Structure and function of Mycobacterium tuberculosis meso-diaminopimelic acid (DAP) biosynthetic enzymes

FEMS Microbiology Letters

Volumn 330, Issue 1, 2012, Pages 10-16

  Usha, Veeraraghavan ^a   Lloyd, Adrian J ^b   Lovering, Andrew L ^a   Besra, Gurdyal S ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

DAP biosynthesis; Lysine; meso DAP; Mycobacteria; Peptidoglycan; Tuberculosis

Indexed keywords

ASPARTATE KINASE; ASPARTATE SEMIALDEHYDE DEHYDROGENASE; BACTERIAL ENZYME; DIAMINOPIMELATE EPIMERASE; DIAMINOPIMELIC ACID; DIHYDRODIPICOLINATE REDUCTASE; DIHYDRODIPICOLINATE SYNTHASE; DIHYDROLIPOAMIDE SUCCINYLTRANSFERASE; EPIMERASE; N SUCCINYL DIAMINOPIMELIC ACID DESUCCINYLASE; PEPTIDOGLYCAN; SUCCINYLDIAMINOPIMELATE AMINOTRANSFERASE; SYNTHETASE; TETRAHYDRODIPICOLINATE N SUCCINYLTRANSFERASE; UNCLASSIFIED DRUG;

BACTERIAL CELL WALL; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SYNTHESIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

BACTERIAL PROTEINS; DIAMINOPIMELIC ACID; METABOLIC NETWORKS AND PATHWAYS; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; PROTEIN CONFORMATION;

CORYNEBACTERINEAE; MAMMALIA; MYCOBACTERIUM TUBERCULOSIS;

EID: 84859430242     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2012.02527.x     Document Type: Review

References (58)

1. Antia M, Hoare DS & Work E (1957) The stereoisomers of alpha epsilon-diaminopimelic acid. III. Properties and distribution of diaminopimelic acid racemase, an enzyme causing interconversion of the LL and meso isomers. Biochem J 65: 448-459.
2. Badger J, Sauder JM, Adams JM et al. (2005) Structural analysis of a set of proteins resulting from a bacterial genomics project. Proteins 60: 787-796.
3. Bienvenue DL, Gilner DM, Davis RS, Bennett B & Holz RC (2003) Substrate specificity, metal binding properties, and spectroscopic characterization of the DapE-encoded N-succinyl-L, L-diaminopimelic acid desuccinylase from Haemophilus influenzae. Biochemistry 42: 10756-10763.
4. Born TL & Blanchard JS (1999) Structure/function studies on enzymes in the diaminopimelate pathway of bacterial cell wall biosynthesis. Curr Opin Chem Biol 3: 607-613.
5. Born TL, Zheng R & Blanchard JS (1998) Hydrolysis of N-succinyl-L, L-diaminopimelic acid by the Haemophilus influenzae dapE-encoded desuccinylase: metal activation, solvent isotope effects, and kinetic mechanism. Biochemistry 37: 10478-10487.
6. Bouvier J, Richaud C, Higgins W, Bogler O & Stragier P (1992) Cloning, characterization, and expression of the dapE gene of Escherichia coli. J Bacteriol 174: 5265-5271.
7. 2+. J Bacteriol 185: 4748-4754.
8. Bzymek KP & Holz RC (2004) The catalytic role of glutamate 151 in the leucine aminopeptidase from Aeromonas proteolytica. J Biol Chem 279: 31018-31025.
9. Cirilli M, Zheng R, Scapin G & Blanchard JS (2003) The three-dimensional structures of the Mycobacterium tuberculosis dihydrodipicolinate reductase-NADH-2, 6-PDC and -NADPH-2, 6-PDC complexes. Structural and mutagenic analysis of relaxed nucleotide specificity. Biochemistry 42: 10644-10650.
10. Cirillo JD, Weisbrod TR, Banerjee A, Bloom BR & Jacobs WR Jr (1994a) Genetic determination of the meso-diaminopimelate biosynthetic pathway of mycobacteria. J Bacteriol 176: 4424-4429.
11. Cirillo JD, Weisbrod TR, Pascopella L, Bloom BR & Jacobs WR Jr (1994b) Isolation and characterization of the aspartokinase and aspartate semialdehyde dehydrogenase operon from mycobacteria. Mol Microbiol 11: 629-639.
12. Corbett L & Raviglione M (2005). Global burden of tuberculosis: past, present and future. Tuberculosis and The Tubercle Bacillus (Cole ST, Eisenach KD, McMurray DN & Jacobs WR Jr), pp. 3-12. ASM Press, Washington, DC.
13. Cosper NJ, Bienvenue DL, Shokes JE, Gilner DM, Tsukamoto T, Scott RA & Holz RC (2003) The dapE-encoded N-succinyl-L, L-diaminopimelic acid desuccinylase from Haemophilus influenzae is a dinuclear metallohydrolase. J Am Chem Soc 125: 14654-14655.
14. Cox RJ, Sutherland A & Vederas JC (2000) Bacterial diaminopimelate metabolism as a target for antibiotic design. Bioorg Med Chem 8: 843-871.
15. Davis R, Bienvenue D, Swierczek SI, Gilner DM, Rajagopal L, Bennett B & Holz RC (2006) Kinetic and spectroscopic characterization of the E134A- and E134D-altered dapE-encoded N-succinyl-L, L-diaminopimelic acid desuccinylase from Haemophilus influenzae. J Biol Inorg Chem 11: 206-216.
16. Diaper CM, Sutherland A, Pillai B, James MN, Semchuk P, Blanchard JS & Vederas JC (2005) The stereoselective synthesis of aziridine analogues of diaminopimelic acid (DAP) and their interaction with dap epimerase. Org Biomol Chem 3: 4402-4411.
17. Dorman SE & Chaisson RE (2007) From magic bullets back to the magic mountain: the rise of extensively drug-resistant tuberculosis. Nat Med 13: 295-298.
18. Evans G, Schuldt L, Griffin MD et al. (2011) A tetrameric structure is not essential for activity in dihydrodipicolinate synthase (DHDPS) from Mycobacterium tuberculosis. Arch Biochem Biophys 512: 154-159.
19. Frieden TR, Sterling TR, Munsiff SS, Watt CJ & Dye C (2003) Tuberculosis. Lancet 362: 887-899.
20. Ghuysen JM (1980). Antibiotics and peptidoglycan metabolism. Topics in Antibiotic Chemistry (PG Sammes, ed), pp. 9-117. Wiley and Sons, New York.
21. Gillner D, Armoush N, Holz RC & Becker DP (2009a) Inhibitors of bacterial N-succinyl-L, L-diaminopimelic acid desuccinylase (DapE) and demonstration of in vitro antimicrobial activity. Bioorg Med Chem Lett 19: 6350-6352.
22. Gillner DM, Bienvenue DL, Nocek BP, Joachimiak A, Zachary V, Bennett B & Holz RC (2009b) The dapE-encoded N-succinyl-L, L-diaminopimelic acid desuccinylase from Haemophilus influenzae contains two active-site histidine residues. J Biol Inorg Chem 14: 1-10.
23. Girodeau JM, Agouridas C, Masson M, Pineau R & Le Goffic F (1986) The lysine pathway as a target for a new genera of synthetic antibacterial antibiotics? J Med Chem 29: 1023-1030.
24. Harper C (2007) Tuberculosis, a neglected opportunity? Nat Med 13: 309-312.
25. Hudson AO, Bless C, Macedo P, Chatterjee SP, Singh BK, Gilvarg C & Leustek T (2005) Biosynthesis of lysine in plants: evidence for a variant of the known bacterial pathways. Biochim Biophys Acta 1721: 27-36.
26. Janowski R, Kefala G & Weiss MS (2009) The structure of dihydrodipicolinate reductase (DapB) from Mycobacterium tuberculosis in three crystal forms. Acta Crystallogr D Biol Crystallogr 66: 61-72.
27. Karita M, Etterbeek ML, Forsyth MH, Tummuru MK & Blaser MJ (1997) Characterization of Helicobacter pylori dapE and construction of a conditionally lethal dapE mutant. Infect Immun 65: 4158-4164.
28. Kefala G & Weiss MS (2006) Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of DapA (Rv2753c) from Mycobacterium tuberculosis. Acta Crystallogr Sect F Struct Biol Cryst Commun 62: 1116-1119.
29. Kefala G, Janowski R, Panjikar S, Mueller-Dieckmann C & Weiss MS (2005) Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of DapB (Rv2773c) from Mycobacterium tuberculosis. Acta Crystallogr Sect F Struct Biol Cryst Commun 61: 718-721.
30. Kefala G, Evans GL, Griffin MD, Devenish SR, Pearce FG, Perugini MA, Gerrard JA, Weiss MS & Dobson RC (2008) Crystal structure and kinetic study of dihydrodipicolinate synthase from Mycobacterium tuberculosis. Biochem J 411: 351-360.
31. Koo CW & Blanchard JS (1999) Chemical mechanism of Haemophilus influenzae diaminopimelate epimerase. Biochemistry 38: 4416-4422.
32. Lloyd AJ, Huyton T, Turkenburg J & Roper DI (2004) Refinement of Haemophilus influenzae diaminopimelic acid epimerase (DapF) at 1.75 Å resolution suggests a mechanism for stereocontrol during catalysis. Acta Crystallogr D Biol Crystallogr 60: 397-400.
33. Mathema B, Kurepina NE, Bifani PJ & Kreiswirth BN (2006) Molecular epidemiology of tuberculosis: current insights. Clin Microbiol Rev 19: 658-685.
34. Matsuhashi M (1994) Utilization of lipid-linked precursors and the formation of peptidoglycan in the process of cell growth and division: membrane enzymes involved in the final steps of peptidoglycan synthesis and the mechanism of their regulation. Bacterial Cell Wall (Ghuysen JM & Hakenbeck R, eds), pp. 55-71. Elsevier Science, Amsterdam, the Netherlands.
35. Nocek BP, Gillner DM, Fan Y, Holz RC & Joachimiak A (2010) Structural basis for catalysis by the mono- and dimetalated forms of the dapE-encoded N-succinyl-L, L-diaminopimelic acid desuccinylase. J Mol Biol 397: 617-626.
36. Paiva AM, Vanderwall DE, Blanchard JS, Kozarich JW, Williamson JM & Kelly TM (2001) Inhibitors of dihydrodipicolinate reductase, a key enzyme of the diaminopimelate pathway of Mycobacterium tuberculosis. Biochim Biophys Acta 1545: 67-77.
37. Pavelka MS Jr (2000). Genetics of mycobacterial metabolism. Molecular Genetics of Mycobacteria (Hatfull GF & Jacobs WR Jr, eds), pp. 221-234. ASM Press, Washington, DC.
38. Pavelka MS Jr & Jacobs WR Jr (1996) Biosynthesis of diaminopimelate, the precursor of lysine and a component of peptidoglycan, is an essential function of Mycobacterium smegmatis. J Bacteriol 178: 6496-6507.
39. Pavelka MS Jr, Weisbrod TR & Jacobs WR Jr (1997) Cloning of the dapB gene, encoding dihydrodipicolinate reductase, from Mycobacterium tuberculosis. J Bacteriol 179: 2777-2782.
40. Pillai B, Cherney MM, Diaper CM, Sutherland A, Blanchard JS, Vederas JC & James MN (2006) Structural insights into stereochemical inversion by diaminopimelate epimerase: an antibacterial drug target. P Natl Acad Sci USA 103: 8668-8673.
41. Sassetti CM, Boyd DH & Rubin EJ (2001) Comprehensive identification of conditionally essential genes in mycobacteria. P Natl Acad Sci USA 98: 12712-12717.
42. Sassetti CM, Boyd DH & Rubin EJ (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77-84.
43. Schleifer KH & Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36: 407-477.
44. Schuldt L, Weyand S, Kefala G & Weiss MS (2008) Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of tetrahydrodipicolinate-N-succinyltransferase (Rv1201c) from Mycobacterium tuberculosis. Acta Crystallogr Sect F Struct Biol Cryst Commun 64: 863-866.
45. Schuldt L, Weyand S, Kefala G & Weiss MS (2009) The three-dimensional structure of a mycobacterial DapD provides insights into DapD diversity and reveals unexpected particulars about the enzymatic mechanism. J Mol Biol 389: 863-879.
46. Schuldt L, Suchowersky R, Veith K, Mueller-Dieckmann J & Weiss MS (2011) Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of the regulatory domain of aspartokinase (Rv3709c) from Mycobacterium tuberculosis. Acta Crystallogr Sect F Struct Biol Cryst Commun 67: 380-385.
47. Shafiani S, Sharma P, Vohra RM & Tewari R (2005) Cloning and characterization of aspartate-beta-semialdehyde dehydrogenase from Mycobacterium tuberculosis H37 Rv. J Appl Microbiol 98: 832-838.
48. Singh A, Kushwaha HR & Sharma P (2008) Molecular modelling and comparative structural account of aspartyl beta-semialdehyde dehydrogenase of Mycobacterium tuberculosis (H37Rv). J Mol Model 14: 249-263.
49. Sritharan V, Wheeler PR & Ratledge C (1989) Metabolism of aspartate in Mycobacterium smegmatis. Eur J Biochem 180: 587-593.
50. Uda NR & Creus M (2011) Selectivity of Inhibition of N-Succinyl-L, L-diaminopimelic acid desuccinylase in bacteria: the product of dapE-gene is not the target of L-Captopril antimicrobial activity. Bioinorg Chem Appl 2011: 306465.
51. Usha V, Dover LG, Roper DL, Lloyd AJ & Besra GS (2006) Use of a codon alteration strategy in a novel approach to cloning the Mycobacterium tuberculosis diaminopimelic acid epimerase. FEMS Microbiol Lett 262: 39-47.
52. Usha V, Dover LG, Roper DL & Besra GS (2008) Characterization of Mycobacterium tuberculosis diaminopimelic acid epimerase: paired cysteine residues are crucial for racemization. FEMS Microbiol Lett 280: 57-63.
53. Usha V, Dover LG, Roper DI, Futterer K & Besra GS (2009) Structure of the diaminopimelate epimerase DapF from Mycobacterium tuberculosis. Acta Crystallogr D Biol Crystallogr 65: 383-387.
54. Vyas R, Kumar V, Panjikar S, Karthikeyan S, Kishan KV, Tewari R & Weiss MS (2008) Purification, crystallization and preliminary X-ray diffraction analysis of aspartate semialdehyde dehydrogenase (Rv3708c) from Mycobacterium tuberculosis. Acta Crystallogr Sect F Struct Biol Cryst Commun 64: 167-170.
55. Weyand S, Kefala G & Weiss MS (2006) Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of DapC (Rv0858c) from Mycobacterium tuberculosis. Acta Crystallogr Sect F Struct Biol Cryst Commun 62: 794-797.
56. Weyand S, Kefala G & Weiss MS (2007) The three-dimensional structure of N-succinyldiaminopimelate aminotransferase from Mycobacterium tuberculosis. J Mol Biol 367: 825-838.
57. Wheeler PR & Blanchard JS (2005). General metabolism and biochemical pathways of tubercle bacilli. Tuberculosis and The Tubercle Bacillus (Cole ST, Eisenach KD, McMurray DN & Jacobs WR Jr, eds), pp. 309-340. ASM Press, Washington, DC.
58. Wietzerbin J, Das BC, Petit JF, Lederer E, Leyh-Bouille M & Ghuysen JM (1974) Occurrence of D-alanyl-(D)-meso-diaminopimelic acid and meso-diaminopimelyl-meso-diaminopimelic acid interpeptide linkages in the peptidoglycan of mycobacteria. Biochemistry 13: 3471-3476.