Autoproteolytic activation of ThnT results in structural reorganization necessary for substrate binding and catalysis

Journal of Molecular Biology

Volumn 422, Issue 4, 2012, Pages 508-518

  Buller, Andrew R ^a   Labonte, Jason W ^b,c   Freeman, Michael F ^b,d   Wright, Nathan T ^b,e   Schildbach, Joel F ^b   Townsend, Craig A ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c Johns Hopkins University   (United States)

^d UNIVERSITY OF BONN   (Germany)

^e JAMES MADISON UNIVERSITY   (United States)

Author keywords

cis autoproteolysis; mechanism of chloromethyl ketone inhibition; N terminal nucleophile; thienamycin biosynthesis; X ray crystallography

Indexed keywords

ENZYME PRECURSOR; ETHER; HYDROLASE; KETONE DERIVATIVE; NUCLEOPHILE; PANTETHEINE; PROTEIN THNT; UNCLASSIFIED DRUG;

ARTICLE; BIOCATALYSIS; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; MOLECULAR EVOLUTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; REACTION ANALYSIS; X RAY CRYSTALLOGRAPHY;

EID: 84865507762     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.06.012     Document Type: Article

References (47)

1. B. Macao, D.G.A. Johansson, G.C. Hansson, and T. Hard Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin Nat. Struct. Mol. Biol. 13 2006 71 76 (Pubitemid 43049405)
2. H.H. Lin, G.W. Chang, J.Q. Davies, M. Stacey, J. Harris, and S. Gordon Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif J. Biol. Chem. 279 2004 31823 31832 (Pubitemid 39037855)
3. J.S. Rosenblum, and G. Blobel Autoproteolysis in nucleoporin biogenesis Proc. Natl Acad. Sci. USA 96 1999 11370 11375 (Pubitemid 29487387)
4. A. Tinel, S. Janssens, S. Lippens, S. Cuenin, E. Logette, and B. Jaccard Autoproteolysis of PIDD marks the bifurcation between pro-death caspase-2 and pro-survival NF-κB pathway EMBO J. 26 2007 197 208 (Pubitemid 46094711)
5. 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
6. F.B. Perler, M.Q. Xu, and H. Paulus Protein splicing and autoproteolysis mechanisms Curr. Opin. Chem. Biol. 1 1997 292 299 (Pubitemid 127437154)
7. 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 (Pubitemid 29418956)
8. C.D. Guan, T. Cui, V. Rao, W. Liao, J. Benner, C.L. Lin, and D. Comb Activation of glycosylasparaginase. Formation of active N-terminal threonine by intramolecular autoproteolysis J. Biol. Chem. 271 1996 1732 1737
9. E. Seemuller, A. Lupas, D. Stock, J. Lowe, R. Huber, and W. Baumeister Proteasome from Thermoplasma acidophilum: a threonine protease Science 268 1995 579 582
10. C. Bompard-Gilles, V. Villeret, G.J. Davies, L. Fanuel, B. Joris, J.M. Frere, 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 (Pubitemid 30097361)
11. H. Cheng, and N.V. Grishin DOM-fold: a structure with crossing loops found in DmpA, ornithine acetyltransferase, and molybdenum cofactor-binding domain Protein Sci. 14 2005 1902 1910 (Pubitemid 40994161)
12. M.F. Freeman, K.A. McIshos, M.J. Bodner, R.F. Li, and C.A. Townsend Four enzymes define the incorporation of coenzyme A in thienamycin biosynthesis Proc. Natl Acad. Sci. USA 105 2008 11128 11133
13. 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
14. Y.M. Wang, and H.C. Guo Crystallographic snapshot of glycosylasparaginase precursor poised for autoprocessing J. Mol. Biol. 403 2010 120 130
15. Y.M. Wang, and H.C. Guo Crystallographic snapshot of a productive glycosylasparaginase-substrate complex J. Mol. Biol. 366 2007 82 92
16. L. Ditzel, R. Huber, K. Mann, W. Heinemeyer, D.H. Wolf, and M. Groll Conformational constraints for protein self-cleavage in the proteasome J. Mol. Biol. 279 1998 1187 1191 (Pubitemid 28302394)
17. G. Volpato, R.C. Rodrigues, and R. Fernandez-Lafuente Use of enzymes in the production of semi-synthetic penicillins and cephalosporins: drawbacks and perspectives Curr. Med. Chem. 17 2010 3855 3873
18. C.F. Sio, and W.J. Quax Improved β-lactam acylases and their use as industrial biocatalysts Curr. Opin. Biotechnol. 15 2004 349 355 (Pubitemid 39028914)
19. C. Oinonen, and J. Rouvinen Structural comparison of Ntn-hydrolases Protein Sci. 9 2000 2329 2337 (Pubitemid 32105715)
20. 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 (Pubitemid 47086261)
21. J.D. Dunitz The entropic cost of bound water in crystals and biomolecules Science 264 1994 670 (Pubitemid 24186849)
22. 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 center Nature 373 1995 264 268
23. D. Zhiryakova, I. Ivanov, S. Ilieva, M. Guncheva, B. Galunsky, and N. Stambolieva Do N-terminal nucleophile hydrolases indeed have a single amino acid catalytic center? FEBS J. 276 2009 2589 2598
24. C.S. Bond TopDraw: a sketchpad for protein structure topology cartoons Bioinformatics 19 2003 311 312 (Pubitemid 36181928)
25. M.E. Jung, and J. Gervay gem-Dialkyl effect in the intramolecular Diels-Alder reaction of 2-furfuryl methyl fumarates: the reactive rotamer effect, enthalpic basis for acceleration, and evidence for a polar transition state J. Am. Chem. Soc. 113 1991 224 232
26. A. Lqbal, I.J. Clifton, M. Bagonis, N.J. Kershaw, C. Domene, and T.D.W. Claridge Anatomy of a simple acyl intermediate in enzyme catalysis: combined biophysical and modeling studies on ornithine acetyl transferase J. Am. Chem. Soc. 131 2009 749 757
27. J. Yin, Z. Deng, G. Zhao, and X. Huang The N-terminal nucleophile serine of cephalosporin acylase executes the second autoproteolytic cleavage and acylpeptide hydrolysis J. Biol. Chem. 286 2011 24476 24486
28. J.C. Powers, J.L. Asgian, O.D. Ekici, and K.E. James Irreversible inhibitors of serine, cysteine, and threonine proteases Chem. Rev. 102 2002 4639 4750
29. J. Yin, M.M. Cherney, E.M. Bergmann, J. Zhang, C. Huitema, and H. Pettersson An episulfide cation (thiiranium ring) trapped in the active site of HAV 3C proteinase inactivated by peptide-based ketone inhibitors J. Mol. Biol. 361 2006 673 686 (Pubitemid 44175381)
30. P.J. Savory, H. Djaballah, H. Angliker, E. Shaw, and A.J. Rivett Reaction of proteasomes with peptidylchloromethanes and peptidyldiazomethanes Biochem. J. 296 1993 601 605 (Pubitemid 24008174)
31. M. Prorok, A. Albeck, B.M. Foxman, and R.H. Abeles Chloroketone hydrolysis by chymotrypsin and N-methylhistidyl-57-chymotrypsin: implications for the mechanism of chymotrypsin inactivation by chloroketones Biochemistry 33 1994 9784 9790 (Pubitemid 24272940)
32. J. Drenth, K.H. Kalk, and H.M. Swen Binding of chloromethyl ketone substrate analogs to crystalline papain Biochemistry 15 1976 3731 3738
33. pro) structure: basis for design of anti-SARS drugs Science 300 2003 1763 1767 (Pubitemid 36712575)
34. J.A. Yin, C.G. Niu, M.M. Cherney, J.M. Zhang, C. Huitema, and L.D. Eltis A mechanistic view of enzyme inhibition and peptide hydrolysis in the active site of the SARS-CoV 3C-like peptidase J. Mol. Biol. 371 2007 1060 1074 (Pubitemid 47101817)
35. N2 reactions J. Am. Chem. Soc. 86 1964 4645
36. M.J. Bodner, R.M. Phelan, M.F. Freeman, R. Li, and C.A. Townsend Non-heme iron oxygenases generate natural structural diversity in carbapenem antibiotics J. Am. Chem. Soc. 132 2010 12- +
37. M.J. Bodner, R.F. Li, R.M. Phelan, M.F. Freeman, K.A. Moshos, E.P. Lloyd, and C.A. Townsend Definition of the common and divergent steps in carbapenem β-lactam antibiotic biosynthesis ChemBioChem 12 2011 2159 2165
38. L. Fanuel, C. Goffin, A. Cheggour, B. Devreese, G. Van Driessche, and B. Joris The DmpA aminopeptidase from Ochrobactrum anthropi LMG7991 is the prototype of a new terminal nucleophile hydrolase family Biochem. J. 341 1999 147 155 (Pubitemid 29359059)
39. P. Syrén, and K. Hult Amidases have a hydrogen bond that facilitates nitrogen inversion, but esterases have not ChemCatChem 3 2011 853 860
40. M. Bokhove, H. Yoshida, C.M.H. Hensgens, J.M. van der Laan, J.D. Sutherland, and B.W. Dijkstra Structures of an isopenicillin N converting Ntn-hydrolase reveal different catalytic roles for the active site residues of precursor and mature enzyme Structure 18 2010 301 308
41. Y. Kim, S. Kim, T.N. Earnest, and W.G.J. Hol Precursor structure of cephalosporin acylase: insights into autoproteolytic activation in a new N-terminal hydrolase family J. Biol. Chem. 277 2002 2823 2829 (Pubitemid 34953314)
42. 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. Crystallogr. 40 2007 658 674 (Pubitemid 47080256)
43. S. Bailey The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763
44. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
45. M.D. Winn, G.N. Murshudov, and M.Z. Papiz Macromolecular TLS refinement in REFMAC at moderate resolutions Methods Enzymol. 374 2003 300 321 (Pubitemid 37531815)
46. J. Painter, and E.A. Merritt TLSMD web server for the generation of multi-group TLS models J. Appl. Crystallogr. 39 2006 109 111
47. B.R. Brooks, R.E. Bruccoleri, B.D. Olafson, D.J. States, S. Swaminathan, and M. Karplus CHARMM: a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217