Structural insights into the activation of P. vivax plasmepsin

Journal of Molecular Biology

Volumn 329, Issue 3, 2003, Pages 505-524

  Bernstein, Nina Khazanovich ^a   Cherney, Maia M ^a   Yowell, Charles A ^b   Dame, John B ^b   James, Michael N G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b University of Florida College of Veterinary Medicine   (United States)

Author keywords

Crystallography; Malaria; Plasmepsin; Proplasmepsin; Proteinase

Indexed keywords

AMINO ACID; ANTIMALARIAL AGENT; ASPARTIC PROTEINASE; ENZYME PRECURSOR; HEMOGLOBIN; HISTO ASPARTIC PROTEASE; PLASMEPSIN I; PLASMEPSIN II; PLASMEPSIN IV; PROPLASMEPSIN; PROPLASMEPSIN II; PROTEINASE; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; AMINO TERMINAL SEQUENCE; ARTICLE; BIOCHEMISTRY; CRYSTAL STRUCTURE; DRUG DESIGN; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME INACTIVATION; ENZYME STRUCTURE; ENZYME SYNTHESIS; MALARIA; PLANT; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PROCESSING; STRUCTURE ANALYSIS;

EID: 0038630491     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00444-3     Document Type: Article

References (52)

1. Francis S.E., Banerjee R., Goldberg D.E. Biosynthesis and maturation of the malaria aspartic hemoglobinases plasmepsins I and II. J. Biol. Chem. 272:1997;14961-14968.
2. Goldberg D.E., Slater A.F., Cerami A., Henderson G.B. Hemoglobin degradation in the malaria parasite Plasmodium falciparum: an ordered process in a unique organelle. Proc. Natl Acad. Sci. USA. 87:1990;2931-2935.
3. Olliaro P.L., Goldberg D.E. The Plasmodium digestive vacuole: metabolic headquarters and choice drug target. Parasitol. Today. 11:1995;294-297.
4. Goldberg D.E., Slater A.F., Beavis R., Chait B., Cerami A., Henderson G.B. Hemoglobin degradation in the human malaria pathogen Plasmodium falciparum: a catabolic pathway initiated by a specific aspartic protease. J. Exp. Med. 173:1991;961-969.
5. Francis S.E., Gluzman I.Y., Oksman A., Knickerbocker A., Mueller R., Bryant M.L., et al. Molecular characterization and inhibition of a Plasmodium falciparum aspartic hemoglobinase. EMBO J. 13:1994;306-317.
6. Gluzman I.Y., Francis S.E., Oksman A., Smith C.E., Duffin K.L., Goldberg D.E. Order and specificity of the Plasmodium falciparum hemoglobin pathway. J. Clin. Invest. 93:1994;1602-1608.
7. Salas F., Fichmann J., Lee G.K., Scott M.D., Rosenthal P.J. Functional expression of falcipain, a Plasmodium falciparum cysteine proteinase, its role as a malarial hemoglobinase. Infect. Immun. 63:1995;2120-2125.
8. Francis S.E., Gluzman I.Y., Oksman A., Banerjee D., Goldberg D.E. Characterization of native falcipain, an enzyme involved in Plasmodium falciparum hemoglobin degradation. Mol. Biochem. Parasitol. 83:1996;189-200.
9. Eggleson K.K., Duffin K.L., Goldberg D.E. Identification and characterization of falcilysin, a metallopeptidase in hemoglobin catabolism within the malaria parasite Plasmodium falciparum. J. Biol. Chem. 274:1999;32411-32417.
10. Banerjee R., Liu J., Beatty W., Pelosof L., Klemba M., Goldberg D.E. Four plasmepsins are active in the Plasmodium falciparum food vacuole, including a protease with an active-site histidine. Proc. Natl Acad. Sci. USA. 99:2002;990-995.
11. Shenai B.R., Sijwali P.S., Singh A., Rosenthal P.J. Characterization of native and recombinant falcipain-2, a principal trophozoite cysteine protease and essential hemoglobinase of Plasmodium falciparum. J. Biol. Chem. 275:2000;29000-29010.
12. Sijwali P.S., Shenai B.R., Gut J., Singh A., Rosenthal P.J. Expression and characterization of the Plasmodium falciparum haemoglobinase falcipain-3. Biochem. J. 360:2001;481-489.
13. Dame J. Additional plasmepsins. Barrett A.J., Rawlings N.D., Woessner F.J. Handbook of Proteolytic Enzymes. 1996;862-864 Academic Press, London.
14. Humphreys M.J., Moon R.P., Klinder A., Fowler S.D., Rupp K., Bur D., et al. The aspartic proteinase from the rodent parasite Plasmodium berghei as a potential model for plasmepsins from the human malaria parasite, Plasmodium falciparum. FEBS Letters. 463:1999;43-48.
15. Le Bonniec S., Deregnaucourt C., Redeker V., Banerjee R., Grellier P., Goldberg D.E., Schrevel J. Plasmepsin II an acidic hemoglobinase from the Plasmodium falciparum. J. Biol. Chem. 274:1999;14218-14223.
16. Wyatt D.M., Berry C. Activity and inhibition of plasmepsin IV, a new aspartic proteinase from the malaria parasite, Plasmodium falciparum. FEBS Letters. 513:2002;159-162.
17. Hill J., Tyas L., Phylip L.H., Kay J., Dunn B.M., Berry C. High level expression and characterisation of Plasmepsin II, an aspartic proteinase from Plasmodium falciparum. FEBS Letters. 352:1994;155-158.
18. Westling J., Yowell C.A., Majer P., Erickson J.W., Dame J.B., Dunn B.M. Plasmodium falciparum, P. vivax, and P. malariae: a comparison of the active site properties of plasmepsins cloned and expressed from three different species of the malaria parasite. Exp. Parasitol. 87:1997;185-193.
19. Silva A.M., Lee A.Y., Gulnik S.V., Maier P., Collins J., Bhat T.N., et al. Structure and inhibition of plasmepsin II, a hemoglobin-degrading enzyme from Plasmodium falciparum. Proc. Natl Acad. Sci. USA. 93:1996;10034-10039.
20. Bernstein N.K., Cherney M.M., Loetscher H., Ridley R.G., James M.N.G. Crystal structure of the novel aspartic proteinase zymogen proplasmepsin II from Plasmodium falciparum. Nature Struct. Biol. 6:1999;32-37.
21. Pearl L., Blundell T. The active site of aspartic proteinases. FEBS Letters. 174:1984;96-101.
22. Sielecki A.R., Fujinaga M., Read R.J., James M.N.G. Refined structure of porcine pepsinogen at 1.8 Å resolution. J. Mol. Biol. 219:1991;671-692.
23. Beveridge A. A theoretical study of torsional flexibility in the active site of aspartic proteinases: implications for catalysis. Proteins: Struct. Funct. Genet. 24:1996;322-334.
24. Coombs G.H., Goldberg D.E., Klemba M., Berry C., Kay J., Mottram J.C. Aspartic proteases of Plasmodium falciparum and other parasitic protozoa as drug targets. Trends Parasitol. 17:2001;532-537.
25. Westling J., Cipullo P., Hung S.H., Saft H., Dame J.B., Dunn B.M. Active site specificity of plasmepsin II. Protein Sci. 8:1999;2001-2009.
26. Umezawa H., Aoyagi T., Morishima H., Matsuzaki M., Hamada M. Pepstatin, a new pepsin inhibitor produced by Actinomycetes. J. Antibiot. (Tokyo). 23:1970;259-262.
27. Read R.J., Fujinaga M., Sielecki A.R., James M.N.G. Structure of the complex of Streptomyces griseus protease B and the third domain of the turkey ovomucoid inhibitor at 1.8 Å resolution. Biochemistry. 22:1983;4420-4433.
28. Berry C., Humphreys M.J., Matharu P., Granger R., Horrocks P., Moon R.P., et al. A distinct member of the aspartic proteinase gene family from the human malaria parasite Plasmodium falciparum. FEBS Letters. 447:1999;149-154.
29. Wyatt D.M., Berry C. Activity and inhibition of plasmepsin IV, a new aspartic proteinase from the malaria parasite, Plasmodium falciparum. FEBS Letters. 513:2002;159-162.
30. Andreeva N.S., Rumsh L.D. Analysis of crystal structures of aspartic proteinases: on the role of amino acid residues adjacent to the catalytic site of pepsin-like enzymes. Protein Sci. 10:2001;2439-2450.
31. James M.N.G., Sielecki A.R. Molecular structure of an aspartic proteinase zymogen, porcine pepsinogen, at 1.8 Å resolution. Nature. 319:1986;33-38.
32. Hartsuck J.A., Koelsch G., Remington S.J. The high-resolution crystal structure of porcine pepsinogen. Proteins: Struct. Funct. Genet. 13:1992;1-25.
33. Moore S.A., Sielecki A.R., Chernaia M.M., Tarasova N.I., James M.N.G. Crystal and molecular structures of human progastricsin at 1.62 Å resolution. J. Mol. Biol. 247:1995;466-485.
34. Khan A.R., Cherney M.M., Tarasova N.I., James M.N.G. Structural characterization of activation 'intermediate 2' on the pathway to human gastricsin. Nature Struct. Biol. 4:1997;1010-1015.
35. Bateman K.S., Chernaia M.M., Tarasova N.I., James M.N.G. Crystal structure of human pepsinogen A. Advan. Exp. Med. Biol. 436:1998;259-263.
36. Kervinen J., Tobin G.J., Costa J., Waugh D.S., Wlodawer A., Zdanov A. Crystal structure of plant aspartic proteinase prophytepsin: inactivation and vacuolar targeting. EMBO J. 18:1999;3947-3955.
37. Carcache D.A., Hortner S.R., Bertogg A., Binkert C., Bur D., Marki H.P., et al. De novo design, synthesis, and in vitro evaluation of a new class of non-peptidic inhibitors of the malarial enzyme plasmepsin II. ChemBiochem. 3:2002;1137-1141.
38. Oefner C., Binggeli A., Breu V., Bur D., Clozel J.P., D'Arcy A., et al. Renin inhibition by substituted piperidines: a novel paradigm for the inhibition of monomeric aspartic proteinases? Chem. Biol. 6:1999;127-131.
39. Vieira E., Binggeli A., Breu V., Bur D., Fischli W., Guller R., et al. Substituted piperidines - highly potent renin inhibitors due to induced fit adaptation of the active site. Bioorg. Med. Chem. Letters. 9:1999;1397-1402.
40. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 33:1968;491-497.
41. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Carter C.W. Jr, Sweet R. Methods in Enzymology. vol. 276:1996;307-326 Academic Press, London.
42. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163.
43. Jones T.A., Kjeldgaard M. O the Manual, Version 5.11. 1995;. Uppsala, Sweden.
44. Brunger A.T. XPLOR: a System for X-ray Crystallography and NMR. 1993;Yale University Press, New Haven, Connecticut.
45. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta. Crystallog. sect. D, Biol. Crystallog. 54:1998;905-921.
46. Pannu N.S., Read R.J. Improved structure refinement through maximum likelihood. Acta Crystallog. sect. A. 52:1996;659-668.
47. Winn M.D., Isupov M.N., Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta. Crystallog. sect. D, Biol. Crystallog. 57:2001;122-133.
48. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
49. Brunger A.T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 355:1992;472-475.
50. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
51. Esnouf R.M. An extensively modified version of MolScript that includes greatly enhanced colouring capabilities. J. Mol. Graph. 15:1997;133-138.
52. Merritt E.A., Murphy M.E.P. Raster3D version 2.0: a program for photorealistic molecular graphics. Acta Crystallog. sect. D. 50:1994;869-873.