Regulation of homocysteine metabolism by Mycobacterium tuberculosis S-adenosylhomocysteine hydrolase

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Singhal, Anshika ^a   Arora, Gunjan ^a   Sajid, Andaleeb ^a   Maji, Abhijit ^a   Bhat, Ajay ^a   Virmani, Richa ^a   Upadhyay, Sandeep ^b   Nandicoori, Vinay K ^b   Sengupta, Shantanu ^a   Singh, Yogendra ^a  

^a CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

^b NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSYLHOMOCYSTEINASE; HISTIDINE; HOMOCYSTEINE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVATION; ENZYMOLOGY; HYDROLYSIS; KINETICS; METABOLISM; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; PHOSPHORYLATION; PROTEIN CONFORMATION; REPRODUCIBILITY;

ADENOSYLHOMOCYSTEINASE; ENZYME ACTIVATION; HISTIDINE; HOMOCYSTEINE; HYDROLYSIS; KINETICS; METABOLIC NETWORKS AND PATHWAYS; MODELS, MOLECULAR; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; PHOSPHORYLATION; PROTEIN CONFORMATION; REPRODUCIBILITY OF RESULTS;

EID: 84880839314     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep02264     Document Type: Article

References (49)

1. De La Haba, G. & Cantoni, G. L. The enzymatic synthesis of S-adenosyl-Lhomocysteine from adenosine and homocysteine. J. Biol. Chem. 234, 603-608 (1959).
2. Finkelstein, J. D. Regulation of homocysteine metabolism. In Homocysteine in Health and Disease (eds Carmel, R., Jacobsen, D.) P 92-99 (Cambridge University Press, Cambridge, U.K. 2001).
3. Baric, I. et al. S-adenosylhomocysteine hydrolase deficiency in a human: a genetic disorder of methionine metabolism. Proc. Natl. Acad. Sci. U. S. A. 101, 4234-4239 (2004).
4. Weretilnyk, E. A. et al. Maintaining methylation activities during salt stress. The involvement of adenosine kinase. Plant Physiol. 125, 856-865 (2001).
5. Sganga, M. W., Aksamit, R. R., Cantoni, G. L. & Bauer, C. E. Mutational and nucleotide sequence analysis of S-adenosyl-L-homocysteine hydrolase from Rhodobacter capsulatus. Proc. Natl. Acad. Sci. U. S. A. 89, 6328-6332 (1992).
6. Fisher, E. W., Decedue, C. J., Keller, B. T. & Borchardt, R. T. Neplanocin A inhibition of S-adenosylhomocysteine hydrolase in Alcaligenes faecalis has no effect on growth of the microorganism. J. Antibiot. (Tokyo) 40, 873-881 (1987).
7. Griffin, J. E. et al. Cholesterol catabolism by Mycobacterium tuberculosis requires transcriptional and metabolic adaptations. Chem. Biol. 19, 218-227 (2012).
8. Chakraborty, S., Gruber, T., Barry, C. E., III, Boshoff, H. I. & Rhee, K. Y. Paraaminosalicylic acid acts as an alternative substrate of folate metabolism in Mycobacterium tuberculosis. Science 339, 88-91 (2013).
9. Sassetti, C. M., Boyd, D. H. & Rubin, E. J. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48, 77-84 (2003).
10. Turner, M. A. et al. Structure and function of S-adenosylhomocysteine hydrolase. Cell Biochem. Biophys. 33, 101-125 (2000).
11. Palmer, J. L. & Abeles, R. H. The mechanism of action of Sadenosylhomocysteinase. J. Biol. Chem. 254, 1217-1226 (1979).
12. Reddy, M. C. et al. Crystal structures of Mycobacterium tuberculosis S-adenosyl-Lhomocysteine hydrolase in ternary complex with substrate and inhibitors. Protein Sci. 17, 2134-2144 (2008).
13. Lozada-Ramirez, J. D., Martinez-Martinez, I., Sanchez-Ferrer, A. & Garcia- Carmona, F. A colorimetric assay for S-adenosylhomocysteine hydrolase. J. Biochem. Biophys. Methods 67, 131-140 (2006).
14. Matuszewska, B. & Borchardt, R. T. The role of nicotinamide adenine dinucleotide in the inhibition of bovine liver S-adenosylhomocysteine hydrolase by neplanocin A. J. Biol. Chem. 262, 265-268 (1987).
15. Singhal, N., Sharma, P., Kumar, M., Joshi, B. & Bisht, D. Analysis of intracellular expressed proteins of Mycobacterium tuberculosis clinical isolates. Proteome Sci. 10, 14 (2012).
16. Prisic, S. et al. Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases. Proc. Natl. Acad. Sci. U. S. A. 107, 7521-7526 (2010).
17. Boitel, B. et al. PknB kinase activity is regulated by phosphorylation in two Thr residues and dephosphorylation by PstP, the cognate phospho-Ser/Thr phosphatase, in Mycobacterium tuberculosis. Mol. Microbiol. 49, 1493-1508 (2003).
18. Kang, C.M. et al. The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev. 19, 1692-1704 (2005).
19. Deshayes, C. et al. Interrupted coding sequences in Mycobacterium smegmatis: authentic mutations or sequencing errors? Genome Biol. 8, R20 (2007).
20. Cole, S. T. et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544 (1998).
21. Cole, S. T. et al.Massive gene decay in the leprosy bacillus. Nature 409, 1007-1011 (2001).
22. Fernandez, P. et al. The Ser/Thr protein kinase PknB is essential for sustaining mycobacterial growth. J. Bacteriol. 188, 7778-7784 (2006).
23. Park, S. T., Kang, C. M. & Husson, R. N. Regulation of the SigH stress response regulon by an essential protein kinase in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 105, 13105-13110 (2008).
24. Parikh, A., Verma, S. K., Khan, S., Prakash, B. & Nandicoori, V. K. PknB-mediated phosphorylation of a novel substrate, N-acetylglucosamine-1- phosphate uridyltransferase, modulates its acetyltransferase activity. J. Mol. Biol. 386, 451-464 (2009).
25. Villarino, A. et al. Proteomic identification of M. tuberculosis protein kinase substrates: PknB recruits GarA, a FHA domain-containing protein, through activation loop-mediated interactions. J. Mol. Biol. 350, 953-963 (2005).
26. Dasgupta, A.,Datta, P., Kundu, M. & Basu, J. The serine/threonine kinase PknB of Mycobacterium tuberculosis phosphorylates PBPA, a penicillin-binding protein required for cell division. Microbiology 152, 493-504 (2006).
27. Sajid, A. et al. Interaction of Mycobacterium tuberculosis elongation factor Tu with GTP is regulated by phosphorylation. J. Bacteriol. 193, 5347-5358 (2011).
28. Boitel, B. et al. PknB kinase activity is regulated by phosphorylation in two Thr residues and dephosphorylation by PstP, the cognate phospho-Ser/Thr phosphatase, in Mycobacterium tuberculosis. Mol. Microbiol. 49, 1493-1508 (2003).
29. Wheeler, P. R. et al. Functional demonstration of reverse transsulfuration in the Mycobacterium tuberculosis complex reveals that methionine is the preferred sulfur source for pathogenic Mycobacteria. J. Biol. Chem. 280, 8069-8078 (2005).
30. Parker, W. B. & Long, M. C. Purine metabolism in Mycobacterium tuberculosis as a target for drug development. Curr. Pharm. Des. 13, 599-608 (2007).
31. Jakubowski, H. The determination of homocysteine-thiolactone in biological samples. Anal. Biochem. 308, 112-119 (2002).
32. Corrales, R. M., Leiba, J., Cohen-Gonsaud, M., Molle, V. & Kremer, L. Mycobacterium tuberculosis S-adenosyl-l-homocysteine hydrolase is negatively regulated by Ser/Thr phosphorylation. Biochem. Biophys. Res. Commun. 430, 858-864 (2013).
33. Tuite, N. L., Fraser, K. R. & O'byrne, C. P. Homocysteine toxicity in Escherichia coli is caused by a perturbation of branched-chain amino acid biosynthesis. J. Bacteriol. 187, 4362-4371 (2005).
34. Roe, A. J., O'Byrne, C., McLaggan, D. & Booth, I. R. Inhibition of Escherichia coli growth by acetic acid: a problem with methionine biosynthesis and homocysteine toxicity. Microbiology 148, 2215-2222 (2002).
35. Arora, G. et al. Unveiling the novel dual specificity protein kinases in Bacillus anthracis: identification of the first prokaryotic dual specificity tyrosine phosphorylation-regulated kinase (DYRK)-like kinase. J. Biol. Chem. 287, 26749-26763 (2012).
36. Wang, F. et al.Mycobacterium tuberculosis dihydrofolate reductase is not a target relevant to the antitubercular activity of isoniazid. Antimicrob. Agents Chemother. 54, 3776-3782 (2010).
37. Sharma, K. et al. Transcriptional control of themycobacterial embCAB operon by PknH through a regulatory protein, EmbR, in vivo. J. Bacteriol. 188, 2936-2944 (2006).
38. Bashiri, G., Rehan, A. M., Greenwood, D. R., Dickson, J. M. & Baker, E. N. Metabolic engineering of cofactor F420 production in Mycobacterium smegmatis. PLoS One. 5, e15803 (2010).
39. Khan, S. et al. Phosphorylation of enoyl-acyl carrier protein reductase InhA impacts mycobacterial growth and survival. J. Biol. Chem. 285, 37860-37871 (2010).
40. Gupta, M., Sajid, A., Arora, G., Tandon, V. & Singh, Y. Forkhead-associated domain-containing protein Rv0019c and polyketide-associated protein PapA5, from substrates of serine/threonine protein kinase PknB to interacting proteins of Mycobacterium tuberculosis. J. Biol. Chem. 284, 34723-34734 (2009).
41. Gomi, T., Takata, Y. & Fujioka, M. Rat liver S- adenosylhomocysteinase. Spectrophotometric study of coenzyme binding. Biochim. Biophys. Acta 994, 172-179 (1989).
42. Hershfield, M. S. Apparent suicide inactivation of human lymphoblast Sadenosylhomocysteine hydrolase by 29-deoxyadenosine and adenine arabinoside. A basis for direct toxic effects of analogs of adenosine. J. Biol. Chem. 254, 22-25 (1979).
43. Jacobsen, D. W. et al. Rapid HPLC determination of total homocysteine and other thiols in serum and plasma: sex differences and correlation with cobalamin and folate concentrations in healthy subjects. Clin. Chem. 40, 873-881 (1994).
44. Kumar, A. et al. Homocysteine- and cysteine-mediated growth defect is not associated with induction of oxidative stress response genes in yeast. Biochem. J. 396, 61-69 (2006).
45. Arora, G. et al. Understanding the role of PknJ in Mycobacterium tuberculosis: biochemical characterization and identification of novel substrate pyruvate kinase A. PLoS One 5, e10772 (2010).
46. Sajid, A. et al. Phosphorylation of Mycobacterium tuberculosis Ser/Thr phosphatase by PknA and PknB. PLoS One 6, e17871 (2011).
47. Boyle, W. J., van der, G. P. & Hunter, T. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201, 110-149 (1991).
48. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).
49. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).