Exploring inhibition of Pdx1, a component of the PLP synthase complex of the human malaria parasite Plasmodium falciparum

Biochemical Journal

Volumn 449, Issue 1, 2013, Pages 175-187

  Reeksting, Shaun B ^a,b   Müller, Ingrid B ^b   Burger, Pieter B ^a   Burgos, Emmanuel S ^c   Salmon, Laurent ^d   Louw, Abraham I ^a   Birkholtz, Lyn Marie ^a   Wrenger, Carsten ^b,e  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d UNIVERSITÉ PARIS SUD   (France)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

D erythrose 4 phosphate (E4P); Pdx1; Plasmodium falciparum; PLP synthase; Pyridoxal 5 phosphate (PLP); Vitamin B6

Indexed keywords

DEXTRO ERYTHROSE 4 PHOSPHATE; DEXTRO RIBOSE 5 PHOSPHATE; PHOSPHATE; PYRIDOXAL 5 PHOSPHATE; TRANSCRIPTION FACTOR PDX 1; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ANIMALS; ANTIMALARIALS; HUMANS; HYDROXAMIC ACIDS; PLASMODIUM FALCIPARUM; PYRUVATE DEHYDROGENASE COMPLEX; SUBSTRATE SPECIFICITY; SUGAR PHOSPHATES;

PLASMODIUM FALCIPARUM;

EID: 84870875476     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120925     Document Type: Article

References (52)

1. Greenwood, B. M., Fidock, D. A., Kyle, D. E., Kappe, S. H. I., Alonso, P. L., Collins, F. H. and Duffy, P. E. (2008) Malaria: progress, perils, and prospects for eradication. J. Clin. Invest. 118, 1266-1276 (Pubitemid 351500419)
2. Greenwood, B. M. (2008) Control to elimination: implications for malaria research. Trends Parasitol. 24, 449-454
3. Guiguemde, W. A., Shelat, A. A., Garcia-Bustos, J. F., Diagana, T. T., Gamo, F. J. and Guy, R. K. (2012) Global phenotypic screening for antimalarials. Chem. Biol. 19, 116-129
4. Eliot, A. C. and Kirsch, J. F. (2004) Pyridoxal phosphate enzymes: mechanistic, structural, and evolutionary considerations. Annu. Rev. Biochem. 73, 383-415 (Pubitemid 39050374)
5. 6 biosynthesis pathway in the human malaria parasite Plasmodium falciparum. J. Biol. Chem. 280, 5242-5248
6. 6 in Plasmodium falciparum validated by protein interference. Biochem. J. 443, 397-405
7. Müller, I. B., Hyde, J. E. and Wrenger, C. (2010) Vitamin B metabolism in Plasmodium falciparum as a source of drug targets. Trends Parasitol. 26, 35-43
8. 6: enzymatic conversion of 1-deoxy-D-xylulose-5-phosphate to pyridoxol phosphate. J. Am. Chem. Soc. 121, 7722-7723
9. Knöckel, J., Müller, I. B., Bergmann, B., Walter, R. D. and Wrenger, C. (2007) The apicomplexan parasite Toxoplasma gondii generates pyridoxal phosphate de novo. Mol. Biochem. Parasitol. 152, 108-111 (Pubitemid 46107705)
10. 13C NMR snapshots of the complex reaction coordinate of pyridoxal phosphate synthase. Nat. Chem. Biol. 4, 425-430
11. 6 biosynthesis by the malaria parasite Plasmodium falciparum. J. Biol. Chem. 281, 3633-3641
12. Strohmeier, M., Raschle, T., Mazurkiewicz, J., Rippe, K., Sinning, I., Fitzpatrick, T. B. and Tews, I. (2006) Structure of a bacterial pyridoxal 5′-phosphate synthase complex. Proc. Natl. Acad. Sci. U.S.A. 103, 19284-19289 (Pubitemid 46028495)
13. Zhang, X., Teng, Y., Liu, J., He, Y., Zhou, K., Chen, Y. and Zhou, C. (2010) Structural insights into the catalytic mechanism of the yeast pyridoxal 5-phosphate synthase Snz1. Biochem. J. 432, 445-450
14. Hanes, J. W., Burns, K. E., Hilmey, D. G., Chatterjee, A., Dorrestein, P. C. and Begley, T. P. (2008) Mechanistic studies on pyridoxal phosphate synthase: the reaction pathway leading to a chromophoric intermediate. J. Am. Chem. Soc. 130, 3043-3052 (Pubitemid 351455975)
15. Raschle, T., Arigoni, D., Brunisholz, R., Rechsteiner, H., Amrhein, N. and Fitzpatrick, T. B. (2007) Reaction mechanism of pyridoxal 5′-phosphate synthase: detection of an enzyme-bound chromophoric intermediate. J. Biol. Chem. 282, 6098-6105 (Pubitemid 47100844)
16. Guédez, G., Hipp, K., Windeisen, V., Derrer, B., Gengenbacher, M., Böttcher, B., Sinning, I., Kappes, B. and Tews, I. (2012) Assembly of the eukaryotic PLP-synthase complex from Plasmodium and activation of the Pdx1 enzyme. Structure 20, 172-184
17. Laskowski, R. A. (2001) PDBsum: summaries and analyses of PDB structures. Nucleic Acids Res. 29, 221-222
18. Laskowski, R. A. (2009) PDBsum new things. Nucleic Acids Res. 37, D355-D359
19. Irwin, J. J. and Shoichet, B. K. (2005) ZINC: a free database of commercially available compounds for virtual screening. J. Chem. Inf. Model. 45, 177-182 (Pubitemid 40736970)
20. Venkatachalam, C., Jiang, X., Oldfield, T. and Waldman, M. (2003) LigandFit: a novel method for the shape-directed rapid docking of ligands to protein active sites. J. Mol. Graphics Modell. 21, 289-307 (Pubitemid 35441326)
21. Mayo, S. L., Olafson, B. D. and Goddard, W. A. (1990) DREIDING: a generic force field for molecular simulations. J. Phys. Chem. 94, 8897-8909
22. Krammer, A., Kirchhoff, P. D., Jiang, X., Venkatachalam, C. and Waldman, M. (2005) LigScore: a novel scoring function for predicting binding affinities. J. Mol. Graphics Modell. 23, 395-407 (Pubitemid 40386869)
23. Humphrey, W., Dalke, A. and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graphics 14, 33-38 (Pubitemid 26152973)
24. Müller, I. B., Knöckel, J., Groves, M. R., Jordanova, R., Ealick, S. E., Walter, R. D. and Wrenger, C. (2008) The assembly of the plasmodial PLP synthase complex follows a defined course. PLoS ONE 3, 1-9
25. Knöckel, J., Jordanova, R., Müller, I. B., Wrenger, C. and Groves, M. R. (2009) Mobility of the conserved glycine 155 is required for formation of the active plasmodial dodecamer. Biochim. Biophys. Acta 1790, 347-350
26. Trager, W. and Jensen, J. B. (1976) Human malaria parasites in continuous culture. Science 193, 673-675
27. Das Gupta, R., Krause-Ihle, T., Bergmann, B., Müller, I. B., Khomutov, A. R., Müller, S., Walter, R. D. and Lüersen, K. (2005) 3-Aminooxy-1-aminopropane and derivatives have an antiproliferative effect on cultured Plasmodium falciparum by decreasing intracellular polyamine concentrations. Antimicrob. Agents Chemother. 49, 2857-2864 (Pubitemid 40917603)
28. Lambros, C. and Vanderberg, J. P. (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 3, 418-420 (Pubitemid 10222999)
29. Müller, I. B., Wu, F., Bergmann, B., Knöckel, J., Gehring, H., Walter, R. D. and Wrenger, C. (2009) Poisoning pyridoxal 5-phosphate dependent enzymes: a new strategy to target the malaria parasite Plasmodium falciparum. PLoS ONE 4, 1-9
30. Derrer, B., Windeisen, V., Guedez Rodriguez, G., Seidler, J., Gengenbacher, M., Lehmann, W. D., Rippe, K., Sinning, I., Tews, I. and Kappes, B. (2010) Defining the structural requirements of ribose 5-phosphate-binding and intersubunt cross-talk of the malarial pyridoxal 5-phosphate synthase. FEBS Lett. 584, 4169-4174
31. Zein, F., Zhang, Y., Kang, Y. N., Burns, K., Begley, T. P. and Ealick, S. E. (2006) Structural insights into the mechanism of the PLP synthase holoenzyme from Thermotoga maritima . Biochemistry 45, 14609-14620 (Pubitemid 44906977)
32. Burgos, E. and Salmon, L. (2004) Synthesis and evaluation of new 4-phospho-D-erythronic acid derivatives as competitive inhibitors of spinach ribose-5-phosphate isomerase. Tetrahedron Lett. 45, 753-756 (Pubitemid 38032695)
33. Christen, P. and Mehta, P. K. (2001) From cofactor to enzymes: the molecular evolution of pyridoxal-5′-phosphate-dependent enzymes. Chem. Rec. 1, 436-447 (Pubitemid 33771590)
34. 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. U.S.A. 96, 9374-9378 (Pubitemid 29374762)
35. Galperin, M. Y. and Koonin, E. V. (1997) Seqeunce analysis of an exceptionally conserved operon suggests enzymes for a new link between histidine and purine biosynthesis. Mol. Microbiol. 24, 443-445 (Pubitemid 27223873)
36. Woodruff, W. and Wolfenden, R. (1979) Inhibition of ribose-5-phosphate isomerase by 4-phosphoerythronate. J. Biol. Chem. 254, 5866
37. Backhausen, J. E., Jöstingmeyer, P. and Scheibe, R. (1997) Competitive inhibition of spinach leaf phosphoglucose isomerase isoenzymes by erythrose 4-phosphate. Plant Sci. 130, 121-131 (Pubitemid 28063314)
38. Chirgwin, J., Parsons, T. and Noltmann, E. (1975) Mechanistic implications of the pH independence of inhibition of phosphoglucose isomerase by neutral sugar phosphates. J. Biol. Chem. 250, 7277-7279
39. Ruijter, G. J. G. and Visser, J. (1999) Characterization of Aspergillus niger phosphoglucose isomerase: use for quantitative determination of erythrose 4-phosphate. Biochimie 81, 267-272
40. Jeffery, C. J., Bahnson, B. J., Chien, W., Ringe, D. and Petsko, G. A. (2000) Crystal structure of rabbit phosphoglucose isomerase, a glycolytic enzyme that moonlights as neuroleukin, autocrine motility factor, and differentiation mediator. Biochemistry 39, 955-964 (Pubitemid 30075322)
41. Burns, K. E., Xiang, Y., Kinsland, C. L., McLafferty, F. W. and Begley, T. P. (2005) Reconstitution and biochemical characterization of a new pyridoxal-5′-phosphate biosynthetic pathway. J. Am. Chem. Soc. 127, 3682-3683 (Pubitemid 40411393)
42. 6 biosynthesis: not that different after all. Biochem. J. 407, 1-13
43. Roberts, C. W., Roberts, F., Lyons, R. E., Kirisits, M. J., Mui, E. J., Finnerty, J., Johnson, J. J., Ferguson, D. J. P., Coggins, J. R., Krell, T. et al. (2002) The shikimate pathway and its branches in apicomplexan parasites. J. Infect. Dis. 185, S25-S36 (Pubitemid 34142826)
44. Bozdech, Z. and Ginsburg, H. (2005) Data mining of the transcriptome of Plasmodium falciparum: the pentose phosphate pathway and ancillary processes. Malaria J. 4, 17
45. Joshi, S., Singh, A. R., Kumar, A., Misra, P. C., Siddiqi, M. I. and Saxena, J. K. (2008) Molecular cloning and characterization of Plasmodium falciparum transketolase. Mol. Biochem. Parasitol. 160, 32-41 (Pubitemid 351694357)
46. Moccand, C., Kaufmann, M. and Fitzpatrick, T. B. (2011) It takes two to tango: defining an essential second active site in pyridoxal 5′-phosphate synthase. PLoS ONE 6, e16042
47. Raschle, T., Speziga, D., Kress, W., Moccand, C., Gehrig, P., Amrhein, N., Weber-Ban, E. and Fitzpatrick, T. B. (2009) Intersubunit cross-talk in pyridoxal 5′-phosphate synthase coordinated by the C terminus of the synthase subunit. J. Biol. Chem. 284, 7706-7718
48. Butzloff, S., Groves, M. R., Wrenger, C. and Müller, I. B. (2012) Cytometric quantification of singlet oxygen in the human malaria parasite Plasmodium falciparum. Cytometry, Part A 81, 698-703
49. Davis, A. M., Keeling, D. J., Steele, J., Tomkinson, N. P. and Tinker, A. C. (2005) Components of successful lead generation. Curr. Top. Med. Chem. 5, 421-439 (Pubitemid 40753878)
50. Zhao, H. (2007) Scaffold selection and scaffold hopping in lead generation: a medicinal chemistry perspective. Drug Discovery Today 12, 149-155
51. Oyakhirome, S., Issifou, S., Pongratz, P., Barondi, F., Ramharter, M., Kun, J. F., Missinou, M. A., Lell, B. and Kremsner, P. G. (2007) Randomized controlled trial of fosmidomycin-clindamycin versus sulfadoxine-pyrimethamine in the treatment of Plasmodium falciparum malaria. Antimicrob. Agents Chemother. 51, 1869-1871 (Pubitemid 46744177)
52. Borrmann, S., Issifou, S., Esser, G., Adegnika, A. A., Ramharter, M., Matsiegui, P.-B., Oyakhirome, S., Mboumba, D. P. M., Missinou, M. A., Kun, J. F. J. et al. (2004) Fosmidomycin-clindamycin for the treatment of Plasmodium falciparum malaria. J. Infect. Dis. 190, 1534-1540 (Pubitemid 39411000)