Dimerization of bacterial diaminopimelate decarboxylase is essential for catalysis

Journal of Biological Chemistry

Volumn 291, Issue 18, 2016, Pages 9785-9795

  Peverelli, Martin G ^a,b   Da Costa, Tatiana P Soares ^a   Kirby, Nigel ^c   Perugini, Matthew A ^a,b  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c AUSTRALIAN SYNCHROTRON   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; BACTERIOLOGY; BIOCHEMISTRY; BIOSYNTHESIS; CATALYSIS; CATALYST ACTIVITY; DIMERS; ESCHERICHIA COLI; OLIGOMERS; X RAY SCATTERING;

ANALYTICAL ULTRACENTRIFUGATION; BACILLUS ANTHRACIS; BIOSYNTHESIS PATHWAYS; ESSENTIAL AMINO ACIDS; KINETIC ANALYSIS; MYCOBACTERIUM TUBERCULOSIS; STRUCTURAL STUDIES; VIRULENCE FACTORS;

DIMERIZATION;

ALANINE; ARGININE; ASPARAGINE; CARBOXYLYASE; DIAMINOPIMELATE DECARBOXYLASE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; LYSA PROTEIN, E COLI;

ARTICLE; BACILLUS ANTHRACIS; BACTERIUM MUTANT; CATALYSIS; CONTROLLED STUDY; DIMERIZATION; ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; VIBRIO CHOLERAE; AMINO ACID SUBSTITUTION; BACTERIUM; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MISSENSE MUTATION; PROTEIN MULTIMERIZATION;

AMINO ACID SUBSTITUTION; BACTERIA; CARBOXY-LYASES; CATALYSIS; ESCHERICHIA COLI PROTEINS; MUTATION, MISSENSE; PROTEIN MULTIMERIZATION;

EID: 84994291710     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.696591     Document Type: Article

References (45)

1. Dewey, D. L., and Work, E. (1952) Diaminopimelic acid and lysine: diaminopimelic acid decarboxylase. Nature 169, 533-534
2. Dogovski, C., Atkinson, S. C., Dommaraju, S. R., Hor, L., Dobson, R. C. J., Hutton C. A., Gerrard, J. A., and Perugini, M. A. (2009) in Biotechnology (Doelle, H. W., and Rokem, S., eds) pp. 116-136, Eolss Publishers, Oxford, UK
3. Dogovski, C, Atkinson, S. C, Dommaraju, S. R., Downton, M., Hor, L., Moore, S., Paxman, J. J., Peverelli, M. G., Qiu, T. W., Reumann, M., Siddiqui, T., Taylor, N. L., Wagner, J., Wubben, J. M., and Perugini, M. A. (2012) in Biochemistry (Ekinci, D., ed) pp. 225-262, InTech Open Access Publisher, Rijeka, Croatia
4. Hutton, C. A., Southwood, T. J., and Turner, J. J. (2003) Inhibitors of lysine biosynthesis as antibacterial agents. Mini Rev. Med. Chem. 3, 115-127
5. Asada, Y., Tanizawa, K., Sawada, S., Suzuki, T., Misono, H., and Soda, K. (1981) Stereochemistry of meso-α, ∈-diaminopimelate decarboxylase reaction: the first evidence for pyridoxal 5'-phosphate dependent decarboxylation with inversion of configuration. Biochemistry 20, 6881-6886
6. 13C NMR shift correlation to detect stereospecific deuterium labeling. Biochemistry 24, 3263-3267
7. Gokulan, K., Rupp, B., Pavelka, M. S., Jr., Jacobs, W. R., Jr., and Sacchettini, J. C. (2003) Crystal structure of Mycobacterium tuberculosis diaminopimelate decarboxylase, an essential enzyme in bacterial lysine biosynthesis. J. Biol. Chem. 278, 18588-18596
8. Hu, T., Wu, D., Chen, J., Ding, J., Jiang, H., and Shen, X. (2008) The catalytic intermediate stabilized by a "down" active site loop for diaminopimelate decarboxylase from Helicobacter pylori. J. Biol. Chem. 283, 21284-21293
9. Ray, S. S., Bonanno, J. B., Rajashankar, K. R., Pinho, M. G., He, G., De Lencastre, H., Tomasz, A., and Burley, S. K. (2002) Cocrystal structures of diaminopimelate decarboxylase: mechanism, evolution, and inhibition of an antibiotic resistance accessory factor. Structure 10, 1499-1508
10. Osterman, A., Grishin, N. V., Kinch, L. N., and Phillips, M. A. (1994) Formation of functional cross-species heterodimers of ornithine decarboxylase. Biochemistry 33, 13662-13667
11. Momany, C, Levdikov, V., Blagova, L., and Crews, K. (2002) Crystallization of diaminopimelate decarboxylase from Escherichia coli, a stereospecific D-amino-acid decarboxylase. Acta Crystallogr. D Biol. Crystallogr. 58, 549-552
12. Weyand, S., Kefala, G., Svergun, D. I., and Weiss, M. S. (2009) The three-dimensional structure of diaminopimelate decarboxylase from Mycobacterium tuberculosis reveals a tetrameric enzyme organization. J. Struct. Funct. Genomics 10, 209-217
13. White, P. J., and Kelly, B. (1965) Purification and properties of diaminopimelate decarboxylase from Escherichia coli. Biochem. J. 96, 75-84
14. Peverelli, M. G., and Perugini, M. A. (2015) An optimized coupled assay for quantifying diaminopimelate decarboxylase activity. Biochimie 115, 78-85
15. Hor, L., Peverelli, M. G., Perugini, M. A., and Hutton, C. A. (2013) A new robust kinetic assay for DAP epimerase activity. Biochimie 95, 1949-1953
16. Hor, L., Dobson, R. C, Downton, M. T., Wagner, J., Hutton, C. A., and Perugini, M. A. (2013) Dimerization of bacterial DAP epimerase is essential for catalysis. J. Biol. Chem. 288, 9238-9248
17. Brand, I. L., Civciristov, S., Taylor, N. L., Talbo, G. H, Pantaki-Eimany, D., Levina, V., Clem, R. J., Perugini, M. A., Kvansakul, M., and Hawkins, C. J. (2012) Caspase inhibitors of the P35 family are more active when purified from yeast than bacteria. PLoS ONE 7, e39248
18. Atkinson, S. C, Dogovski, C, Downton, M. T., Pearce, F. G., Reboul, C. F., Buckle, A. M., Gerrard, J. A., Dobson, R. C, Wagner, J., and Perugini, M. A. (2012) Crystal, solution and in silico structural studies of dihydrodipicolinate synthase from the common grapevine. PLoS ONE 7, e38318
19. Atkinson, S. C, Dogovski, C, Downton, M. T., Czabotar, P. E., Dobson, R. C, Gerrard, J. A., Wagner, J., and Perugini, M. A. (2013) Structural, kinetic and computational investigation of Vitis vinifera DHDPS reveals new insight into the mechanism of lysine-mediated allosteric inhibition. PlantMol. Biol. 81, 431-446
20. Voss, J. E., Scally, S. W., Taylor, N. L., Atkinson, S. C, Griffin, M. D., Hutton, C. A., Parker, M. W., Alderton, M. R., Gerrard, J. A., Dobson, R. C, Dogovski, C, and Perugini, M. A. (2010) Substrate-mediated stabilization of a tetrameric drug target reveals achilles heel in anthrax. J. Biol. Chem. 285, 5188-5195
21. Sreerama, N., and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252-260
22. Atkinson, S. C, Hor, L., Dogovski, C, Dobson, R. C, and Perugini, M. A. (2014) Identification of the bona fide DHDPS from a common plant pathogen. Proteins 82, 1869-1883
23. Burgess, B. R., Dobson, R. C, Bailey, M. F., Atkinson, S. C, Griffin, M. D., Jameson, G. B., Parker, M. W., Gerrard, J. A., and Perugini, M. A. (2008) Structure and evolution of a novel dimeric enzyme from a clinically-important bacterial pathogen. J. Biol. Chem. 283, 27598-27603
24. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) in Analytical Ultracentrifugation in Biochemistry and Polymer Science, pp. 90-125, The Royal Society of Chemistry, Cambridge, United Kingdom
25. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. BiophysJ. 78, 1606-1619
26. Schuck, P., Perugini, M. A., Gonzales, N. R., Howlett, G. J., and Schubert, D. (2002) Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys. J. 82, 1096-1111
27. Vistica, J., Dam, J., Balbo, A., Yikilmaz, E., Mariuzza, R. A., Rouault, P. A., and Schuck, P. (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal. Biochem. 326, 234-256
28. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J., and Svergun, D. I. (2003) PRIMUS: a Windows-PC based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282
29. Petoukhov, M. V., Konarev, P. V., Kikhney, A. G., and Svergun, D. I. (2007) ATSAS 2.1: towards automated and web-supported small-angle scattering data analysis. J. Appl. Crystallogr. 40, s223-s228
30. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
31. Mertens, H. D. T., and Svergun, D. I. (2010) Structural characterization of proteins and complexes using small-angle x-ray solution scattering. J. Struct. Biol. 172, 128-141
32. Svergun, D. I., Barberato, C, and Koch, M. H. J. (1995) CRYSOL: a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773
33. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886
34. Krissinel E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797
35. Dogovski, C, Gorman, M. A., Ketaren, N. E., Praszkier, J., Zammit, L. M., Mertens, H. D., Bryant, G., Yang, J., Griffin, M. D., Pearce, F. G., Gerrard, J. A., Jameson, G. B., Parker, M. W., Robins-Browne, R. M., and Perugini, M. A. (2013) From knock-out phenotype to three-dimensional structure of a promising antibiotic target from Streptococcus pneumoniae. PLoS ONE 8, e83419
36. Laber, B., and Amrhein, N. (1989) A spectrophotometric assay for mesodiaminopimelate decarboxylase and L-α-amino-∈-caprolactam hydrolase. Anal. Biochem. 181, 297-301
37. Myers, D. P., Jackson, L. K., Ipe, V. G., Murphy, G. E., and Phillips, M. A. (2001) Long-range interactions in the dimer interface of ornithine decarboxylase are important for enzyme function. Biochemistry 40, 13230-13236
38. Coleman, C. S., Stanley, B. A., and Pegg, A. E. (1993) Effect of mutations at active site residues on the activity of ornithine decarboxylase and its inhibition by active site-directed irreversible inhibitors. J. Biol. Chem. 268, 24572-24579
39. Tsirka, S., and Coffino, P. (1992) Dominant negative mutants of ornithine decarboxylase. J. Biol. Chem. 267, 23057-23062
40. Soares da Costa, T. P., Christensen, J. B., Desbois, S., Gordon, S. E., Gupta, R., Hogan, C. J., Nelson, T. G., Downton, M. T., Gardhi, C. K., Abbott, B. M., Wagner, J., Panjikar, S., Perugini, M. A. (2015) Quaternary structure analyses of an essential oligomeric enzyme. Methods Enzymol. 562, 205-223
41. Renatus, M., Stennicke, H. R., Scott, F. L., Liddington, R. C., and Salvesen, G. S. (2001) Dimer formation drives the activation of the cell death protease caspase 9. Proc. Natl. Acad. Sci. U. S. A. 98, 14250-14255
42. Ali, M. H., and Imperiali, B. (2005) Protein oligomerization: how and why. Bioorg. Med. Chem. 13, 5013-5020
43. Gerrard, J. A., Hutton, C. A., and Perugini, M. A. (2007) Inhibiting proteinprotein interactions as an emerging paradigm for drug discovery. Mini Rev. Med. Chem. 7, 151-157
44. Wells, J. A., and McClendon, C. L. (2007) Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 450, 1001-1009
45. Merabet, N., Dumond, J., Collinet, B., Van Baelinghem, L., Boggetto, N., Ongeri, S., Ressad, F., Reboud-Ravaux, M., and Sicsic, S. (2004) New constrained "molecular tongs" designed to dissociate HIV-1 protease dimer. J. Med. Chem. 47, 6392-6400