007 2884 2890
3. T.R.M. Barends, H. Yoshida, and B.W. Dijkstra Three-dimensional structures of enzymes useful for β-lactam antibiotic production Curr. Opin. Biotechnol. 15 2004 356 363
4. W. Baumeister, and A. Lupas The proteasome Curr. Opin. Struct. Biol. 7 1997 273 278
5. G. Boanca, A. Sand, and J.J. Barycki Uncoupling the enzymatic and autoprocessing activities of Helicobacter pylori γ-glutamyltranspeptidase J. Biol. Chem. 281 2006 19029 19037
6. G. Boanca, A. Sand, T. Okada, H. Suzuki, H. Kumagai, K. Fukuyama, and J.J. Barycki Autoprocessing of Helicobacter pylori γ- glutamyltranspeptidase leads to the formation of a threonine-threonine catalytic dyad J. Biol. Chem. 282 2007 534 541
7. C. Bompard-Gilles, V. Villeret, G.J. Davies, L. Fanuel, B. Joris, J.-M. Frère, and J. Van Beeumen A new variant of the Ntn hydrolase fold revealed by the crystal structure of L-aminopeptidase D-ala-esterase/amidase from Ochrobactrum anthropi Structure 8 2000 153 162
8. J.A. Brannigan, G. Dodson, H.J. Duggleby, P.C.E. Moody, J.L. Smith, D.R. Tomchick, and A.G. Murzin A protein catalytic framework with an N-terminal nucleophile is capable of self-activation Nature 378 1995 416 419
9. A. Bruggink, E.C. Roos, and E. Vroom de Penicillin acylase in the industrial production of β-lactam antibiotics Org. Process Res. Dev. 2 1998 128 133
10. A.R. Buller, M.F. Freeman, N.T. Wright, J.F. Schildbach, and C.A. Townsend Insights into cis-autoproteolysis reveal a reactive state formed through conformational rearrangement Proc. Natl. Acad. Sci. USA 109 2012 2308 2313
11. W.L. DeLano The Pymol Molecular Graphics System 2002 DeLano Scientific San Carlos, CA, USA
12. H.J. Duggleby, S.P. Tolley, C.P. Hill, E.J. Dodson, G. Dodson, and P.C.E. Moody Penicillin acylase has a single-amino-acid catalytic centre Nature 373 1995 264 268
13. J.M. Elkins, N.J. Kershaw, and C.J. Schofield X-ray crystal structure of ornithine acetyltransferase from the clavulanic acid biosynthesis gene cluster Biochem. J. 385 2005 565 573
14. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
15. L. Fanuel, C. Goffin, A. Cheggour, B. Devreese, G. Van Driessche, B. Joris, J. Van Beeumen, and J.M. Frère The DmpA aminopeptidase from Ochrobactrum anthropi LMG7991 is the prototype of a new terminal nucleophile hydrolase family Biochem. J. 341 1999 147 155
16. L. Fanuel, I. Thamm, V. Kostanjevecki, B. Samyn, B. Joris, C. Goffin, J. Brannigan, J. Van Beeumen, and J.M. Frère Two new aminopeptidases from Ochrobactrum anthropi active on D-alanyl-p-nitroanilide Cell. Mol. Life Sci. 55 1999 812 818
17. J. Frackenpohl, P.I. Arvidsson, J.V. Schreiber, and D. Seebach The outstanding biological stability of β- and γ-peptides toward proteolytic enzymes: an in vitro investigation with fifteen peptidases ChemBioChem 2 2001 445 455
18. V. Fuchs, K.-E. Jaeger, S. Wilhelm, and F. Rosenau The BapF protein from Pseudomonas aeruginosa is a β-peptidyl aminopeptidase World J. Microbiol. Biotechnol. 27 2011 713 718
19. B. Geueke, and H.-P.E. Kohler Bacterial β-peptidyl aminopeptidases: on the hydrolytic degradation of β-peptides Appl. Microbiol. Biotechnol. 74 2007 1197 1204
20. B. Geueke, K. Namoto, D. Seebach, and H.-P.E. Kohler A novel β-peptidyl aminopeptidase (BapA) from strain 3-2W4 cleaves peptide bonds of synthetic β-tri- and β-dipeptides J. Bacteriol. 187 2005 5910 5917
21. B. Geueke, T. Heck, M. Limbach, V. Nesatyy, D. Seebach, and H.-P.E. Kohler Bacterial β-peptidyl aminopeptidases with unique substrate specificities for β-oligopeptides and mixed β,α-oligopeptides FEBS J. 273 2006 5261 5272
22. T. Heck, M. Limbach, B. Geueke, M. Zacharias, J. Gardiner, H.-P.E. Kohler, and D. Seebach Enzymatic degradation of β- and mixed α,β-oligopeptides Chem. Biodivers. 3 2006 1325 1348
23. T. Heck, H.-P.E. Kohler, M. Limbach, O. Flögel, D. Seebach, and B. Geueke Enzyme-catalyzed formation of β-peptides: β-peptidyl aminopeptidases BapA and DmpA acting as β-peptide-synthesizing enzymes Chem. Biodivers. 4 2007 2016 2030
24. T. Heck, D. Seebach, S. Osswald, M.K.J. Wielter, H.-P.E. Kohler, and B. Geueke Kinetic resolution of aliphatic β-amino acid amides by β-aminopeptidases ChemBioChem 10 2009 1558 1561
25. 2-dipeptides: kinetic resolution and enzymatic coupling ChemBioChem 11 2010 1129 1136
26. T. Heck, T. Merz, A. Reimer, D. Seebach, D. Rentsch, C. Briand, M.G. Grütter, H.-P.E. Kohler, and B. Geueke Crystal structures of BapA complexes with β-lactam-derived inhibitors illustrate substrate specificity and enantioselectivity of β-aminopeptidases ChemBioChem 2012 10.1002/cbic.201200393 Published online September 22, 2012
27. D.G. Johansson, G. Wallin, A. Sandberg, B. Macao, J. Aqvist, and T. Härd Protein autoproteolysis: conformational strain linked to the rate of peptide cleavage by the pH dependence of the N - > O acyl shift reaction J. Am. Chem. Soc. 131 2009 9475 9477
28. W. Kabsch Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Cryst. 26 1993 795 800
29. J.K. Kim, I.S. Yang, S. Rhee, Z. Dauter, Y.S. Lee, S.S. Park, and K.H. Kim Crystal structures of glutaryl 7-aminocephalosporanic acid acylase: insight into autoproteolytic activation Biochemistry 42 2003 4084 4093
30. J.K. Kim, I.S. Yang, H.J. Shin, K.J. Cho, E.K. Ryu, S.H. Kim, S.S. Park, and K.H. Kim Insight into autoproteolytic activation from the structure of cephalosporin acylase: a protein with two proteolytic chemistries Proc. Natl. Acad. Sci. USA 103 2006 1732 1737
31. H. Komeda, and Y. Asano A DmpA-homologous protein from Pseudomonas sp. is a dipeptidase specific for β-alanyl dipeptides FEBS J. 272 2005 3075 3084
32. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D Biol. Crystallogr. 60 2004 2256 2268
33. J. Löwe, D. Stock, B. Jap, P. Zwickl, W. Baumeister, and R. Huber Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution Science 268 1995 533 539
34. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674
35. C.E. McVey, M.A. Walsh, G.G. Dodson, K.S. Wilson, and J.A. Brannigan Crystal structures of penicillin acylase enzyme-substrate complexes: structural insights into the catalytic mechanism J. Mol. Biol. 313 2001 139 150
36. K. Michalska, A. Hernandez-Santoyo, and M. Jaskolski The mechanism of autocatalytic activation of plant-type L-asparaginases J. Biol. Chem. 283 2008 13388 13397
37. C. Oinonen, and J. Rouvinen Structural comparison of Ntn-hydrolases Protein Sci. 9 2000 2329 2337
38. J. Saarela, C. Oinonen, A. Jalanko, J. Rouvinen, and L. Peltonen Autoproteolytic activation of human aspartylglucosaminidase Biochem. J. 378 2004 363 371
39. D. Seebach, and J. Gardiner β-peptidic peptidomimetics Acc. Chem. Res. 41 2008 1366 1375
40. C.G. Suresh, A.V. Pundle, H. SivaRaman, K.N. Rao, J.A. Brannigan, C.E. McVey, C.S. Verma, Z. Dauter, E.J. Dodson, and G.G. Dodson Penicillin V acylase crystal structure reveals new Ntn-hydrolase family members Nat. Struct. Biol. 6 1999 414 416
41. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22 1994 4673 4680
42. R. Tikkanen, A. Riikonen, C. Oinonen, R. Rouvinen, and L. Peltonen Functional analyses of active site residues of human lysosomal aspartylglucosaminidase: implications for catalytic mechanism and autocatalytic activation EMBO J. 15 1996 2954 2960
43. 14C-labeled β-nonapeptide in rats - in vitro and in vivo pharmacokinetic studies Biopharm. Drug Dispos. 23 2002 251 262
44. Q.A. Xu, D. Buckley, C.D. Guan, and H.C. Guo Structural insights into the mechanism of intramolecular proteolysis Cell 98 1999 651 661