Crystallographic snapshots of the complete catalytic cycle of the unregulated aspartate transcarbamoylase from Bacillus subtilis

Journal of Molecular Biology

Volumn 411, Issue 1, 2011, Pages 190-200

  Harris, Katharine M ^a   Cockrell, Gregory M ^a   Puleo, David E ^a   Kantrowitz, Evan R ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

catalytic cycle; pyrimidine nucleotide biosynthesis; transferase enzymes; X ray crystallography

Indexed keywords

ASPARTATE CARBAMOYLTRANSFERASE; ASPARTIC ACID; CARBAMOYL PHOSPHATE; PYRIMIDINE NUCLEOTIDE; SPARFOSIC ACID;

ARTICLE; BACILLUS SUBTILIS; BIOSYNTHESIS; CATALYSIS; COMPUTER MODEL; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; ENZYME STRUCTURE; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

BACILLUS SUBTILIS;

EID: 79960697550     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.05.036     Document Type: Article

References (42)

1. Gerhart J.C., and Pardee A.B. Enzymology of control by feedback inhibition J. Biol. Chem. 237 1962 891 896
2. Wedler F.C., and Gasser F.J. Ordered substrate binding and evidence for a thermally induced change in mechanism for E. coli aspartate transcarbamylase Arch. Biochem. Biophys. 163 1974 57 68
3. Krause K.L., Voltz K.W., and Lipscomb W.N. Structure at 2.9-Å resolution of aspartate carbamoyltransferase complexed with the bisubstrate analogue N-(phosphonacetyl)-l-aspartate Proc. Natl Acad. Sci. USA 82 1985 1643 1647 (Pubitemid 15079449)
4. Robey E.A., and Schachman H.K. Regeneration of active enzyme by formation of hybrids from inactive derivatives: implications for active sites shared between polypeptide chains of aspartate transcarbamoylase Proc. Natl Acad. Sci. USA 82 1985 361 365 (Pubitemid 15128268)
5. Jencks W.P. Catalysis in Chemistry and Enzymology 1969 McGraw-Hill New York, NY
6. Hervé G., Nagy M., Le Gouar M., Penverne B., and Ladjimi M. The carbamoyl phosphate synthetase-aspartate transcarbamoylase complex of Saccharomyces cerevisiae: molecular and cellular aspects Biochem. Soc. Trans. 21 1993 195 198 (Pubitemid 23092469)
7. Grayson D.R., and Evans D.R. The isolation and characterization of the aspartate transcarbamylase domain of the multifunctional protein, CAD J. Biol. Chem. 258 1983 4123 4129
8. Lipscomb W.N. Aspartate transcarbamoylase from Escherichia coli: activity and regulation Adv. Enzymol. 68 1994 67 151 (Pubitemid 2050643)
9. Beernink P.T., Endrizzi J.A., Alber T., and Schachman H.K. Assessment of the allosteric mechanism of aspartate transcarbamoylase based on the crystalline structure of the unregulated catalytic subunit Proc. Natl Acad. Sci. USA 96 1999 5388 5393 (Pubitemid 29234627)
10. Endrizzi J.A., Beernink P.T., Alber T., and Schachman H.K. Binding of bisubstrate analog promotes large structural changes in the unregulated catalytic trimer of aspartate transcarbamoylase: implications for allosteric regulation Proc. Natl Acad. Sci. USA 97 2000 5077 5082 (Pubitemid 30313674)
11. Wang J., Stieglitz K.A., Cardia J.P., and Kantrowitz E.R. Structural basis for ordered substrate binding and cooperativity in aspartate transcarbamoylase Proc. Natl Acad. Sci. USA 102 2005 8881 8886 (Pubitemid 40881047)
12. Ke H.M., Honzatko R.B., and Lipscomb W.N. Structure of unligated aspartate carbamoyltransferase of Escherichia coli at 2.6-Å resolution Proc. Natl Acad. Sci. USA 81 1984 4027 4040
13. Stevens R.C., Reinisch K.M., and Lipscomb W.N. Molecular structure of Bacillus subtilis aspartate transcarbamoylase at 3.0 Å resolution Proc. Natl Acad. Sci. USA 88 1991 6087 6091 (Pubitemid 21914891)
14. Stevens R.C., Chook Y.M., Cho C.Y., Lipscomb W.N., and Kantrowitz E.R. Escherichia coli aspartate carbamoyltransferase: the probing of crystal structure analysis via site-specific mutagenesis Protein Eng. 4 1991 391 408
15. Jin L., Stec B., Lipscomb W.N., and Kantrowitz E.R. Insights into the mechanism of catalysis and heterotropic regulation of E. coli aspartate transcarbamoylase based upon a structure of enzyme complexed with the bisubstrate analog N-phosphonacetyl-l-aspartate at 2.1 Å Proteins 37 1999 729 742
16. Dundas J., Ouyang Z., Tseng J., Binkowski A., Turpaz Y., and Liang J. CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues Nucleic Acids Res. 34 2006 W116 W118
17. Gilson M., and Honig B. Calculations of electrostatic potentials in an enzyme active site Nature 330 1987 84 86 (Pubitemid 17152422)
18. Friesner R.A., Banks J.L., Murphy R.B., Halgren T.A., Klicic J.J., and Mainz D.T. Glide: a new approach for rapid, accurate docking and scoring: 1. Method and assessment of docking accuracy J. Med. Chem. 47 2004 1739 1749 (Pubitemid 38380917)
19. Halgren T.A., Murphy R.B., Friesner R.A., Beard H.S., Frye L.L., Pollard W.T., and Banks J.L. Glide: a new approach for rapid, accurate docking and scoring: 2. Enrichment factors in database screening J. Med. Chem. 47 2004 1750 1759 (Pubitemid 38380918)
20. Friesner R.A., Murphy R.B., Repasky M.P., Frye L.L., Greenwood J.R., and Halgren T.A. Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes J. Med. Chem. 49 2006 6177 6196 (Pubitemid 44595196)
21. Baker D.P., Aucoin J.M., Williams M.K., DeMello L.A., and Kantrowitz E.R. Overexpression and purification of the trimeric aspartate transcarbamoylase from Bacillus subtilis Protein Expression Purif. 6 1995 679 684
22. a values Proteins 61 2005 704 721 (Pubitemid 41753142)
23. a values for protein-ligand complexes Proteins 73 2008 765 783 (Pubitemid 352788657)
24. Tsuruta H., Sano T., Vachette P., Tauc P., Moody M.F., and Wakabayashi K. Structural kinetics of the allosteric transition of aspartate transcarbamoylase produced by physiological substrates FEBS Lett. 263 1990 66 68 (Pubitemid 20107780)
25. Collins K.D., and Stark G.R. Aspartate transcarbamylase: interaction with the transition state analogue N-(phosphonacetyl)-l-aspartate J. Biol. Chem. 246 1971 6599 6605
26. Gouaux J.E., Krause K.L., and Lipscomb W.N. The catalytic mechanism of Escherichia coli aspartate carbamoyltransferase: a molecular modeling study Biochem. Biophys. Res. Commun. 142 1987 893 897 (Pubitemid 17021116)
27. Stebbins J.W., and Kantrowitz E.R. Conversion of the non-cooperative Bacillus subtilis aspartate transcarbamoylase into a cooperative enzyme by a single amino acid substitution Biochemistry 31 1992 2328 2332
28. Koshland D.E., Nemethy G., and Filmer D. Comparison of experimental binding data and theoretical models in proteins containing subunits Biochemistry 5 1966 365 385
29. Monod J., Wyman J., and Changeux J.P. On the nature of allosteric transitions: a plausible model J. Mol. Biol. 12 1965 88 118
30. Hervé G., Moody M.F., Tauc P., Vachette P., and Jones P.T. Quaternary structure changes in aspartate transcarbamylase studied by X-ray solution scattering. Signal transmission following effector binding J. Mol. Biol. 185 1985 189 199 (Pubitemid 16250052)
31. Chan R.S., Sakash J.B., Macol C.P., West J.M., Tsuruta H., and Kantrowitz E.R. The role of intersubunit interactions for the stabilization of the T state of Escherichia coli aspartate transcarbamoylase J. Biol. Chem. 277 2002 49755 49760 (Pubitemid 36014421)
32. Sakash J.B., Chan R.S., Tsuruta H., and Kantrowitz E.R. Three of the six possible intersubunit stabilizing interactions involving Glu239 are sufficient for restoration of the homotropic and heterotropic properties of Escherichia coli aspartate transcarbamoylase J. Biol. Chem. 275 2000 752 758 (Pubitemid 30051112)
33. Nowlan S.F., and Kantrowitz E.R. Superproduction and rapid purification of E. coli aspartate transcarbamoylase and its catalytic subunit under extreme derepression of the pyrimidine pathway J. Biol. Chem. 260 1985 14712 14716 (Pubitemid 16211004)
34. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
35. Brabson J.S., and Switzer R.L. Purification and properties of Bacillus subtilis aspartate transcarbamoylase J. Biol. Chem. 250 1975 8664 8669
36. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode C.W. Carter Jr. R.M. Sweet, Methods in Enzymology 276 1997 Academic Press New York, NY 307 326 (Pubitemid 27085611)
37. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., and Echols N. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 213 221
38. Long F., Vagin A.A., Young P., and Murshudov G.N. BALBES: a molecular-replacement pipeline Acta Crystallogr., Sect. D: Biol. Crystallogr. 64 2008 125 132 (Pubitemid 350308686)
39. Emsley P., Lohkamp B., Scott W.G., and Cowtan K. Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 486 501
40. Chen V.B., Arendall W.B. III, Headd J.J., Keedy D.A., Immormino R.M., and Kapral G.J. MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 12 21
41. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., and Wang X. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35 2007 W375 W383
42. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291