A potential target enzyme for trypanocidal drugs revealed by the crystal structure of NAD-dependent glycerol-3-phosphate dehydrogenase from Leishmania mexicana

Structure

Volumn 8, Issue 5, 2000, Pages 541-552

  Suresh, Stephen ^a   Turley, Stewart ^a   Opperdoes, Fred R ^b   Michels, Paul A M ^b   Hol, Wim G J ^a,c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b DE DUVE INSTITUTE   (Belgium)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Glycerol 3 phosphate dehydrogenase; Glycosome; Isomeroreductase; Leishmania mexicana; Trypanosomiasis

Indexed keywords

ANTITRYPANOSOMAL AGENT; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE;

AFRICAN TRYPANOSOMIASIS; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; DRUG TARGETING; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBUNIT; LEISHMANIA MEXICANA; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING;

LEISHMANIA MEXICANA; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 0034658406     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(00)00135-0     Document Type: Article

References (55)

1. WHO. (1997). Tropical Disease Research: Progress 1995-1996, Thirteenth Programme Report.
2. WHO. (1999). Tropical Disease Research: Progress 1997-1998, Fourteenth Programme Report.
3. Smith, D.H., Pepin, J. & Stich, A.H. (1998). Human African trypanosomiasis: an emerging public health crisis. Br. Med. Bull. 54, 341-355.
4. Moore, A., Richer, M., Enrile, M., Losio, E., Roberts, J. & Levy, D. (1999). Resurgence of sleeping sickness in Tambura County, Sudan. Am. J. Trop. Med. Hyg. 61, 315-318.
5. Alvar, J., et al., & Moreno, J. (1997). Leishmania and human immunodeficiency virus coinfection: the first 10 years. Clin. Microbiol. Rev. 10, 298-319.
6. Denise, H., Matthews, K., Lindergard, G., Croft, S. & Barrett, M.P. (1999). Trypanosomiasis and leishmaniasis: between the idea and and the reality of control. Parasitol. Today 15, 43-45.
7. Wang, C.C. (1995). Molecular mechanisms and therapeutic approaches to the treatment of African trypanosomiasis. Annu. Rev. Pharmacol. Toxicol. 35, 93-127.
8. Barrett, M.P. (1999). The fall and rise of sleeping sickness. Lancet 353, 1113-1114.
9. Barrett, M.P., Mottram, J.C. & Coombs, G.H. (1999). Recent advances in identifying and validating drug targets in trypanosomes and leishmanias. Trends Microbiol. 7, 82-88.
10. Tielens, A.G.M. & Van Hellemond, J.J. (1998). Differences in energy metabolism between trypanosomatidae. Parasitol. Today 14, 265-271.
11. Opperdoes, F.R. & Borst, P. (1977). Locliization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Lett. 80, 360-364.
12. Opperdoes, F.R. (1987). Compartmentation of carbohydrate metabolism in trypanosomes. Annu. Rev. Microbiol. 41, 127-151.
13. Hannaert, V. & Michels, P.A. (1994). Structure, function, and biogenesis of glycosomes in kinetoplastida. J. Bioenerg. Biomembr. 26, 205-212.
14. Bakker, B.M., Michels, P.A., Opperdoes, F.R. & Westerhoff, H.V. (1999). What controls glycolysis in bloodstream form Trypanosoma brucei? J. Biol. Chem. 274, 14551-14559.
15. Opperdoes, F.R. & Michels, P.A. (1993). The glycosomes of the kinetoplastida. Biochimie 75, 231-234.
16. Verlinde, C.L., et al., & Hol, W.G. (1994). Protein crystallography and infectious diseases. Protein Sci. 3, 1670-1686.
17. Bernstein, B.E., Michels, P.A. & Hol, W.G. (1997). Synergistic effects of substrate-induced conformational changes in phosphoglycerate kinase activation. Nature 385, 275-278.
18. Aronov, A.M., et al., & Gelb, M.H. (1999). Structure-based design of submicromolar, biologically active inhibitors of trypanosomatid glyceraldehyde-3-phosphate dehydrogenase. Proc. Natl Acad. Sci USA 96, 4273-4278.
19. Lo, T.W., Westwood, M.E., McLellan, A.C., Selwood, T. & Thornalley, P.J. (1994). Binding and modification of proteins by methylglyoxal under physiological conditions. A kinetic and mechanistic study with N α-acetylarginine, N α-acetylcysteine, and N α-actyllysine, and bovine serum albumin. J. Biol. Chem. 269, 32299-32305.
20. Denise, H., Giroud, C., Barrett, M.P. & Baltz, T. (1999). Affinity chromatography using trypanocidal arsenical drugs identifies a specific interaction between glycerol-3-phosphate dehydrogenase from Trypanosoma brucei and Cymelarsan. Eur. J. Biochem. 259, 339-346.
21. Kohl, L., et al., & Michels, P.A. (1996). Cloning and characterization of the NAD-linked glycerol-3-phosphate dehydrogenases of Trypanosoma brucei brucei and Leishmania mexicana mexicana and expression of the trypanosome enzyme in Escherichia coli. Mol. Biochem. Parasitol. 76, 159-173.
22. Marché, S., Michels, P.A.M. & Opperdoes, F.R. (2000). Comparative study of Leishmania mexicana and Trypanosoma brucei NAD dependent glycerol-3-phosphate dehydrogenase. Mol. Biochem. Parasitol. 106, 83-91.
23. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
24. Rossmann, M.G., Liljas, A., Brändén, C.-I. & Banaszak, L.J. (1975). Evolutionary and structural relationships among dehydrogenases. In The Enzymes. (Boyer, PD., ed.), Vol. XI Part A, pp. 61-102, Academic Press, New York.
25. Wierenga, R.K., Terpstra, P. & Hoi, W.G. (1986). Prediction of the occurrence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187, 101-107.
26. Carugo, O. & Argos, P. (1997). NADP-dependent enzymes. I: Conserved stereochemistry of cofactor binding. Proteins 28, 10-28.
27. Johansson, K., El-Ahmad, M., Ramaswamy, S., Hjelmqvist, L., Jornall, H. & Eklund, H. (1998). Structure of betaine aldehyde dehydrogenase at 2.1 Å resolution. Protein Sci. 7, 2106-2117.
28. Pidoux, A.L., Fawell, E.H. & Armstrong, J. (1990). Glycerol-3-phosphate dehydrogenase homologue from Schizosaccharomyces pombe. Nucleic Acids Res. 18, 7145.
29. Goodford, P.J. (1985). A computational procedure for determining energetically favorable binding sites on biologically important macromolecules. J. Med. Chem. 28, 849-857.
30. Stillman, T.J., Baker, P.J., Britton, K.L & Rice, D.W. (1993). Conformational flexibility in glutamate dehydrogenase. Role of water in substrate recognition and catalysis. J. Mol. Biol. 234, 1131-1139.
31. Stillman, T.J., et al., & Rice, D.W. (1999). Insights into the mechanism of domain closure and substrate specificity of glutamate dehydrogenase from Clostridium symbiosum. J. Mol. Biol. 285, 875-885.
32. Colonna-Cesari, F., Perahia, D., Karplus, M., Eklund, H., Brändén, C.I. & Tapia, O. (1986). Interdomain motion in liver alcohol dehydrogenase. Structural and energetic analysis of the hinge bending mode. J. Biol. Chem. 261, 15273-15280.
33. Skarzynski, T. & Wonacott, A.J. (1988). Coenzyme-induced conformational changes in glyceradehyde-3-phosphate dehydrogenase from Bacillus stearothermophilus. J. Mol. Biol. 203, 1097-1118.
34. Otto, J., Argos, P. & Rossmann, M.G. (1980). Prediction of secondary structural elements in glycerol-3-phosphate dehydrogenase by comparison with other dehydrogenases. Eur. J. Biochem. 109, 325-330.
35. Holm, L. & Sander, C. (1993). Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
36. Biou, V., Dumas, R., Cohen-Addad, C., Douce, R., Job, D. & Pebay-Peyroula, E. (1997). The crystal structure of plant acetohydroxy acid isomeroreductase complexed with NADPH, two magnesium ions and a herbicidal transition state analog determined at 1.65 Å resolution. EMBO J. 16, 3405-3415.
37. Redinbo, M.R., Stewart, L., Kuhn, P., Champoux, J.J. & Hol, W.G.J. (1998). Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279, 1504-1513.
38. Armah, D.A. & Mensa-Wilmot, K. (1999). S-myristoylation of a glycosylphosphatidylinositol-specific phospholipase C in Trypanosoma brucei. J. Biol. Chem. 274, 5931-5938.
39. Armah, D.A. & Mensa-Wilmot, K. (1999). Protein S-myristoylation in Leishmania revealed with a heterologous reporter. Biochem. Biophys. Res. Commun. 256, 569-572.
40. Godsel, L.M. & Engman, D.M. (1999). Flagellar protein localization mediated by a calcium-myristoyl/palmitoyl switch mechanism. EMBO J. 18, 2057-2065.
41. +-dependent glycerol 3-phosphate dehydrogenase from Trypanosoma brucei rhodesiense. Mol. Biochem. Parasitol. 76, 145-158.
42. Fairlamb, A.H. & Bowman, I.B. (1980). Uptake of the trypanocidal drug suramin by bloodstream forms of Trypanosoma brucei and its effect on respiration and growth rate in vivo. Mol. Biochem. Parasitol. 1, 315-333.
43. Willson, M., Callens, M., Kuntz, D.A., Perie, J. & Opperdoes, F.R. (1993). Synthesis and activity of inhibitors highly specific for the glycolytic enzymes from Trypanosoma brucei. Mol. Biochem. Parasitol. 59, 201-210.
44. de la Fortelle, E. & Bricogne, G. (1997). Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. In Methods in Enzymology. (Carter, C.W.J. & Sweet, R.M., eds), Vol. 276, pp. 472-494, Academic Press, San Diego.
45. Perrakis, A., Sixma, T.K., Wilson, K.S. & Lamzin, V.S. (1997). wARP: Improvement and extension of crystallographic phases by weighted averaging of multiple refined dummy atomic models. Acta Crystallogr. D 53, 448-455.
46. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119.
47. Brünger, AT. (1988). X-PLOR Manual, Version 3.1, Yale University, New Haven, CT.
48. Tronrud, D.E., Ten Eyck, L.F. & Matthews, B.W. (1987). An efficient general-purpose least-squares refinement program for macromolecular structures. Acta Crystallogr. A 43, 489-501.
49. Brünger, A.T., et al., & Warren, G.L. (1998). Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921.
50. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
51. Merritt, E.A. & Murphy, M.E.P. (1994). Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. D 50, 869-873.
52. Esnouf, R.M. (1997). An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J. Mol. Graph. 15, 133-138.
53. Brünger, AT, Krukowski, A. & Erickson, J.W. (1990). Slow-cooling protocols for crystallographic refinement by simulated annealing. Acta Crystallogr. A 46, 585-593.
54. Wallace, A.C., Laskowski, R.A. & Thornton, J.M. (1995). LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8, 127-134.
55. Nicholls, A., Shar, K.A. & Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 282-296.