Kinetic mechanism and inhibition of Mycobacterium tuberculosis d-alanine: D-alanine ligase by the antibiotic d-cycloserine

FEBS Journal

Volumn 280, Issue 4, 2013, Pages 1150-1166

  Prosser, Gareth A ^a   De Carvalho, Luiz Pedro S ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

d amino acid; peptidoglycan biosynthesis; Rv2981c; tuberculosis

Indexed keywords

CYCLOSERINE; DEXTRO ALANINE DEXTRO ALANINE LIGASE;

AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVE SITE; ENZYME INHIBITION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; INHIBITION KINETICS; LIGAND BINDING; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PH; PRIORITY JOURNAL; STEADY STATE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ALANINE; ANTIBIOTICS, ANTITUBERCULAR; BACTERIAL PROTEINS; BINDING, COMPETITIVE; CYCLOSERINE; DIPEPTIDES; HYDROGEN-ION CONCENTRATION; KINETICS; MYCOBACTERIUM TUBERCULOSIS; PEPTIDE SYNTHASES; PROTEIN BINDING;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 84874114728     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12108     Document Type: Article

References (49)

1. Lambert MP, &, Neuhaus FC, (1972) Mechanism of d -cycloserine action: alanine racemase from Escherichia coli W. J Bacteriol 110, 978-987.
2. Neuhaus FC, &, Lynch JL, (1964) The enzymatic synthesis of d -alanyl- d -alanine. 3. On the inhibition of d -alanyl- d -alanine synthetase by the antibiotic d -cycloserine. Biochemistry 3, 471-480.
3. Neuhaus FC, (1962) The enzymatic synthesis of d -alanyl- d -alanine. I. Purification and properties of d -alanyl- d -alanine synthetase. J Biol Chem 237, 778-786.
4. Wood WA, &, Gunsalus IC, (1951) d -Alanine formation; a racemase in Streptococcus faecalis. J Biol Chem 190, 403-416.
5. Caminero JA, Sotgiu G, Zumla A, &, Migliori GB, (2010) Best drug treatment for multidrug-resistant and extensively drug-resistant tuberculosis. Lancet Infect Dis 10, 621-629.
6. Yew WW, Wong CF, Wong PC, Lee J, &, Chau CH, (1993) Adverse neurological reactions in patients with multidrug-resistant pulmonary tuberculosis after coadministration of cycloserine and ofloxacin. Clin Infect Dis 17, 288-289.
7. Arbex MA, Varella MC, Siqueira HR, &, Mello FA, (2010) Antituberculosis drugs: drug interactions, adverse effects, and use in special situations. Part 2: second line drugs. J Bras Pneumol 36, 641-656.
8. Sassetti CM, Boyd DH, &, Rubin EJ, (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48, 77-84.
9. Sassetti CM, &, Rubin EJ, (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100, 12989-12994.
10. Milligan DL, Tran SL, Strych U, Cook GM, &, Krause KL, (2007) The alanine racemase of Mycobacterium smegmatis is essential for growth in the absence of d -alanine. J Bacteriol 189, 8381-8386.
11. Awasthy D, Bharath S, Subbulakshmi V, &, Sharma U, (2012) Alanine racemase mutants of Mycobacterium tuberculosis require d -alanine for growth and are defective for survival in macrophages and mice. Microbiology 158, 319-327.
12. Caceres NE, Harris NB, Wellehan JF, Feng Z, Kapur V, &, Barletta RG, (1997) Overexpression of the d -alanine racemase gene confers resistance to d -cycloserine in Mycobacterium smegmatis. J Bacteriol 179, 5046-5055.
13. Feng Z, &, Barletta RG, (2003) Roles of Mycobacterium smegmatis d -alanine: d -alanine ligase and d -alanine racemase in the mechanisms of action of and resistance to the peptidoglycan inhibitor d -cycloserine. Antimicrob Agents Chemother 47, 283-291.
14. Halouska S, Chacon O, Fenton RJ, Zinniel DK, Barletta RG, &, Powers R, (2007) Use of NMR metabolomics to analyze the targets of d -cycloserine in mycobacteria: role of d -alanine racemase. J Proteome Res 6, 4608-4614.
15. Fenn TD, Holyoak T, Stamper GF, &, Ringe D, (2005) Effect of a Y265F mutant on the transamination-based cycloserine inactivation of alanine racemase. Biochemistry 44, 5317-5327.
16. Priyadarshi A, Lee EH, Sung MW, Nam KH, Lee WH, Kim EE, &, Hwang KY, (2009) Structural insights into the alanine racemase from Enterococcus faecalis. Biochim Biophys Acta 1794, 1030-1040.
17. Fenn TD, Stamper GF, Morollo AA, &, Ringe D, (2003) A side reaction of alanine racemase: transamination of cycloserine. Biochemistry 42, 5775-5783.
18. Kim MG, Strych U, Krause K, Benedik M, &, Kohn H, (2003) N(2)-substituted d, l -cycloserine derivatives: synthesis and evaluation as alanine racemase inhibitors. J Antibiot (Tokyo) 56, 160-168.
19. Anthony KG, Strych U, Yeung KR, Shoen CS, Perez O, Krause KL, Cynamon MH, Aristoff PA, &, Koski RA, (2011) New classes of alanine racemase inhibitors identified by high-throughput screening show antimicrobial activity against Mycobacterium tuberculosis. PLoS One 6, e20374.
20. Ciustea M, Mootien S, Rosato AE, Perez O, Cirillo P, Yeung KR, Ledizet M, Cynamon MH, Aristoff PA, Koski RA, et al,. (2012) Thiadiazolidinones: a new class of alanine racemase inhibitors with antimicrobial activity against methicillin-resistant Staphylococcus aureus. Biochem Pharmacol 83, 368-377.
21. Mustata GI, &, Briggs JM, (2002) A structure-based design approach for the identification of novel inhibitors: application to an alanine racemase. J Comput Aided Mol Des 16, 935-953.
22. Bugg TD, Dutka-Malen S, Arthur M, Courvalin P, &, Walsh CT, (1991) Identification of vancomycin resistance protein VanA as a d -alanine: d -alanine ligase of altered substrate specificity. Biochemistry 30, 2017-2021.
23. Zawadzke LE, Bugg TD, &, Walsh CT, (1991) Existence of two d -alanine: d -alanine ligases in Escherichia coli: cloning and sequencing of the ddlA gene and purification and characterization of the DdlA and DdlB enzymes. Biochemistry 30, 1673-1682.
24. Liu S, Chang JS, Herberg JT, Horng MM, Tomich PK, Lin AH, &, Marotti KR, (2006) Allosteric inhibition of Staphylococcus aureus d -alanine: d -alanine ligase revealed by crystallographic studies. Proc Natl Acad Sci USA 103, 15178-15183.
25. Noda M, Kawahara Y, Ichikawa A, Matoba Y, Matsuo H, Lee DG, Kumagai T, &, Sugiyama M, (2004) Self-protection mechanism in d -cycloserine-producing Streptomyces lavendulae. Gene cloning, characterization, and kinetics of its alanine racemase and d -alanyl- d -alanine ligase, which are target enzymes of d -cycloserine. J Biol Chem 279, 46143-46152.
26. Fan C, Moews PC, Walsh CT, &, Knox JR, (1994) Vancomycin resistance: structure of d -alanine: d -alanine ligase at 2.3 Å resolution. Science 266, 439-443.
27. Fan C, Park IS, Walsh CT, &, Knox JR, (1997) d -alanine: d -alanine ligase: phosphonate and phosphinate intermediates with wild type and the Y216F mutant. Biochemistry 36, 2531-2538.
28. Kitamura Y, Ebihara A, Agari Y, Shinkai A, Hirotsu K, &, Kuramitsu S, (2009) Structure of d -alanine- d -alanine ligase from Thermus thermophilus HB8: cumulative conformational change and enzyme-ligand interactions. Acta Crystallogr D Biol Crystallogr 65, 1098-1106.
29. Bruning JB, Murillo AC, Chacon O, Barletta RG, &, Sacchettini JC, (2011) Structure of the Mycobacterium tuberculosis d -alanine: d -alanine ligase, a target of the antituberculosis drug d -cycloserine. Antimicrob Agents Chemother 55, 291-301.
30. Lee JH, Na Y, Song HE, Kim D, Park BH, Rho SH, Im YJ, Kim MK, Kang GB, Lee DS, et al,. (2006) Crystal structure of the apo form of d -alanine: d -alanine ligase (Ddl) from Thermus caldophilus: a basis for the substrate-induced conformational changes. Proteins 64, 1078-1082.
31. Wu D, Zhang L, Kong Y, Du J, Chen S, Chen J, Ding J, Jiang H, &, Shen X, (2008) Enzymatic characterization and crystal structure analysis of the d -alanine- d -alanine ligase from Helicobacter pylori. Proteins 72, 1148-1160.
32. David HL, Takayama K, &, Goldman DS, (1969) Susceptibility of mycobacterial d -alanyl- d -alanine synthetase to d -cycloserine. Am Rev Respir Dis 100, 579-581.
33. Strominger JL, Ito E, &, Threnn RH, (1960) Competitive inhibition of enzymatic reactions by oxamycin. J Am Chem Soc 82, 998-999.
34. Neuhaus FC, (1962) The enzymatic synthesis of d -alanyl- d -alanine. II. Kinetic studies on d -alanyl- d -alanine synthetase. J Biol Chem 237, 3128-3135.
35. Park IS, &, Walsh CT, (1997) d -Alanyl- d -lactate and d -alanyl- d -alanine synthesis by d -alanyl- d -alanine ligase from vancomycin-resistant Leuconostoc mesenteroides. Effects of a phenylalanine 261 to tyrosine mutation. J Biol Chem 272, 9210-9214.
36. Daub E, Zawadzke LE, Botstein D, &, Walsh CT, (1988) Isolation, cloning, and sequencing of the Salmonella typhimurium ddlA gene with purification and characterization of its product, d -alanine: d -alanine ligase (ADP forming). Biochemistry 27, 3701-3708.
37. Park IS, Lin CH, &, Walsh CT, (1997) Bacterial resistance to vancomycin: overproduction, purification, and characterization of VanC2 from Enterococcus casseliflavus as a d -Ala- d -Ser ligase. Proc Natl Acad Sci USA 94, 10040-10044.
38. Follmann M, Becker M, Ochrombel I, Ott V, Kramer R, &, Marin K, (2009) Potassium transport in Corynebacterium glutamicum is facilitated by the putative channel protein CglK, which is essential for pH homeostasis and growth at acidic pH. J Bacteriol 191, 2944-2952.
39. Mullins LS, Zawadzke LE, Walsh CT, &, Raushel FM, (1990) Kinetic evidence for the formation of d -alanyl phosphate in the mechanism of d -alanyl- d -alanine ligase. J Biol Chem 265, 8993-8998.
40. Fan C, Moews PC, Shi Y, Walsh CT, &, Knox JR, (1995) A common fold for peptide synthetases cleaving ATP to ADP: glutathione synthetase and d -alanine: d -alanine ligase of Escherichia coli. Proc Natl Acad Sci USA 92, 1172-1176.
41. Park IS, Lin CH, &, Walsh CT, (1996) Gain of d -alanyl- d -lactate or d -lactyl- d -alanine synthetase activities in three active-site mutants of the Escherichia coli d -alanyl- d -alanine ligase B. Biochemistry 35, 10464-10471.
42. Shi Y, &, Walsh CT, (1995) Active site mapping of Escherichia coli d -Ala- d -Ala ligase by structure-based mutagenesis. Biochemistry 34, 2768-2776.
43. a values for the ligands and side chains of Escherichia coli d -alanine: d -alanine ligase. J Med Chem 42, 109-117.
44. Lessard IA, Healy VL, Park IS, &, Walsh CT, (1999) Determinants for differential effects on d -Ala- d -lactate vs d -Ala- d -Ala formation by the VanA ligase from vancomycin-resistant enterococci. Biochemistry 38, 14006-14022.
45. Healy VL, Mullins LS, Li X, Hall SE, Raushel FM, &, Walsh CT, (2000) d -Ala- d -X ligases: evaluation of d -alanyl phosphate intermediate by MIX, PIX and rapid quench studies. Chem Biol 7, 505-514.
46. Tian J, Bryk R, Itoh M, Suematsu M, &, Nathan C, (2005) Variant tricarboxylic acid cycle in Mycobacterium tuberculosis: identification of α-ketoglutarate decarboxylase. Proc Natl Acad Sci USA 102, 10670-10675.
47. Chacon O, Bermudez LE, Zinniel DK, Chahal HK, Fenton RJ, Feng Z, Hanford K, Adams LG, &, Barletta RG, (2009) Impairment of d -alanine biosynthesis in Mycobacterium smegmatis determines decreased intracellular survival in human macrophages. Microbiology 155, 1440-1450.
48. McBain CJ, Kleckner NW, Wyrick S, &, Dingledine R, (1989) Structural requirements for activation of the glycine coagonist site of N-methyl- d -aspartate receptors expressed in Xenopus oocytes. Mol Pharmacol 36, 556-565.
49. Fersht A, (1999) Structure and Mechanism in Protein Science, 3rd edn. W.H. Freeman, New York, p. 206.