Anopheles gambiae purine nucleoside phosphorylase: Catalysis, structure, and inhibition

Biochemistry

Volumn 46, Issue 43, 2007, Pages 12405-12415

  Taylor, Erika A ^a,b   Rinaldo Matthis, Agnes ^a   Li, Lei ^a   Ghanem, Mahmoud ^a   Hazleton, Keith Z ^a   Cassera, María B ^a   Almo, Steven C ^a   Schramm, Vern L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b WESLEYAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CRYSTAL STRUCTURE; DISEASES; ESCHERICHIA COLI; GENES; POSITIVE IONS;

GUANOSINE; PURINE AUXOTROPHS; PURINE NUCLEOSIDE PHOSPHORYLASE (PNP); SEQUENCE HOMOLOGY;

ENZYME INHIBITION;

DEOXYINOSINE; GUANOSINE; INOSINE; PURINE NUCLEOSIDE PHOSPHORYLASE;

ANOPHELES GAMBIAE; ARTICLE; CATALYSIS; CHEMICAL BOND; DISSOCIATION CONSTANT; ENZYME INHIBITION; ENZYME INHIBITOR INTERACTION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; ESCHERICHIA COLI; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPECIES COMPARISON;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; KINETICS; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PURINE-NUCLEOSIDE PHOSPHORYLASE; SEQUENCE HOMOLOGY, AMINO ACID;

ANOPHELES GAMBIAE; ESCHERICHIA COLI; HOMO SAPIENS; PLASMODIUM FALCIPARUM;

EID: 35649003770     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7010256     Document Type: Article

References (41)

1. Gilles, H. M. (2002) in Essential Malariology (Warrell, D. A., and Gilles, H. M., Eds.) pp 1-7, Arnold, New York.
2. World Health Organization (2007) Malaria, Fact Sheet No. 94, Geneva, Switzerland.
3. Sachs, J. D., and Malaney, P. (2002) The economic and social burden of malaria, Nature 415, 680-685.
4. Sachs, J. D. (2002) A new global effort to control malaria, Science 298, 122-124.
5. Wellems, T. E. (2002) Plasmodium chloroquine resistance and the search for a replacement antimalarial drug, Science 298, 124-125.
6. Sherman, I. W. (1998) in Parasite Biology, pathogenesis and protection (Sherman, I. W., Ed.) pp 89-117, ASM Press, Washington, DC.
7. Stoeckler, J. D. (1984) Purine nucleoside Phosphorylase: A target for chemotherapy, in Development in Cancer Chemotherapy (Glazer, R. I., Ed.) pp 35-60, CRC Press, Inc., Boca Raton, FL.
8. de Koning, H. P., Bridges, D. J., and Burchmore, R. J. S. (2005) Purine and pyrimidine transport in pathogenic protozoa: From biology to therapy, FEMS Microbiol. Rev. 29, 987-1020.
9. Kicska, G. A., Tyler, P. C., Evans, G. B., Furneaux, R. H., Schramm, V. L., and Kim, K. (2002) Purine-less death in Plasmodium falciparum induced by Immucillin-H, a transition state analogue of purine nucleoside Phosphorylase, J. Biol. Chem. 277, 3226-3231.
10. Ting, L. M., Shi, W., Lewandowicz, A., Singh, V., Mwakingwe, A., Birck, M. R., Taylor, Ringia, E. A., Bench, G., Madrid, D. C., Tyler, P. C., Evans, G. B., Furneaux, R. H., Schramm, V. L., and Kim, K. (2005) Targeting a novel Plasmodium falciparum purine recycling pathway with specific immucillins, J. Biol. Chem. 280, 9547-9554.
11. Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., Wincker, P., Clark, A. G., Ribeiro, J. M. C., Wides, R., Salzberg, S. L., Loftus, B., Yandell, M., Majoras, W. H., Rusch, D. B., Lai, Z., Kraft, C. L., Abril, J. F., Anthouard, V., Arensburger, P., Atkinson, P. W., Baden, H., de Berardinis, V., Baldwin, D., Benes, V., Biedler, J., Blass, C., Bolanos, R., Boscus, D., Barnstead, M., Cai, S., Center, A., Chatuverdi, K., Christophides, G. K., Chrystal, M. A., Clamp, M., Cravchik, A., Curwen, V., Dana, A., Delcher, A., Dew, I., Evans, C. A., Flanigan, M., Grundschober- Freimoser, A., Friedli, L., Gu, Z., Guan, P., Guigo, R., Hillenmeyer, M. E., Hladun, S. L., Hogan, J. R., Hong, Y. S., Hoover, J., Jaillon, O., Ke, Z., Kodira, C., Kokoza, E., Koutsos, A., Letunic, I., Levitsky, A., Liang, Y., Lin, J.-J., Lobo, N. F., Lopez, J. R., Malek, J. A., McIntosh, T. C., Meister, S., Miller, J., Mobarry, C., Mongin, E., Murphy, S. D., O'Brochta, D. A., Pfannkoch, C., Qi, R., Regier, M. A., Remington, K., Shao, H., Sharakhova, M. V., Sitter, C. D., Shetty, J., Smith, T. J., Strong, R., Sun, J., Thomasova, D., Ton, L. Q., Topalis, P., Tu, Z., Unger, M. F., Walenz, B., Wang, A., Wang, J., Wang, M., Wang, X., Woodford, K. J., Wormian, J. R., Wu, M., Yao, A., Zdobnov, E. M., Zhang, H., Zhao, Q., Zhao, S., Zhu, S. C., Zhimulev, I., Coluzzi, M., della Torre, A., Roth, C. W., Louis, C., Kalush, F., Mural, R. J., Myers, E. W., Adams, M. D., Smith, H. O., Broder, S., Gardner, M. J., Fraser, C. M., Birney, E., Bork, P., Brey, P. T., Venter, J. C., Weissenbach, J., Kafatos, F. C., Collins, F. H., and Hoffman, S. L. (2002) The genome sequence of the malaria mosquito Anopheles gambiae, Science 298, 129-149.
12. Kaufman, T. C., Severson, D. W., and Robinson, G. E. (2002) The Anopheles genome and comparative insect genomics, Science 298, 97-98.
13. Lewandowicz, A., Taylor Ringia, E. A., Ting, L. M., Kim, K., Tyler, P. C., Evans, G. B., Zubkova, O. V., Mee, S., Painter, G. F., Lenz, D. H., Furneaux, R. H., and Schramm, V. L. (2005) Energetic mapping of transition state analogue interactions with human and Plasmodium falciparum purine nucleoside phosphorylases, J. Biol. Chem. 280, 30320-30328.
14. Extinction coefficients were determined by use of the Protparam tool (www.expasy.org/tools/protparam/html).
15. Miles, R. W., Tyler, P. C., Furneaux, R. H., Bagdassarian, C. K., and Schramm, V. L. (1998) One-third-the-sites transition-state inhibitors for purine nucleoside Phosphorylase, Biochemistry 37, 8615-8621.
16. Singh, V., Evans, G. B., Lenz, D. H., Mason, J. M., Clinch, K., Mee, S., Painter, G. F., Tyler, P. C., Furneaux, R. H., Lee, J. E., Howell, P. L., and Schramm, V. L. (2005) Femtomolar transition state analogue inhibitors of 5′-methylthioadenosine/S-adenosylhomocysteine nucleosidase from Escherichia coli, J. Biol. Chem. 280, 18265-18273.
17. Kicska, G. A., Tyler, P. C., Evans, G. B., Furneaux, R. H., Kim, K., and Schramm, V. L. (2002) Transition state analogue inhibitors of purine nucleoside Phosphorylase from Plasmodium falciparum, J. Biol. Chem. 277, 3219-3225.
18. Merkler, D. J., Brenowitz, M., and Schramm, V. L. (1990) The rate constant describing slow-onset inhibition of yeast AMP deaminase by coformycin analogs is independent of inhibitor structure, Biochemistry 29, 8358-8364.
19. Singh, V., Shi, W., Evans, G. B., Tyler, P. C., Furneaux, R. H., Almo, S. C., and Schramm, V. L. (2004) Picomolar transition state analogue inhibitors of human 5′-methylthioadenosine Phosphorylase and X-ray structure with MT-Immucillin-A, Biochemistry 43, 9-18.
20. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
21. Read, R. J. (2001) Pushing the boundaries of molecular replacement with maximum likelihood, Acta Crystallogr. D57, 1373-1382.
22. Storoni, L. C., McCoy, A. J., and Read, R. J. (2004) Likelihood enhanced fast rotation functions, Acta Crystallogr. D59, 1145-1153.
23. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr. D53, 240-255.
24. Potterton, E., Briggs, P., Turkenburg, M., and Dodson, E. J. (2003) A graphical user interface to the CCP4 program suite, Acta Crystallogr. D59, 1131-1137.
25. Lamzin, V. S., and Wilson, K. S. (1993) Automated refinement of protein models, Acta Crystallogr. D49, 129-147.
26. Emsley, P., and Cowtan, K. (2004) Model-building tools for molecular graphics, Acta Cryst. D60, 2126-2132.
27. DeLano, W. L. (2002) The PyMOL molecular graphics system, San Carlos, CA.
28. Clements, A. N. (1992) The biology of mosquitoes, Vol. 1, Chapman and Hall, New York.
29. Rinaldo-Matthis, A., Wing, C., Ghanem, M., Deng, H., Wu, P., Gupta, A., Tyler, P. C., Evans, G. B., Furneaux, R. H., Almo, S. C., Wang, C. C., and Schramm, V. L. (2007) Inhibition and structure of Trichomonas vaginalis purine nucleoside phosphorylase with picomolar transition state analogues, Biochemistry 46, 659-668.
30. Barsacchi, D., Cappiello, M., Tozzi, M. G., Del, Corso, A., Peccatori, M., Camici, M., Ipata, P. L., and Mura, U. (1992) Purine nucleoside Phosphorylase from bovine lens: purification and properties, Biochim. Biophys. Acta 1160, 163-170.
31. Stoeckler, J. D., Cambor, C., and Parks, R. E. (1980) Human erythrocytic purine nucleoside phosphorylase: Reaction with sugar-modified nucleoside substrates, Biochemistry 19, 102-107.
32. Bzowska, A., Kulikowskaa, E., and Shugar, D. (2000) Purine nucleoside phosphorylases: properties, functions, and clinical aspects, Pharmacol. Ther. 88, 349-425.
33. Erion, M. D., Takabayashi, K., Smith, H. B., Kessi, J., Wagner, S., Hoenger, S., Shames, S. L., and Ealick, S. E. (1997) Purine nucleoside Phosphorylase. 1. Structure-function studies, Biochemistry 36, 11725-11734.
34. Schramm, V. L. (1998) Enzymatic transition states and transition state analog design, Annu. Rev. Biochem. 67, 693-720.
35. Bzowska, A. (2002) Calf spleen purine nucleoside phosphorylase: complex kinetic mechanism, hydrolysis of 7-methylguanosine, and oligomeric state in solution, Biochim. Biophys. Acta 1596, 293-317.
36. Kline, P. C., and Schramm, V. L. (1993) Purine nucleoside Phosphorylase. Catalytic mechanism and transition-state analysis of the arsenolysis reaction, Biochemistry 32, 13212-13219.
37. Taylor, E. A., Clinch, K., Kelly, P. M., Li, L., Evans, G. B., Tyler, P. C., and Schramm, V. L. (2007) Acyclic ribooxacarbenium ion mimics as transition state analogues of human and malarial purine nucleoside phosphorylases, J. Am. Chem. Soc. 129, 2985-2987.
38. Taylor Ringia, E. A., Tyler, P. C., Evans, G. B., Furneaux, R. H., Murkin, A. S., and Schramm, V. L. (2006) Transition state analogue discrimination by related purine nucleoside phosphorylases, J. Am. Chem. Soc. 128, 7126-7127.
39. Cruickshank, D. W. (1999) Remarks about protein structure precision, Acta Crystallogr. D55, 583-601.
40. Fedorov, A., Shi, W., Kicska, G., Fedorov, E., Tyler, P. C., Furneaux, R. H., Hanson, J. C., Gainsford, G. J., Larese, J. Z., Schramm, V. L., and Almo, S. C. (2001) Transition State Structure of Purine Nucleoside Phosphorylase and Principles of Atomic Motion in Enzymatic Catalysis, Biochemistry 40, 853-860.
41. Schramm, V. L. (2003) Enzymatic transition state poise and transition state analogues, Acc. Chem. Res. 36, 588-596.