Chemical, genetic and structural assessment of pyridoxal kinase as a drug target in the African trypanosome

Molecular Microbiology

Volumn 86, Issue 1, 2012, Pages 51-64

  Jones, Deuan C ^a   Alphey, Magnus S ^a,b   Wyllie, Susan ^a   Fairlamb, Alan H ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; PYRIDOXAL KINASE; PYRIDOXAMINE; PYRIDOXINE;

AFRICAN TRYPANOSOMIASIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG TARGETING; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; GENETIC ANALYSIS; MICROMORPHOLOGY; MOLECULAR CLONING; MOUSE; NONHUMAN; PARASITE DEVELOPMENT; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS; TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; ANIMALS; ANTIPROTOZOAL AGENTS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; GENE DELETION; GENES, ESSENTIAL; GENES, PROTOZOAN; HUMANS; KINETICS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN CONFORMATION; PYRIDOXAL; PYRIDOXAL KINASE; PYRIDOXAMINE; PYRIDOXINE; SEQUENCE ALIGNMENT; SURVIVAL ANALYSIS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN; VIRULENCE FACTORS;

MUS; TRYPANOSOMA BRUCEI;

EID: 84867086396     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08189.x     Document Type: Article

References (57)

1. Bach, S., Knockaert, M., Reinhardt, J., Lozach, O., Schmitt, S., Baratte, B., etal. (2005) Roscovitine targets, protein kinases and pyridoxal kinase. J Biol Chem 280: 31208-31219.
2. Baker, H., DeAngelis, B., and Frank, O. (1988) Vitamins and other metabolites in various sera commonly used for cell culturing. Experientia 44: 1007-1010.
3. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D.C., etal. (2005) The Genome of the African Trypanosome Trypanosoma brucei. Science 309: 416-422.
4. Bond, C.S., and Schuttelkopf, A.W. (2009) ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr D Biol Crystallogr 65: 510-512.
5. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
6. Burkard, G., Fragoso, C.M., and Roditi, I. (2007) Highly efficient stable transformation of bloodstream forms of Trypanosoma brucei. Mol Biochem Parasitol 153: 220-223.
7. Burri, C. (2010) Chemotherapy against human African trypanosomiasis: is there a road to success? Parasitol 137: 1987-1994.
8. Cadet, J., Douki, T., and Ravanat, J.L. (2010) Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 49: 9-21.
9. Campobasso, N., Mathews, I.I., Begley, T.P., and Ealick, S.E. (2000) Crystal structure of 4-methyl-5-beta-hydroxyethylthiazole kinase from Bacillus subtilis at 1.5 Å resolution. Biochemistry 39: 7868-7877.
10. Cheng, G., Bennett, E.M., Begley, T.P., and Ealick, S.E. (2002) Crystal structure of 4-amino-5-hydroxymethyl-2-methylpyrimidine phosphate kinase from Salmonella typhimurium at 2.3 Å resolution. Structure 10: 225-235.
11. Clayton, P.T. (2006) B6-responsive disorders: a model of vitamin dependency. J Inherit Metab Dis 29: 317-326.
12. DeLano, W.L. (2005) The PyMOL Molecular Graphics System. [WWW document]. URL http://www.pymol.org
13. Di Cera, E. (2006) A structural perspective on enzymes activated by monovalent cations. J Biol Chem 281: 1305-1308.
14. Dick, T., Manjunatha, U., Kappes, B., and Gengenbacher, M. (2010) Vitamin B6 biosynthesis is essential for survival and virulence of Mycobacterium tuberculosis. Mol Microbiol 78: 980-988.
15. Ehrenshaft, M., Bilski, P., Li, M.Y., Chignell, C.F., and Daub, M.E. (1999) A highly conserved sequence is a novel gene involved in de novo vitamin B6 biosynthesis. Proc Natl Acad Sci USA 96: 9374-9378.
16. Eliot, A.C., and Kirsch, J.F. (2004) Pyridoxal phosphate enzymes: mechanistic, structural, and evolutionary considerations. Annu Rev Biochem 73: 383-415.
17. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
18. Fairlamb, A.H., Henderson, G.B., Bacchi, C.J., and Cerami, A. (1987) In vivo effects of difluoromethylornithine on trypanothione and polyamine levels in bloodstream forms of Trypanosoma brucei. Mol Biochem Parasitol 24: 185-191.
19. Fitzpatrick, T.B., Moccand, C., and Roux, C. (2010) Vitamin B-6 biosynthesis: charting the mechanistic landscape. Chembiochem 11: 1185-1193.
20. Frearson, J.A., Wyatt, P.A., Gilbert, I.H., and Fairlamb, A.H. (2007) Target assessment for antiparasitic drug discovery. Trends Parasitol 23: 589-595.
21. Gandhi, A.K., Ghatge, M.S., Musayev, F.N., Sease, A., Aboagye, S.O., Di Salvo, M.L., etal. (2009) Kinetic and structural studies of the role of the active site residue Asp235 of human pyridoxal kinase. Biochem Biophys Res Commun 381: 12-15.
22. Gray, A. (1995) Trypanosoma brucei brucei - uptake and metabolism of pyridoxine and pyridoxal. Exp Parasitol 80: 390-400.
23. Greig, N., Wyllie, S., Patterson, S., and Fairlamb, A.H. (2009) A comparative study of methylglyoxal metabolism in trypanosomatids. FEBS J 276: 376-386.
24. Hirumi, H., and Hirumi, K. (1989) Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J Parasitol 75: 985-989.
25. Jones, D.C., Hallyburton, I., Stojanovski, L., Read, K.D., Frearson, J.A., and Fairlamb, A.H. (2010) Identification of a kappa-opioid agonist as a potent and selective lead for drug development against human African trypanosomiasis. Biochem Pharmacol 80: 1478-1486.
26. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst 26: 795-800.
27. Kastner, U., Hallmen, C., Wiese, M., Leistner, E., and Drewke, C. (2007) The human pyridoxal kinase, a plausible target for ginkgotoxin from Ginkgo biloba. FEBS J 274: 1036-1045.
28. Kidder, G.W., and Dutta, B.N. (1958) The growth and nutrition of Crithidia fasciulata. J Gen Microbiol 18: 621-638.
29. Konig, J., Wyllie, S., Wells, G., Stevens, M.F., Wyatt, P.G., and Fairlamb, A.H. (2011) Antitumor quinol PMX464 is a cytocidal anti-trypanosomal inhibitor targeting trypanothione metabolism. J Biol Chem 286: 8523-8533.
30. Kwok, F., and Churchich, J.E. (1979) Brain pyridoxal kinase - purification, substrate specificities, and sensitized photodestruction of an essential histidine. J Biol Chem 254: 6489-6495.
31. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
32. Leistner, E., and Drewke, C. (2010) Ginkgo biloba and ginkgotoxin. J Nat Prod 73: 86-92.
33. Li, F., Hua, S.B., Wang, C.C., and Gottesdiener, K.M. (1998) Trypanosoma brucei brucei: characterization of an ODC null bloodstream form mutant and the action of α-difluoromethylornithine. Exp Parasitol 88: 255-257.
34. Li, M.H., Kwok, F., Chang, W.R., Lau, C.K., Zhang, J.P., Lo, S.C., etal. (2002) Crystal structure of brain pyridoxal kinase, a novel member of the ribokinase superfamily. J Biol Chem 277: 46385-46390.
35. Mathews, I.I., Erion, M.D., and Ealick, S.E. (1998) Structure of human adenosine kinase at 1.5 Å resolution. Biochemistry 37: 15607-15620.
36. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
37. 2+ activation. Protein Sci 16: 2184-2194.
38. Percudani, R., and Peracchi, A. (2009) The B6 database: a tool for the description and classification of vitamin B6-dependent enzymatic activities and of the corresponding protein families. BMC Bioinformatics 10: e273.
39. Peterson, E.A., and Sober, H.A. (1954) Preparation of crystalline phosphorylated derivatives of vitamin B6. J Am Chem Soc 76: 169-175.
40. Raz, B., Iten, M., Grether-Buhler, Y., Kaminsky, R., and Brun, R. (1997) The Alamar Blue® assay to determine drug sensitivity of African trypanosomes (T.b.rhodesiense and T.b.gambiense) in vitro. Acta Trop 68: 139-147.
41. Roper, J.R., Guther, M.L.S., Milne, K.G., and Ferguson, M.A.J. (2002) Galactose metabolism is essential for the African sleeping sickness parasite Trypanosoma brucei. Proc Natl Acad Sci USA 99: 5884-5889.
42. Safo, M.K., Musayev, F.N., Di Salvo, M.L., Hunt, S., Claude, J.B., and Schirch, V. (2006) Crystal structure of pyridoxal kinase from the Escherichia coli pdxK gene: implications for the classification of pyridoxal kinases. J Bacteriol 188: 4542-4552.
43. Schumacher, M.A., Scott, D.M., Mathews, I.I., Ealick, S.E., Roos, D.S., Ullman, B., and Brennan, R.G. (2000) Crystal structures of Toxoplasma gondii adenosine kinase reveal a novel catalytic mechanism and prodrug binding. J Mol Biol 298: 875-893.
44. Scott, T.C., and Phillips, M.A. (1997) Characterization of Trypanosoma brucei pyridoxal kinase: purification, gene isolation and expression in Escherichia coli. Mol Biochem Parasitol 88: 1-11.
45. Sienkiewicz, N., Jaroslawski, S., Wyllie, S., and Fairlamb, A.H. (2008) Chemical and genetic validation of dihydrofolate reductase-thymidylate synthase as a drug target in African trypanosomes. Mol Microbiol 69: 520-533.
46. Sigrell, J.A., Cameron, A.D., Jones, T.A., and Mowbray, S.L. (1998) Structure of Escherichia coli ribokinase in complex with ribose and dinucleotide determined to 1.8 Å resolution: insights into a new family of kinase structures. Structure 6: 183-193.
47. Snider, D.E. (1980) Pyridoxine supplementation during isoniazid therapy. Tubercle 61: 191-196.
48. Stuart, K.D., Brun, R., Croft, S.L., Fairlamb, A.H., Gurtler, R.E., McKerrow, J.H., etal. (2008) Kinetoplastids: related protozoan pathogens, different diseases. J Clin Invest 118: 1301-1310.
49. Tang, L., Li, M.H., Cao, P., Wang, F., Chang, W.R., Bach, S., etal. (2005) Crystal structure of pyridoxal kinase in complex with roscovitine and derivatives. J Biol Chem 280: 31220-31229.
50. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J Appl Cryst 30: 1022-1025.
51. Watkins, R.C., Hambrick, E.L., Benjamin, G., and Chavda, S.N. (1990) Isoniazid toxicity presenting as seizures and metabolic acidosis. J Natl Med Assoc 82: 57-5&.
52. Wirtz, E., Leal, S., Ochatt, C., and Cross, G.A.M. (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 99: 89-101.
53. Wrenger, C., Knockel, J., Walter, R.D., and Muller, I.B. (2008) Vitamin B1 and B6 in the malaria parasite: requisite or dispensable? Braz J Med Biol Res 41: 82-88.
54. Wyatt, P.G., Gilbert, I.H., Read, K.D., and Fairlamb, A.H. (2011) Target validation: linking target and chemical properties to desired product profile. Curr Top Med Chem 11: 1275-1283.
55. Wyllie, S., Oza, S.L., Patterson, S., Spinks, D., Thompson, S., and Fairlamb, A.H. (2009) Dissecting the essentiality of the bifunctional trypanothione synthetase-amidase in Trypanosoma brucei using chemical and genetic methods. Mol Microbiol 74: 529-540.
56. Yun, O., Priotto, G., Tong, J., Flevaud, L., and Chappuis, F. (2010) NECT is next: implementing the new drug combination therapy for Trypanosoma brucei gambiense sleeping sickness. PLoS Negl Trop Dis 4: e720.
57. Ziegelhoffer, E.C., and Donohue, T.J. (2009) Bacterial responses to photo-oxidative stress. Nat Rev Microbiol 7: 856-863.