Food vacuole plasmepsins are processed at a conserved site by an acidic convertase activity in Plasmodium falciparum

Molecular and Biochemical Parasitology

Volumn 129, Issue 2, 2003, Pages 157-165

  Banerjee, Ritu ^a   Francis, Susan E ^a   Goldberg, Daniel E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calpain; Convertase; Plasmepsin; Protease

Indexed keywords

ASPARTIC PROTEINASE; CALPAIN; PLASMEPSIN I;

ARTICLE; CELL FREE SYSTEM; CELL VACUOLE; ENZYME ASSAY; ENZYME KINETICS; NONHUMAN; PH MEASUREMENT; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MOTIF;

PLASMODIUM FALCIPARUM;

EID: 0038691865     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-6851(03)00119-1     Document Type: Article

References (41)

1. Trigg PI, Kondrachine AV. Malaria: parasite biology, pathogenesis and protection. Washington, DC: American Society of Microbiology; 1998.
2. Banerjee R, Goldberg DE. The Plasmodium food vacuole. In: Rosenthal PJ, editor. Antimalarial chemotherapy: mechanisms of action, resistance, and new directions in drug discovery. Totowa, NJ: Humana Press Inc.; 2001. p. 43-63.
3. Rosenthal P.J. Plasmodium falciparum: effects of proteinase inhibitors on globin hydrolysis by cultured malaria parasites. Exp. Parasitol. 80:1995;272-281.
4. Olson J.E., Lee G.K., Semenov A., Rosenthal P.J. Antimalarial effects in mice of orally administered peptidyl cysteine protease inhibitors. Bioorg. Med. Chem. 7:1999;633-638.
5. Aikawa M., Hepler P.K., Huff C.G., Sprinz H. The feeding mechanism of avian malarial parasites. J. Cell Biol. 28:1966;355-373.
6. Langreth S.G., Jensen J.B., Reese R.T., Trager W. Fine structure in human malaria in vitro. J. Protozool. 25:1978;443-452.
7. Slomianny C. Three-dimensional reconstruction of the feeding process of the malaria parasite. Blood Cells. 16:1990;369-378.
8. Goldberg D.E. Hemoglobin degradation in Plasmodium-infected red blood cells. Semin. Cell Biol. 4:1993;355-361.
9. Francis S.E., Sullivan D.J., Goldberg D.E. Hemoglobin metabolism in the malaria parasite Plasmodium falciparum. Annu. Rev. Microbiol. 51:1997;97-123.
10. 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 degradation pathway. J. Clin. Invest. 93:1994;1602-1608.
11. Salas F., Fichmann J., Lee G.K., Scott M.D., Rosenthal P.J. Functional expression of falcipain, a Plasmodium falciparum cysteine proteinase, supports its role as a malarial hemoglobinase. Infect. Immun. 63:1995;2120-2125.
12. 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.
13. 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.
14. 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 Lett. 447:1999;149-154.
15. 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 Lett. 463:1999;43-48.
16. 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. U.S.A. 99:2002;990-995.
17. 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.
18. Eggleson K.K., Duffin K.L., Goldberg D.E. Identification and characterization of falcilysin, a metallopeptidase involved in hemoglobin catabolism within the malaria parasite Plasmodium falciparum. J. Biol. Chem. 274:1999;32411-32417.
19. Kolakovich K.A., Gluzman I.Y., Duffin K.L., Goldberg D.E. Generation of hemoglobin peptides in the acidic digestive vacuole of Plasmodium falciparum implicates peptide transport in amino acid production. Mol. Biochem. Parasitol. 87:1997;123-135.
20. Francis S.E., Banerjee R., Goldberg D.E. Biosynthesis and maturation of the malarial aspartic hemoglobinases plasmepsins I and II. J. Biol. Chem. 272:1997;14961-14968.
21. Lambros C., Vanderberg J.P. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65:1979;418-420.
22. Luker K.E., Francis S.E., Gluzman I.Y., Goldberg D.E. Kinetic analysis of plasmepsins I and II, aspartic proteases of the Plasmodium falciparum digestive vacuole. Mol. Biochem. Parasitol. 79:1996;71-78.
23. Angliker H., Anagli J., Shaw E. Inactivation of calpain by peptidyl fluoromethyl ketones. J. Med. Chem. 35:1992;216-220.
24. Gottschalk S., Waheed A., Schmidt B., Laidler P., von Figura K. Sequential processing of lysosomal acid phosphatase by a cytoplasmic thiol proteinase and a lysosomal aspartyl proteinase. EMBO J. 8:1989;3215-3219.
25. Kim W., Hatsuzawa K., Ishizuka Y., Hashiba K., Murakami K., Nakayama K. A processing enzyme for prorenin in mouse submandibular gland. J. Biol. Chem. 265:1990;5930-5933.
26. Shinagawa T., Do Y.S., Baxter J.D., Carilli C., Schilling J., Hsueh W.A. Identification of an enzyme in human kidney that correctly processes prorenin. Proc. Natl. Acad. Sci. U.S.A. 87:1990;1927-1931.
27. Kim W., Nakayama K., Nakagawa T., Kawamura Y., Haraguchi K., Murakami K. Mouse submandibular gland prorenin-converting enzyme is a member of glandular kallikrein family. J. Biol. Chem. 266:1991;19283-19287.
28. Wang P.H., Do Y.S., Macaulay L., Shinagawa T., Anderson P.W., Baxter J.D.et al. Identification of renal cathepsin B as a human prorenin-processing enzyme. J. Biol. Chem. 266:1991;12633-12638.
29. Van den Eijnden M., Saris J.J., de Bruin R.J., de Wit E., Sluiter W., Reudelhuber T.L.et al. Prorenin accumulation and activation in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 21:2001;911-916.
30. Bennet B.D., Denis P., Haniu M., Teplow D.B., Kahn S., Louis J.C.et al. A furin-like convertase mediates propeptide cleavage of BACE, the Alzheimer' β-secretase. J. Biol. Chem. 275:2000;37712-37717.
31. Khan A.R., Khazanovich-Bernstein N., Bergmann E.M., James M.N. Structural aspects of activation pathways of aspartic protease zymogens and viral 3C protease precursors. Proc. Natl. Acad. Sci. U.S.A. 96:1999;10968-10975.
32. Mac L., Mort J.S., Gloss J. Maturation of human cathepsin B. Proenzyme activation and proteolytic processing of the precursor to the mature proteinase, in vitro, are primarily unimolecular processes. J. Biol. Chem. 269:1994;13030-13035.
33. Sorimachi H., Toyama-Sorimachi N., Saido T.C., Kawasaki H., Sugita H., Miyasaka M.et al. Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J. Biol. Chem. 268:1993;10593-10605.
34. Sorimachi H., Ishiura S., Suzuki K. Structure and physiological function of calpains. Biochem. J. 328:1997;721-732.
35. Suzuki K., Sorimachi H. A novel aspect of calpain activation. FEBS Lett. 433:1998;1-4.
36. Carafoli E., Molinari M. Calpain, a protease in search of a function? Biochem. Biophys. Res. Commun. 247:1998;193-203.
37. Kinbara K.I.S., Tomioka S., Sorimachi H., Jeong S., Amano S., Kawasaki H.et al. Purification of native p94, a muscle specific calpain, and characterization of its autolysis. Biochem. J. 335:1998;589-596.
38. Dear N., Matena K., Vingron M., Boehm T. A new subfamily of vertebrate calpains lacking a calmodulin-like domain: implications for calpain regulation and evolution. Genomics. 45:1997;175-184.
39. Franz T., Vingron M., Boehm T., Dear T.N. Calpain 7: a highly divergent vertebrate calpain with a novel C-terminal domain. Mamm. Genome. 10:1999;318-321.
40. Carruth L.M., Demczuk S., Mizel S.B. Involvement of a calpain-like protease in the processing of the murine interleukin 1α precursor. J. Biol. Chem. 266:1991;12162-12167.
41. Ono Y., Sorimachi H., Suzuki K. Structure and physiology of calpain, an enigmatic protease. Biochem. Biophys. Res. Commun. 245:1998;289-294.