Data-mining approaches reveal hidden families of proteases in the genome of malaria parasite

Genome Research

Volumn 13, Issue 4, 2003, Pages 601-616

  Wu, Yimin ^a,c   Wang, Xiangyun ^b   Liu, Xia ^a   Wang, Yufeng ^a  

^a American Type Culture Collection ^*  (United States)

^b ASTRAZENECA   (United Kingdom)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT; CALPAIN; CASPASE; GENE PRODUCT; HEMOGLOBIN; PROTEINASE; PROTEINASE INHIBITOR; SIGNAL PEPTIDASE I;

ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; DRUG DESIGN; DRUG TARGETING; ENZYME ACTIVITY; GENE SEQUENCE; GENETIC CODE; GENETIC TRANSCRIPTION; HEMOLYSIS; HOST PARASITE INTERACTION; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITOSIS; PLASMODIUM; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; UNINDEXED SEQUENCE;

AMINO ACID SEQUENCE; ANIMALS; CALPAIN; ENDOPEPTIDASES; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOME, PROTOZOAN; HUMANS; MALARIA, FALCIPARUM; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PLASMODIUM FALCIPARUM; PREDICTIVE VALUE OF TESTS; SEQUENCE ALIGNMENT; SERINE ENDOPEPTIDASES;

PLASMODIUM FALCIPARUM; PROTOZOA; VERTEBRATA;

EID: 0242669367     PISSN: 10889051     EISSN: None     Source Type: Journal    
DOI: 10.1101/gr.913403     Document Type: Article

References (67)

1. Aravind, L., Dixit, V.M., and Koonin, E.V. 1999. The domains of death: Evolution of the apoptosis machinery. Trends Biochem. Sci. 24: 47-53.
2. Arthur, J.S., Gauthier, S., and Elce, J.S. 1995. Active site residues in m-calpain: Identification by site-directed mutagenesis. FEBS Lett. 368: 397-400.
3. 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. 99: 990-995.
4. Barale, J.C., Blisnick, T., Fujioka, H., Alzari, P.M., Aikawa, M., Braun-Breton, C., and Langsley, G. 1999. Plasmodium falciparum subtilisin-like protease 2, a merozoite candidate for the merozoite surface protein 1-42 maturase. Proc. Natl. Acad. Sci. 96: 6445-6450.
5. Ben Mamoun, C., Gluzman, I.Y., Hott, C., MacMillan, S.K., Amarakone, A.S., Anderson, D.L., Carlton, J.M., Dame, J.B., Chakrabarti, D., Martin, R.K., et al. 2001. Coordinated programme of gene expression during asexual intraerythrocytic development of the human malaria parasite Plasmodium falciparum revealed by microarray analysis. Mol. Microbiol. 39: 26-36.
6. Bernstein, N.K., Cherney, M.M., Loetscher, H., Ridley, R.G., and James, M.N. 1999. Crystal structure of the novel aspartic proteinase zymogen proplasmepsin II from Plasmodium falciparum. Nat. Struct. Biol. 6: 32-37.
7. Blackman, M.J. 2000. Proteases involved in erythrocyte invasion by the malaria parasite: Function and potential as chemotherapeutic targets. Curr. Drug Targets 1: 59-83.
8. Blackman, M.J., Fujioka, H., Stafford, W.H., Sajid, M., Clough, B., Fleck, S.L., Aikawa, M., Grainger, M., and Hackett, F. 1998. A subtilisin-like protein in secretory organelles of Plasmodium falciparum merozoites. J. Biol. Chem. 273: 23398-23409.
9. Braun-Breton, C., Rosenberry, T.L., and da Silva, L.P. 1988. Induction of the proteolytic activity of a membrane protein in Plasmodium falciparum by phosphatidyl inositol-specific phospholipase C. Nature 332: 457-459.
10. 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.
11. Craik, C.S., Rutter, W.J., and Fletterick, R. 1983. Splice junctions: Association with variation in protein structure. Science 220: 1125-1129.
12. Curley, G.P., O'Donovan, S.M., McNally, J., Mullally, M., O'Hara, H., Troy, A., O'Callaghan, S.A., and Dalton, J.P. 1994. Aminopeptidases from Plasmodium falciparum, Plasmodium chabaudi chabaudi and Plasmodium berghei. J. Eukaryot. Microbiol. 41: 119-123.
13. David, P.H., Hadley, T.J., Aikawa, M., and Miller, L.H. 1984. Processing of a major parasite surface glycoprotein during the ultimate stages of differentiation in Plasmodium knowlesi. Mol. Biochem. Parasitol. 11: 267-282.
14. Delplace, P., Bhatia, A., Cagnard, M., Camus, D., Colombet, G., Debrabant, A., Dubremetz, J.F., Dubreuil, N., Prensier, G., Fortier, B., et al. 1988. Protein p126: A parasitophorous vacuole antigen associated with the release of Plasmodium falciparum merozoites. Biol. Cell 64: 215-221.
15. Denison, S.H., Orejas, M., and Arst Jr., H.N. 1995. Signaling of ambient pH in Aspergillus involves a cysteine protease. J. Biol. Chem. 270: 28519-28522.
16. Doerig, C., Meijer, L., and Mottram, J.C. 2002. Protein kinases as drug targets in parasitic protozoa. Trends Parasitol. 18: 366-371.
17. Dua, M., Raphael, P., Sijwali, P.S., Rosenthal, P.J., and Hanspal, M. 2001. Recombinant falcipain-2 cleaves erythrocyte membrane ankyrin and protein 4.1. Mol. Biochem. Parasitol. 116: 95-99
18. Eggleson, K.K., Duffin, K.L., and Goldberg, D.E. 1999. Identification and characterization of falcilysin, a metallopeptidase involved in hemoglobin catabolism within the malaria parasite Plasmodium falciparum. J. Biol. Chem. 274: 32411-32417.
19. Fast, N.M., Kissinger, J.C., Roos, D.S., and Keeling, P.J. 2001. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol. 18: 418-426.
20. Florens, L., Washburn, M.P., Raine, J.D., Anthony, R.M., Grainger, M., Haynes, J.D., Moch, J.K., Muster, N., Sacci, J.B., Tabb, D.L., et al. 2002. A proteomic view of the Plasmodium falciparum life cycle. Nature 419: 520-526.
21. Florent, I., Derhy, Z., Allary, M., Monsigny, M., Mayer, R., and Schrevel, J. 1998. A Plasmodium falciparum aminopeptidase gene belonging to the M1 family of zinc-metallopeptidases is expressed in erythrocytic stages. Mol. Biochem. Parasitol. 97: 149-160.
22. Franz, T., Vingron, M., Boehm, T., and Dear, T.N. 1999. Capn7: A highly divergent vertebrate calpain with a novel C-terminal domain. Mamm. Genome, 10: 318-321.
23. Friedman, R., and Hughes, A.L. 2001. Pattern and timing of gene duplication in animal genomes. Genome Res. 11: 1842-1847.
24. Gantt, S.M., Myung, J.M., Briones, M.R., Li, W.D., Corey, E.J., Omura, S., Nussenzweig, V., and Sinnis, P. 1998. Proteasome inhibitors block development of Plasmodium spp. Antimicrob. Agents Chemother. 42: 2731-2738
25. Gardner, M.J., Hall, N,, Fung, E., White, O., Berriman, M., Hyman, R.W., Carlton, J.M., Pain, A., Nelson, K.E., Bowman, S., et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 41: 498-511.
26. Glading, A., Lauffenburger, D.A., and Wells, A. 2002. Cutting to the chase: Calpain proteases in cell motility. Trends Cell Biol. 12: 46-54.
27. Gu, X., Wang, Y., and Gu, J. 2002. Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat Genet. 31: 205-209.
28. Hackett, F., Sajid, M., Withers-Martinez, C., Grainger, M., and Blackman, M.J. 1999. PfSUB-2: A second subtilisin-like protein in Plasmodium falciparum merozoites. Mol. Biochem. Parasitol. 103: 183-195.
29. Hayward, R.E., Derisi, J.L., Alfadhli, S., Kaslow, D.C., Brown, P.O., and Rathod, P.K. 2000. Shotgun DNA microarrays and stage-specific gene expression in Plasmodium falciparum malaria. Mol. Microbiol. 35: 6-14.
30. Jean, L., Long, M., Young, J., Pery, P., and Tomley, F. 2001. Aspartyl proteinase genes from apicomplexan parasites: Evidence for evolution of the gene structure. Trends Parasitol. 17: 491-498.
31. Kissinger, J.C., Brunk, B.P., Crabtree, J., Fraunholz, M.J., Gajria, B., Milgram, A.J., Pearson, D.S., Schug, J., Bahl, A., Diskin, S.J., et al. 2002. The Plasmodium genome database. Nature 419: 490-492.
32. Li, J., Matsuoka, H., Mitamura, T., and Horii, T. 2002. Characterization of proteases involved in the processing of Plasmodium falciparum serine repeat antigen (SERA). Mol. Biochem. Parasitol. 120: 177-186.
33. Li, W-H. 1983. Evolution of duplicate genes and pseudogenes. In Evolution of genes and proteins (eds. M. Nei and R.K. Keohn), pp. 14-37. RK Sinauer Associates, Sunderland, MA.
34. Madeo, F., Herker, E., Maldener, C., Wissing, S., Lachelt, S., Herlan, M., Fehr, M., Lauber, K., Sigrist, S.J., Wesselborg, S., et al. 2002. A caspase-related protease regulates apoptosis in yeast. Mol. Cell. 9: 911-917.
35. McKerrow, J.H., Sun, E., Rosenthal, P.J., and Bouvier, J. 1993. The proteases and pathogenicity of parasitic protozoa. Annu. Rev. Microbiol. 47: 821-853.
36. McLysaght, A., Hokamp, K., and Wolfe, K.H. 2002. Extensive genomic duplication during early chordate evolution. Nat. Genet. 31: 200-204.
37. Miller, S.K., Good, R., Drew, D.R., Delorenzi, M., Sanders, P.R., Hodder, A.N., Speed, T.P., Cowman, A.F., De Koning-Ward, T.F., and Crabb, B.S. 2002. A subset of Plasmodium falciparum SERA genes are expressed and appear to play an important role in the erythrocytic cycle. J. Biol. Chem. 277: 47524-47532.
38. Mu, J., Duan, J., Makova, K.D., Joy, D.A., Huynh, C.Q., Branch, O.H., Li, W.H., and Su, X.Z. 2002. Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature 418: 323-326.
39. Narum, D.L. and Thomas, A.W. 1994. Differential localization of full-length and processed forms of PF83/AMA-1 an apical membrane antigen of Plasmodium falciparum merozoites. Mol. Biochem. Parasitol. 67: 59-68.
40. Notredame, C., Higgins, D.G., and Heringa, J. 2000. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302: 205-217.
41. Ohno, S. 1970. Evolution by gene duplication. Springer-Verlag, Berlin
42. Olaya, P. and Wasserman, M. 1991. Effect of calpain inhibitors on the invasion of human erythrocytes by the parasite Plasmodium falciparum. Biochim. Biophys. Acta. 1096: 217-221.
43. Paetzel, M., Dalbey, R.E., and Strynadka, N.C. 2000. The structure and mechanism of bacterial type I signal peptidases. A novel antibiotic target. Pharmacol. Ther. 87: 27-49.
44. Rawlings, N.D. and Barrett, A.J. 1993. Evolutionary families of peptidases. Biochem. J. 290: 205-218.
45. Rich, S.M., Licht, M.C., Hudson, R.R., and Ayala, F.J. 1998. Malaria's Eve: Evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc. Natl. Acad. Sci. 95: 4425-4430.
46. Rosenthal, P.J. 1998. Proteases of malaria parasites: New targets for chemotherapy. Emery. Infect. Dis. 4: 49-57.
47. Rosenthal, P.J. 2002. Hydrolysis of erythrocyte proteins by proteases of malaria parasites. Curr. Opin. Hematol. 9: 140-145.
48. Rosenthal, P.J., Kim, K., McKerrow, J.H., and Leech, J.H. 1987. Identification of three stage-specific proteinases of Plasmodium falciparum. J. Exp. Med. 166: 816-821.
49. Saitou, N. and Nei, M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
50. Salmon, B.L., Oksman, A., and Goldberg, D.E. 2001. Malaria parasite exit from the host erythrocyte: A two-step process requiring extraerythrocytic proteolysis. Proc. Natl. Acad. Sci. 98: 271-276.
51. Shenai, B.R., Sijwali, P.S., Singh, A., and Rosenthal, P.J. 2000. Characterization of native and recombinant falcipain-2, a principal trophozoite cysteine protease and essential hemoglobinase of Plasmodium falciparum. J. Biol. Chem. 275: 29000-29010.
52. 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., et al. 1996. Structure and inhibition of plasmepsin II, a hemoglobin-degrading enzyme from Plasmodium falciparum. Proc. Natl. Acad. Sci. 93: 10034-10039.
53. Sorimachi, H., Ishiura, S., and Suzuki, K. 1997. Structure and physiological function of calpains. Biochem. J. 328: 721-732.
54. Southan, C. 2001. A genomic perspective on human proteases. FEBS Lett. 498: 214-218.
55. Thornberry, N.A. and Lazbnik, L. 1998. Caspases: Enemies within. Science 281: 1312-1316.
56. Trager, W. and Jensen, J.B. 1976. Human malaria parasites in continuous culture. Science. 193: 673-675.
57. Triglia, T., Thompson, J.K., and Cowman, A.F. 2001. An EBA175 homolog which is transcribed but not translated in erythrocytic stages of Plasmodium falciparum. Mol. Biochem. Parasitol. 116: 55-63.
58. 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.
59. Uren, A.G., O'Rourke, K., Aravind, L.A., Pisabarro, M.T., Seshagiri, S., Koonin, E.V., and Dixit, V.M. 2000. Identification of paracaspases and metacaspases: Two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 6: 961-967.
60. Verma, R., Aravind, L., Oania, R., McDonald, W.H., Yates III, J.R. Koonin, E.V., and Deshaies, R.J. 2002. Role of Rpn 11 Metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298: 611-615.
61. Verra, F. and Hughes, A.L. 1999. Natural selection on apical membrane antigen-1 of Plasmodium falciparum. Parassitologi. 41: 93-95.
62. Volkman, S.K., Barry, A.E., Lyons, E.J., Nielsen, K.M., Thomas, S.M., Choi, M., Thakore, S.S., Day, K.P., Wirth, D.F., and Hartl, D.L. 2001. Recent origin of Plasmodium falciparum from a single progenitor. Science 293: 482-484.
63. Wang, Y. and Gu, X. 2001. Functional divergence in caspase gene family and altered functional constraints: Statistical analysis and prediction. Genetics 158: 1311-1320.
64. Wilson, R.J., Denny, P.W., Preiser, P.R., Rangachari, K., Roberts, K., Roy, A., Whyte, A., Strath, M., Moore, D.J., Moore, P.W., et al. 1996. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 261: 155-172.
65. Wootton, J.C., Feng, X., Ferdig, M.T., Cooper, R.A., Mu, J., Baruch, D.I., Magill, A.J., and Su, X.Z. 2002. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418: 320-323.
66. Yoshizawa, T., Sorimachi, H., Tomioka, S., Ishiura, S., and Suzuki, K. 1995. A catalytic subunit of calpain possesses full proteolytic activity. FEBS Lett. 358: 101-103.
67. Zuegge, J., Ralph, S., Schmuker, M., McFadden, G.I., and Schneider, G. 2001. Deciphering apicoplast targeting signals-feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins. Gene 280: 19-26.