Purification and characterization of a hemoglobin degrading aspartic protease from the malarial parasite Plasmodium vivax

Journal of Biochemistry

Volumn 138, Issue 1, 2005, Pages 71-78

  Sharma, Arun ^a   Eapen, Alex ^a   Subbarao, Sarala K ^a  

^a NATIONAL INSTITUTE OF MALARIA RESEARCH   (India)

Author keywords

Aspartic protease; Chloroquine; Hemoglobin; Malaria; Plasmepsin; Plasmodium vivax

Indexed keywords

1,10 PHENANTHROLINE; ANTIMALARIAL AGENT; ASPARTIC PROTEINASE; BENZYLSULFONYL FLUORIDE; CALCIUM ION; CHLOROQUINIDINE; COPPER ION; EDETIC ACID; GELATIN; HEMOGLOBIN; MAGNESIUM ION; MEFLOQUINE; MERCURY; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; PEPSTATIN; PRIMAQUINE; QUININE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME PURIFICATION; GEL PERMEATION CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; ION EXCHANGE CHROMATOGRAPHY; MOLECULAR WEIGHT; NONHUMAN; PH; PLASMODIUM VIVAX; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DEGRADATION; ZYMOGRAPHY;

ANIMALS; ASPARTIC ENDOPEPTIDASES; CHELATING AGENTS; CHROMATOGRAPHY, DEAE-CELLULOSE; CHROMATOGRAPHY, GEL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GELATIN; HEMOGLOBINS; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; METALS, HEAVY; PEPSTATINS; PLASMODIUM VIVAX; PROTEASE INHIBITORS; SULFHYDRYL REAGENTS;

PLASMODIUM VIVAX;

EID: 23344449249     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvi105     Document Type: Article

References (57)

1. Walsh, J.A. (1989) Disease problems in the third world. Ann. N. Y. Acad. Sci. 569, 1-16
2. Olliaro, P., Cattani, J., and Writh, D. (1996) Malaria the submerged diseases. JAMA 275, 230-233
3. Kamchonwongpaisan, S., Samoff, E., and Meshnick, S.R. (1997) Identification of hemoglobin degradation products in Plasmodium falciparum. Mol. Biochem. Parasitol. 86, 179-186
4. Scheibal, L.W. and Sherman, I.W. (1988) Plasmodial metabolism and related organellar function during various stages of the life cycle: Proteins, lipids, nucleic acids and vitamins in Malaria: Principals and practice of Malariology (Wernsdofer, W.H. and McGregerrds, eds.) pp. 219-252, Churchill Livingstone, Edinburgh
5. Mckerrow, J.H., Sun, E., Rosenthal, P.J., and Bouvir, J. (1993) Proteases and pathogenicity of parasitic protozoa. Ann. Rev. Microbiol. 17, 821-853
6. Rosenthal, P.J. and Meshnick, S.R. (1996) Hemoglobin catabolism and Fe utilization by malaria parasites. Mol. Biochem. Parasitol. 83, 131-139
7. Francis, S.E., Sullivan, D.G. Jr., and Goldberg, D.E. (1997) Hemoglobin metabolism in the malaria parasite Plasmodium falciparum. Annu. Rev. Microbiol. 51, 97-123
8. Sherman, I.W. (1979) Biochemistry of plasmodium (malaria parasite). Microbiol. Rev. 43, 453-494
9. 14C-amino acids by malaria (Plasmodium lophurae) IV. In vivo utilization of host cell hemoglobin. Int. J. Biochem. 1, 635-637
10. Salas, F., Fichmann, J., Lee, G.K., Scott, M.D., and Rosenthal, P.J. (1995) Functional expression of falcipain, Plasmodium falciparum cysteine proteinase supports its role as a malarial hemoglobinase. Infect. Immun. 63, 2120-2125
11. Coombs, G.H., Goldberg, D.E., Klemba, M., Berry, C., Kay, J., and Mottram, J. (2001) Aspartic proteases of Plasmodium falciparum and other parasitic protozoa as drug targets. Trends Parasitol. 17, 532-537
12. Boss, C., Richard-Bildstein, S., Weller, T., Fischli, W., Meyer, S., and Binkert, C. (2003) Inhibitors of the Plasmodium falciparum parasite protease plasmepsin II as potential antimalarial agents. Curr. Med. Chem. 10, 883-907
13. Rosenthal, P.J., Mckerrow, J.H., Aikawa, M., and Leach, J.H. (1988) A malarial cysteine proteinase necessary for hemoglobin degradation by Plasmodium falciparum. J. Clin. Invest. 82, 1560-1566
14. Rosenthal, P.J., Ring, C.S., Chen, X., and Cohen, F.E. (1993) Characterization of a Plasmodium vivax cysteine proteinase gene identifies uniquely conserved amino acid that may mediate the substrate specificity of malarial hemoglobinases. J. Mol. Biol. 241, 312-316
15. Martins, T.M., Novo, C., do Rosario, V.E., and Domingos, A. (2003) Aspartic proteases from Plasmodium chabaudi: a rodent model for human malaria. Acta Trop. 89, 1-12
16. 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
17. Berry, C., Dame, J.B., Dunn, B.M., and Kay, J. (1995) Aspartic proteinases from the human malaria parasite Plasmodium falciparum. Adv. Exp. Med. Biol. 362, 511-518
18. Goldberg, D.E., Slater, A.F.G., 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
19. Vander Jagt, D.L., Hunsaker, L.A., Campos, N.M., and Scaletti, J.V. (1992) Localization and characterization of hemoglobin-degrading aspartic proteinases from the malarial parasite Plasmodium falciparum. Biochim. Biophy. Acta 1122, 256-264
20. 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
21. 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
22. Hill, J., Tyas, L., Phylip, L.H., Kay, J., Dunn, B.M., and Berry, C. (1994) High level expression and characterization of plasmepsin II, an aspartic proteinase from Plasmodium falciparum. FEBS Lett. 352, 155-158
23. 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 plasmepsin I and II from the human malaria parasite Plasmodium falciparum. FEBS Lett. 454, 210-214
24. Humphreys, M.J., Moon, R.P., Klinder, A., Fowler, S.D., Rupp, K., Bur, D., Ridley, R.G., and Berry, C. (1999) The aspartic proteinase from the rodent parasite Plasmodium berghei as a potential model for plasmepsin from the human malaria parasite, Plasmodium falciparum. FEBS Lett. 463, 43-48
25. Johansson, P.O., Chen, Y., Belfrage, A.K., Blackman, M.J., Kvarnstrom, I., Jansson, K., Vrang, L., Hamelink, E., Rosenquist, A., and Samuelson, B. (2004) Design and synthesis of potent inhibitors of the malaria aspartyl proteases plasme psin I and II. Use of solid phase synthesis to explore novel statine motifs. J. Med. Chem. 47, 3353-3366
26. 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
27. Francis, S.E., Gluzman, I.Y., Oksman, A., Knickerbocker, A., Muelber, R., Bryant, M.L., Sherman, D.R., Rusell, D.G., and Goldberg, D.G. (1994) Molecular characterization and inhibition of a Plasmodium falciparum aspartic hemoglobinase. EMBO J. 13, 306-317
28. 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 characterization of plasmepsin I from Plasmodium falciparum. Eur. J. Biochem. 244, 552-560
29. Nezami, A. and Freire, E. (2002) The integration of genomic and structural information in the development of high affinity plasmepsin inhibitors. Int. J. Parasitol. 32, 1669-1676
30. Nezami, A., Luque, I., Kimura, T., Kiso, Y., and Freire, E. (2002) Identification and characterization of allophenymorstatine-based inhibitors of plasmepsin II, an antimalarial target. Biochemistry 41, 2273-2280
31. Na, B.K., Lee, E.G., Lee, H.W., Cho, S.H., Bae, Y.A., Kong, Y., Lee, J.K., and Kim, T.S. (2004) Aspartic proteases of Plasmodium vivax are highly conserved in wild isolates. Korean J. Parasitol. 42, 61-66
32. 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
33. 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 different species of malaria parasite. Exp. Parasitol. 87, 185-193
34. 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
35. Fagan, J.M., Waxman, L., and Goldberg, A.L. (1986) Red blood cells contain a pathway for the degradation of oxidant-damaged hemoglobin that does not require ATP or ubiquitin. J. Biol. Chem. 261, 5705-5713
36. Biswas, S., Saxena, Q.B., Roy, A., and Sharma, V.P. (1988) Isolation of different erythrocytic stages of Plasmodium falciparum and synchronization in culture. Ind. J. Malariol. 25, 7-10
37. Sharma, A. (1993) Subcellular distribution of superoxide dismutase and catalase in human malaria parasite Plasmodium vivax. Ind. J. Exp. Biol. 31, 275-277
38. Dacie, J.V. and Lewis, S.M. (1968) Practical Haematology, 4th ed., Churchill, London
39. Walter, R.D., Nordmeyer, J.P., and Konigk, E. (1974) NADP specific glutamate dehydrogenase from P. chabaudi. Hoppe Seyler's Z. Physiol. Chem. 355, 495-500
40. Lowry, O.H., Roseborough, N.J., Fare, A.L., and Randall, R.L. (1951) Protein measurement with Folin phenol reagent. J. Biol. Chem. 193, 265-275
41. Hatakeyama, T., Kohzaki, H., and Yamasaki, N. (1992) Microassay for proteases using succinyl casein as a substrate. Annal. Biochem. 204, 181-184
42. Laemmli, U.K. (1970) Cleavage of structuaral proteins during assembly of the head of bacteriophage T4. Nature 227, 680-685
43. Goldberg, D.E., Slater, A.F.G., Cerami, A., and Henderson, G.B. (1990) Hemoglobin degradation in the malaria parasite Plasmodium falciparum: An ordered process in a unique organelle. Proc. Natl Acad. Sci. USA 87, 2931-2935
44. Moyle, G.J., Youle, M., Higgs, C., Monaghan, J., Prince, W., Chapman, S., Cleudenin, N., and Nelson, M.R. (1998) Safety, pharmacokinetics and antiretrovial activity of the potent specific human immunodeficiency virus protease inhibitor nelfinavir: results of a phase I/II trial and extended follow-up in patients infected with human immunodeficiency virus. J. Clin. Pharmacol. 38, 736-743
45. Vander Jagt, D.L., Hunsaker, L.A., and Campos, N.M. (1986) Characterization of hemoglobin-degrading, low molecular weight protease from Plasmodium falciparum. Mol. Biochem. Parasitol. 18, 389-400
46. Sherman, I.W. and Tanigoshi, L. (1983) Purification of Plasmodium lophurae cathepsin D and its effects on erythrocyte membrane proteins. Mol. Biochem. Parasitol. 8, 207-226
47. Dunn, B.M., Valler, M.J., Rolph, C.E., Jimenez, M., and Kay, J. (1987) The pH dependence of the hydrolysis of chromogenic substrates by selected aspartic proteinases. Biochim. Biophys. Acta 913, 122-130
48. Xie, D., Gulnik, S., Collins, L., Gustchina, E., Suvorov, L., and Erickson, J.W. (1997) Dissection of the pH dependence of inhibitor binding energetics for an aspartic protease: Direct measurement of the protonation states of the catalytic aspartic acid residues. Biochemistry 36, 16166-16172
49. 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
50. Ring, C.S., Sun, E., Mckerrow, J.H., Lee, G.K., Rosenthal, P.J., Kuntz, L.D., and Cohen, F.E. (1993) Structure-based inhibitor design by using protein models for the development of antiparasite agents. Proc. Natl Acad. Sci. USA 90, 3583-3587
51. Kay, J. and Dunn, B.M. (1992) Substrate specificity and inhibitors of aspartic proteinases. Scand. J. Clin. Lab. Invest. 52, 23-30
52. Kolakovich, K.A., Gluzman, I.Y., Duffin, K.L., and Goldberg, D.E. (1997) Generation of hemoglobin peptides in the acidic digestive vacuole of Plasmodium falciparum implicates peptide transport in amino acid production. Mol. Biochem. Parasitol. 87, 123-135
53. Semenov, A., Olson, J.E., and Rosenthal, P.J. (1998) Antimalarial synergy of cysteine and aspartic protease inhibitors. Antimicrobiol. Agents Chemother. 42, 2254-2258
54. Goldberg, D.E. (1992) Plasmodial hemoglobin degradation: An ordered pathway in specialized organelle. Infect. Agents Dis. 1, 207-211
55. Beavis, R.C. and Chait, B.T. (1990) Rapid sensitive analysis of protein mixtures by mass spectrometry. Proc. Natl Acad. Sci. USA 87, 6873-6877
56. 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
57. Krogstad, D.J., Schlesinger, P.H., and Gluzman, I.Y. (1985) Antimalarials increase vesicle pH in Plasmodium falciparum. J. Cell Biol. 101, 2302-2309