A single mutation in the active site swaps the substrate specificity of N-acetyl-L-ornithine transcarbamylase and N-succinyl-L-ornithine transcarbamylase

Protein Science

Volumn 16, Issue 8, 2007, Pages 1689-1699

  Shi, Dashuang ^a,c   Yu, Xiaolin ^a   Cabrera Luque, Juan ^a   Chen, Tony Y ^b   Roth, Lauren ^b   Morizono, Hiroki ^a   Allewell, Norma M ^b   Tuchman, Mendel ^a  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c CHILDREN S RESEARCH INSTITUTE   (United States)

Author keywords

argF gene; Arginine biosynthesis; Crystal structure; N acetylornithine; N succinylornithine; Protein engineering; Transcarbamylase

Indexed keywords

ARGININE; ASPARAGINE; CARBAMOYLTRANSFERASE; GLUTAMINE; LYSINE; MUTANT PROTEIN; N ACETYL NORVALINE; N ACETYL ORNITHINE TRANSCARBAMYLASE; N SUCCINYL ORNITHINE TRANSCARBAMYLASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL MUTATION; BACTEROIDES FRAGILIS; CARBAMOYLATION; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BINDING; ENZYME SPECIFICITY; GENE MUTATION; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY; XANTHOMONAS CAMPESTRIS;

AMINO ACID SEQUENCE; ARGININE; BACTEROIDES FRAGILIS; BINDING SITES; CARBOXYL AND CARBAMOYL TRANSFERASES; CRYSTALLOGRAPHY, X-RAY; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POINT MUTATION; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY; XANTHOMONAS CAMPESTRIS;

BACTEROIDES FRAGILIS; XANTHOMONAS CAMPESTRIS;

EID: 34547611288     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.072919907     Document Type: Article

References (35)

1. Allewell, N.M., Shi, D., Morizono, H., and Tuchman, M. 1999. Molecular recognition by ornithine and aspartate transcarbamoylases. Acc. Chem. Res. 32: 885-894.
2. Born, T.L. and Blanchard, J.S. 1999. Structure/function studies on enzymes in the diaminopimelate pathway of bacterial cell wall biosynthesis. Curr. Opin. Chem. Biol. 3: 607-613.
3. Bradford, M. 1976. Quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 1219-1223.
4. Brown, C.J., Takayama, S., Campen, A.M., Vise, P., Marshall, T.W., Oldfield, C.J., Williams, C.J., and Dunker, A.K. 2002. Evolutionary rate heterogeneity in proteins with long disordered regions. J. Mol. Evol. 55: 104-110.
5. Brünger, A.T. 1992. Free R value: A novel statistical quantity for assessing the accuracy of crystal structures. Nature 355: 472-475.
6. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Crosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D54: 905-921.
7. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D50: 760-763.
8. Cunin, R., Glansdorff, N., Pierard, A., and Stalon, V. 1986. Biosynthesis and metabolism of arginine in bacteria. Microbiol. Rev. 50: 314-352.
9. Davis, R.H. 1986. Compartmental and regulatory mechanisms in arginine pathways of Neurospora crassa and Saccharomyces cerevisiae. Microbiol. Rev. 50: 280-313.
10. DeLano, W.L. 2002. The PyMOL molecular graphics system. http://www.pymol.org.
11. Gouaux, J.E. and Lipscomb, W.N. 1988. Three-dimensional structure of carbamoyl phosphate and succinate bound to aspartate carbamoyltransferase. Proc. Natl. Acad. Sci. 85: 4205-4208.
12. Ha, Y., McCann, M.T., Tuchman, M., and Allewell, N.M. 1997. Substrate-induced conformational change in a trimeric ornithine transcarbamylase. Proc. Natl. Acad. Sci. 94: 9550-9555.
13. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and location of errors in these model. Acta Crystallogr. A47: 110-119.
14. Ke, H.M., Lipscomb, W.N., Cho, Y.J., and Honzatko, R.B. 1988. Complex of N-phosphonacetyl-L-aspartate with aspartate carbamoyltransferase. X-ray refinement, analysis of conformational changes and catalytic and allosteric mechanisms. J. Mol. Biol. 204: 725-747.
15. Khatib, F., Weirauch, M.T., and Rohl, C.A. 2006. Rapid knot detection and application to protein structure prediction. Bioinformatics 22: e252-e259. doi: 10.1093/bioinformatics/btl236.
16. Kraulis, P.J. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946-950.
17. Krause, K.L., Volz, K.W., and Lipscomb, W.N. 1987. 2.5 Å structure of aspartate carbamoyltransferase complexed with the bisubstrate analog N-(phosphonacetyl)-L-aspartate. J. Mol. Biol. 193: 527-553.
18. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
19. Merritt, E.A. and Murphy, M.E. 1994. Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. D50: 869-873.
20. Morizono, H., Tuchman, M., Rajagopal, B.S., McCann, M.T., Listrom, C.D., Yuan, X., Venugopal, D., Barany, G., and Allewell, N.M. 1997. Expression, purification and kinetic characterization of wild-type human ornithine transcarbamylase and a recurrent mutant that produces "late onset" hyperammonaemia. Biochem. J. 322: 625-631.
21. Morizono, H., Cabrera-Luque, J., Shi, D., Gallegos, R., Yamaguchi, S., Yu, X., Allewell, N.M., Malamy, M.H., and Tuchman, M. 2006. Acetylornithine transcarbamylase: A novel enzyme in arginine biosynthesis. J. Bacteriol. 188: 2974-2982.
22. Naumoff, D.G., Xu, Y., Glansdorff, N., and Labedan, B. 2004. Retrieving sequences of enzymes experimentally characterized but erroneously annotated: The case of the putrescine carbamoyltransferase. BMC Genomics 5: 52. doi: 10.1186/1471-2164-5-52.
23. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
24. Pastra-Landis, S.C., Foote, J., and Kantrowitz, E.R. 1981. An improved colorimetric assay for aspartate and ornithine transcarbamylases. Anal. Biochem. 118: 358-363.
25. Qu, Q., Morizono, H., Shi, D., Tuchman, M., and Caldovic, L. 2007. A novel bifunctional N-acetylglutamate synthase-kinase from Xanthomonas campestris that is closely related to mammalian N-acetylglutamate synthase. BMC Biochem. 8: 4. doi: 10.1186/1471-2091-8-4.
26. Shi, D., Morizono, H., Ha, Y., Aoyagi, M., Tuchman, M., and Allewell, N.M. 1998. 1.85 Å resolution crystal structure of human ornithine transcarbamylase complexed with N-phosphonacetyl-L-ornithine. J. Biol. Chem. 273: 34247-34254.
27. Shi, D., Morizono, H., Yu, X., Tong, L., Allewell, N.M., and Tuchman, M. 2001. Human ornithine transcarbamylase: Crystallographic insights into substrate recognition and conformational changes. Biochem. J. 354: 501-509.
28. Shi, D., Gallegos, R., DePonte III, J., Morizono, H., Yu, X., Allewell, N.M., Malamy, M., and Tuchman, M. 2002. Crystal structure of a transcarbamoylase-like protein from the anaerobic bacterium Bacteroides fragilis at 2.0 Å resolution. J. Mol. Biol. 320: 899-908.
29. Shi, D., Morizono, H., Yu, X., Roth, L., Caldovic, L., Allewell, N.M., Malamy, M.H., and Tuchman, M. 2005a. Crystal structure of N- acetylornithine transcarbamoylase from Xanthomonas campestris: A novel enzyme in a new arginine biosynthetic pathway found in several eubacteria. J. Biol. Chem. 280: 14366-14369.
30. Shi, D., Yu, X., Roth, L., Morizono, H., Hathout, Y., Allewell, N.M., and Tuchman, M. 2005b. Expression, purification, crystallization and preliminary X-ray crystallographic studies of a novel acetylcitrulline deacetylase from Xanthomonas campestris. Acta Crystallogr. F61: 676-679.
31. Shi, D., Morizono, H., Cabrera-Luque, J., Yu, X., Roth, L., Malamy, M.H., Allewell, N.M., and Tuchman, M. 2006a. Structure and catalytic mechanism of a novel N-succinyl-L-ornithine transcarbamylase in arginine biosynthesis of Bacteroides fragilis. J. Biol. Chem. 281: 20623-20631.
32. Shi, D., Yu, X., Roth, L., Morizono, H., Tuchman, M., and Allewell, N.M. 2006b. Structures of N-acetylornithine transcarbamoylase from Xanthomonas campestris complexed with substrates and substrate analogues imply mechanisms for substrate binding and catalysis. Proteins 64: 532-542.
33. Shi, D., Yu, X., Roth, L., Tuchman, M., and Allewell, N.M. 2007. Structure of a novel N-acetyl-L-citrulline deacetylase from Xanthomonas campestris. Biophys. Chem. 126: 86-93.
34. Slocum, R.D. 2005. Genes, enzymes and regulation of arginine biosynthesis in plants. Plant Physiol. Biochem. 43: 729-745.
35. Virnau, P., Mirny, L.A., and Kardar, M. 2006. Intricate knots in proteins: Function and evolution. PLoS Comput. Biol. 2: e122. doi: 10.1371/journal.pcbi.0020122.