Recombinant plasmepsin 1 from the human malaria parasite Plasmodium falciparum: Enzymatic characterization, active site inhibitor design, and structural analysis

Biochemistry

Volumn 48, Issue 19, 2009, Pages 4086-4099

  Liu, Peng ^a,d,e   Marzahn, Melissa R ^a   Robbins, Arthur H ^a   Gutiéerrez de Terán, Hugo ^b   Rodríguez, David ^b   McClung, Scott H ^a   Stevens Jr , Stanley M ^a   Yowell, Charles A ^c   Dame, John B ^c   McKenna, Robert ^a   Dunn, Ben M ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

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

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e MMC 295 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; BINDING AFFINITIES; CATHEPSIN D; COMBINATORIAL CHEMISTRY; HUMAN MALARIA PARASITE; INHIBITOR DESIGN; MODELING STUDIES; NATURALLY OCCURRING; PEPTIDE LIBRARY; PEPTIDE SUBSTRATES; PEPTIDOMIMETIC; PLASMEPSINS; PLASMODIUM FALCIPARUM;

AMINES; BINDING ENERGY; BIOASSAY; BIOCHIPS; ESCHERICHIA COLI; STRUCTURAL ANALYSIS;

CRYSTAL STRUCTURE;

CATHEPSIN D; PEPTIDE LIBRARY; PEPTIDOMIMETIC AGENT; PLASMEPSIN I;

ARTICLE; BINDING AFFINITY; CATALYSIS; COMBINATORIAL CHEMISTRY; CRYSTAL STRUCTURE; DRUG PROTEIN BINDING; ENZYME ANALYSIS; ESCHERICHIA COLI; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; PH MEASUREMENT; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN ISOLATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; STRUCTURE ANALYSIS; X RAY DIFFRACTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ASPARTIC ENDOPEPTIDASES; BINDING SITES; CATALYSIS; ENZYME INHIBITORS; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MALARIA, FALCIPARUM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PLASMODIUM FALCIPARUM; PROTEIN RENATURATION; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SOLUBILITY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI; PLASMODIUM FALCIPARUM;

EID: 66049110565     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi802059r     Document Type: Article

References (49)

1. Schechter, I., and Berger, A. (1967) On the size of the active site in proteases I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
2. Coombs, G. H., Goldberg, D. E., Klemba, M., Berry, C., Kay, J., and Mottram, J. C. (2001) Aspartic proteases of Plasmodium falciparum and other parasitic protozoa as drug targets. Trends Parasitol. 17, 532-537. (Pubitemid 34185360)
3. Goldberg, D. E., Slater, A. F., Beavis, R., Chait, B., Cerami, A., and Henderson, G. B. (1991) Hemoglobin degradation in the human malaria pathogen Plasmodium falciparum: a catabolic pathway initiated by a specific aspartic protease. J. Exp. Med. 173, 961-969.
4. Francis, S. E., Gluzman, I. Y., Oksman, A., Knickerbocker, A., Mueller, R., Bryant, M. L., Sherman, D. R., Russell, D. G., and Goldberg, D. E. (1994) Molecular characterization and inhibition of a plasmodium-falciparum aspartic hemoglobinase. EMBO J. 13, 306-317. (Pubitemid 24034212)
5. Dame, J. B., Reddy, G. R., Yowell, C. A., Dunn, B. M., Kay, J., and Berry, C. (1994) Sequence, expression and modeled structure of an aspartic proteinase from the human malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 64, 177-190.
6. Banerjee, R., Liu, J., Beatty, W., Pelosof, L., Klemba, M., and Goldberg, D. E. (2002) Four plasmepsins are active in the Plasmodium falciparum food vacuole, including a protease with an active-site histidine. Proc. Natl. Acad. Sci. U. S. A. 99, 990-995.
7. Dame, J. B., Yowell, C. A., Omara-Opyene, L., Carlton, J. M., Cooper, R. A., and Li, T. (2003) Plasmepsin 4, the food vacuole aspartic proteinase found in all Plasmodium spp. infecting man. Mol. Biochem. Parasitol. 130, 1-12.
8. Asojo, O. A., Afonina, E., Gulnik, S. V., Yu, B., Erickson, J. W., Randad, R., Medjahed, D., and Silva, A. M. (2002) Structures of Ser205 mutant plasmepsin II from Plasmodium falciparum at 1.8 angstrom in complex with the inhibitors rs367 and rs370. Acta Crystallogr. Sect. D 58, 2001-2008. (Pubitemid 35450821)
9. Asojo, O. A., Gulnik, S. V., Afonina, E., Yu, B., Ellman, J. A., Haque, T. S., and Silva, A. M. (2003) Novel uncomplexed and complexed structures of plasmepsin II, an aspartic protease from Plasmodium falciparum. J. Mol. Biol. 327, 173-181.
10. Clemente, J. C., Govindasamy, L., Madabushi, A., Fisher, S. Z., Moose, R. E., Yowell, C. A., Hidaka, K., Kimura, T., Hayashi, Y., Kiso, Y., Agbandje-McKenna, M., Dame, J. B., Dunn, B. M., and McKenna, R. (2006) Structure of the aspartic protease plasmepsin 4 from the malarial parasite Plasmodium malariae bound to an allophenylnorstatine-based inhibitor. Acta Crystallogr. Sect. D 62, 246-252. (Pubitemid 44185133)
11. Silva, A. M., Lee, A. Y., Gulnik, S. V., Maier, P., Collins, J., Bhat, T. N., Collins, P. J., Cachau, R. E., Luker, K. E., Gluzman, I. Y., Francis, S. E., Oksman, A., Goldberg, D. E., and Erickson, J. W. (1996) Structure and inhibition of plasmepsin II, a hemoglobin-degrading enzyme from Plasmodium falciparum. Proc. Natl. Acad. Sci. U. S. A. 93, 10034-10039.
12. Francis, S. E., Banerjee, R., and Goldberg, D. E. (1997) Biosynthesis and maturation of the malaria aspartic hemoglobinases plasmepsins I and II. J. Biol. Chem. 272, 14961-14968. (Pubitemid 27251770)
13. Bailly, E., Jambou, R., Savel, J., and Jaureguiberry, G. (1992) Plasmodium falciparum: differential sensitivity in vitro to E-64 (cysteine protease inhibitor) and Pepstatin A (aspartyl protease inhibitor). J. Protozool. 39, 593-599.
14. Moon, R. P., Tyas, L., Certa, U., Rupp, K., Bur, D., Jacquet, C., Matile, H., Loetscher, H., Grueninger-Leitch, F., Kay, J., Dunn, B. M., Berry, C., and Ridley, R. G. (1997) Expression and characterisation of plasmepsin I from Plasmodium falciparum. Eur. J. Biochem. 244, 552-560. (Pubitemid 27110759)
15. Beyer, B. B., Johnson, J. V., Chung, A. Y., Li, T., Madabushi, A., Agbandje-McKenna, M., McKenna, R., Dame, J. B., and Dunn, B. M. (2005) Active-site specificity of digestive aspartic peptidases from the four species of Plasmodium that infect humans using chromogenic combinatorial peptide libraries. Biochemistry 44, 1768-1779. (Pubitemid 40227471)
16. Hill, J., Tyas, L., Phylip, L. H., Kay, J., Dunn, B. M., and Berry, C. (1994) High level expression and characterisation of Plasmepsin II, an aspartic proteinase from Plasmodium falciparum. FEBS Lett. 352, 155-158.
17. Wyatt, D. M., and Berry, C. (2002) Activity and inhibition of plasmepsin IV, a new aspartic proteinase from the malaria parasite, Plasmodium falciparum. FEBS Lett. 513, 159-162. (Pubitemid 34251256)
18. Westling, J., Yowell, C. A., Majer, P., Erickson, J. W., Dame, J. B., and Dunn, B. M. (1997) 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, 185-193.
19. Scarborough, P. E., Guruprasad, K., Topham, C., Richo, G. R., Conner, G. E., Blundell, T. L., and Dunn, B. M. (1993) Exploration of subsite binding-specificity of human cathepsin-D through kinetics and rule-based molecular modeling. Protein Sci. 2, 264-276. (Pubitemid 23045479)
20. Beyer, B. M., and Dunn, B. M. (1998) Prime region subsite specificity characterization of human cathepsin D: The dominant role of position 128. Protein Sci. 7, 88-95.
21. Dunn, B. M., Scarborough, P. E., Davenport, R., and Swietnicki, W. (1994) Analysis of proteinase specificity by studies of peptide substrates: The use of UV and fluorescence spectroscopy to quantitate rates of enzymatic cleavage, in Peptide Analysis Protocols (Dunn, B. M., and Pennington, M. W., Eds.), pp 225-243, Humana Press, Totowa.
22. Goldfarb, N. E., Lam, M. T., Bose, A. K., Patel, A. M., Duckworth, A. J., and Dunn, B. M. (2005) Electrostatic switches that mediate the pH-dependent conformational change of "short" recombinant human pseudocathepsin D. Biochemistry 44, 15725-15733.
23. Li, T., Yowell, C. A., Beyer, B. B., Hung, S. H., Westling, J., Lam, M.T., Dunn, B. M., and Dame, J. B. (2004) Recombinant expression and enzymatic subsite characterization of plasmepsin 4 from the four Plasmodium species infecting man. Mol. Biochem. Parasitol. 135, 101-109. (Pubitemid 38470079)
24. Westling, J., Cipullo, P., Hung, S. H., Saft, H., Dame, J. B., and Dunn, B. M. (1999) Active site specificity of plasmepsin II. Protein Sci. 8, 2001-2009. (Pubitemid 29489927)
25. Morrison, J. F. (1969) Kinetics of reversible inhibition of enzyme-catalyzed reactions by tight-binding inhibitors. Biochim. Biophys. Acta 185, 269-286.
26. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326. (Pubitemid 27085611)
27. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D 54, 905-921.
28. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for the building of protein models in electron density maps and the location of errors in these models. Acta Crystallogr., Sect. A 47, 110-119.
29. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385.
30. Word, J. M., Lovell, S. C., Richardson, J. S., and Richardson, D. C. (1999) Asparagine and glutamine:Using hydrogen atom contacts in the choice of side-chain amide orientation. J. Mol. Biol. 285, 1735-1747.
31. Weichenberger, C. X., Byzia, P., and Sippl, M. J. (2008) Visualization of unfavorable interactions in protein folds. Bioinformatics 24, 1206-1207.
32. Jones, G., Willett, P., Glen, R. C., Leach, A. R., and Taylor, R. (1997) Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267, 727-748. (Pubitemid 27170693)
33. Verdonk, M. L., Cole, J. C., Hartshorn, M. J., Murray, C. W., and Taylor, R. D. (2003) Improved protein-ligand docking using GOLD. Proteins-Struct. Funct. Genet. 52, 609-623. (Pubitemid 37034158)
34. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kale, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802. (Pubitemid 43078511)
35. Jorgensen, W. L., Maxwell, D. S., and TiradoRives, J. (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118, 11225-11236. (Pubitemid 26399746)
36. Tyas, L., Gluzman, I., Moon, R. P., Rupp, K., Westling, J., Ridley, R. G., Kay, J., Goldberg, D. E., and Berry, C. (1999) Naturally-occurring and recombinant forms of the aspartic proteinases plasmepsins I and II from the human malaria parasite Plasmodium falciparum. FEBS Lett. 454, 210-214. (Pubitemid 29304602)
37. Luker, K. E., Francis, S. E., Gluzman, I. Y., and Goldberg, D. E. (1996) Kinetic analysis of plasmepsins I and II, aspartic proteases of the Plasmodium falciparum digestive vacuole. Mol. Biochem. Parasitol. 79, 71-78.
38. Johansson, P. O., Lindberg, J., Blackman, M. J., Kvarnstrom, I., Vrang, L., Hamelink, E., Hallberg, A., Rosenquist, A., and Samuelsson, B. (2005) Design and synthesis of potent inhibitors of plasmepsin I and II: X-ray crystal structure of inhibitor in complex with plasmepsin II. J. Med. Chem. 48, 4400-4409.
39. Cooper, J., Foundling, S., Hemmings, A., Blundell, T., Jones, D. M., Hallett, A., and Szelke, M. (1987) The structure of a synthetic pepsin inhibitor complexed with endothiapepsin. Eur. J. Biochem. 169, 215-221. (Pubitemid 18007087)
40. Prade, L., A.F., J., Boss, C., Richard-Bildstein, S., Meyer, S., Binkert, C., and Bur, D. (2005) X-ray structure of plasmepsin II complexed with a potent achiral inhibitor. J. Biol. Chem. 280, 23837-23843. (Pubitemid 40884870)
41. Bjelic, S., Nervall, M., Gutierrez-de-Teran, H., Ersmark, K., Hallberg, A., and Aqvist, J. (2007) Computational inhibitor design against malaria plasmepsins. Cell. Mol. Life Sci. 64, 2285-2305. (Pubitemid 47347955)
42. Ferrara, P., and Jacoby, E. (2007) Evaluation of the utility of homology models in high throughput docking. J. Mol. Model. 13, 897-905. (Pubitemid 47028813)
43. Beyer, B. M., and Dunn, B. M. (1996) Self-activation of recombinant human lysosomal procathepsin D at a newly engineered cleavage junction, "short" pseudocathepsin D. J. Biol. Chem. 271, 15590-15596.
44. Krogstad, D. J., Schlesinger, P. H., and Gluzman, I. Y. (1985) Antimalarials increase vesicle pH in Plasmodium falciparum. J. Cell Biol. 101, 2302-2309. (Pubitemid 16169961)
45. Yayon, A., Cabantchik, Z. I., and Ginsburg, H. (1984) Identification of the acidic compartment of Plasmodium falciparum-infected human erythrocytes as the target of the antimalarial drug chloroquine. EMBO J. 3, 2695-2700.
46. Banerjee, R., Francis, S. E., and Goldberg, D. E. (2003) Food vacuole plasmepsins are processed at a conserved site by an active convertase activity in Plasmodium falciparum. Mol. Biochem. Parasitol. 129, 157-165. (Pubitemid 36794568)
47. Gluzman, I. Y., Francis, S. E., Oksman, A., Smith, C. E., Duffin, K. L., and Goldberg, D. E. (1994) Order and specificity of the Plasmodium falciparum hemoglobin degradation pathway. J. Clin. Invest. 93, 1602-1608. (Pubitemid 24116398)
48. Siripurkpong, P., Yuvaniyama, J., Wilairat, P., and Goldberg, D. E. (2002) Active site contribution to specificity of the aspartic proteases plasmepsins I and II. J. Biol. Chem. 277, 41009-41013. (Pubitemid 35215690)
49. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D., and Bairoch, A. (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31, 3784-3788.