The cathepsin L of Toxoplasma gondii (TgCPL) and its endogenous macromolecular inhibitor, toxostatin

Molecular and Biochemical Parasitology

Volumn 164, Issue 1, 2009, Pages 86-94

  Huang, Robert ^a   Que, Xuchu ^a   Hirata, Ken ^b   Brinen, Linda S ^c   Lee, Ji Hyun ^c   Hansell, Elizabeth ^d   Engel, Juan ^d   Sajid, Mohammed ^d   Reed, Sharon ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cathepsin L; Cysteine proteinases; Inhibitor of cysteine proteinases; Toxoplasma gondii

Indexed keywords

ASPARTIC ACID; CATHEPSIN B; CATHEPSIN L; CYSTEINE PROTEINASE INHIBITOR; LEUCINE; TOXOSTATIN 1; TOXOSTATIN 2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; ENZYME KINETICS; ENZYME LOCALIZATION; ENZYME SPECIFICITY; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE DEVELOPMENT; PATHOGENESIS; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; TOXOPLASMA GONDII; TOXOPLASMOSIS;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; CATHEPSINS; CLONING, MOLECULAR; CYSTEINE ENDOPEPTIDASES; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; TOXOPLASMA;

TOXOPLASMA GONDII; VERTEBRATA;

EID: 58549120578     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2008.11.012     Document Type: Article

References (47)

1. Black M.W., and Boothroyd J.C. Lytic cycle of Toxoplasma gondii. Microbiol Mol Biol Rev 64 (2000) 607-623
2. Dobrowolski J.M., and Sibley L.D. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84 (1996) 933-939
3. Montoya J.G., and Liesenfeld O. Toxoplasmosis. Lancet 363 (2004) 1965-1973
4. McAuley J., Boyer K.M., Patel D., et al. Early and longitudinal evaluations of treated infants and children and untreated historical patients with congenital toxoplasmosis: the Chicago Collaborative Treatment Trial. Clin Infect Dis 18 (1994) 38-72
5. Luft B.J., and Remington J.S. Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15 (1992) 211-222
6. Dahl E.L., and Rosenthal P.J. Biosynthesis, localization, and processing of falcipain cysteine proteases of Plasmodium falciparum. Mol Biochem Parasitol 139 (2005) 205-212
7. Eksi S., Czesny B., Greenbaum D.C., Bogyo M., and Williamson K.C. Targeted disruption of Plasmodium falciparum cysteine protease, falcipain 1, reduces oocyst production, not erythrocytic stage growth. Mol Microbiol 53 (2004) 243-250
8. Ojcius D.M., Perfettini J.L., Bonnin A., and Laurent F. Caspase-dependent apoptosis during infection with Cryptosporidium parvum. Microbes Infect 1 (1999) 1163-1168
9. Kissinger J.C., Gajiria B., Li L., Paulsen I.T., and Roos D.S. ToxoDB: accessing the Toxoplasma gondii genome. Nucleic Acids Res 31 (2003) 234-236
10. Que X., Ngo H., Lawton J., et al. The cathepsin B of Toxoplasma gondii, Toxopain-1, is critical for parasite invasion and rhoptry protein processing. J Biol Chem 277 (2002) 25791-25797
11. Que X., Wunderlich A., Joiner K.A., and Reed S.L. Toxopain-1 is critical for infection in a novel chicken embryo model of congenital toxoplasmosis. Infect Immun 72 (2004) 2915-2921
12. Que X., Engel J.C., Ferguson D., Wunderlich A., Tomavo S., and Reed S.L. Cathepsin Cs are key for the intracellular survival of the protozoan parasite, Toxoplasma gondii. J Biol Chem 282 (2007) 4994-5003
13. Monteiro A.C., Abrahamson M., Lima A.P., Vannier-Santos M.A., and Scharfstein J. Identification, characterization and localization of chagasin, a tight-binding cysteine protease inhibitor in Trypanosoma cruzi. J Cell Sci 114 (2001) 3933-3942
14. Santos C.C., Coombs G.H., Lima A.P., and Mottram J.C. Role of the Trypanosoma brucei natural cysteine peptidase inhibitor ICP in differentiation and virulence. Mol Microbiol 66 (2007) 991-1002
15. Besteiro S., Coombs G.H., and Mottram J.C. A potential role for ICP, a leishmanial inhibitor of cysteine peptidases, in the interaction between host and parasite. Mol Microbiol 54 (2004) 1224-1236
16. Riekenberg S., Witjes B., Saric M., Bruchhaus I., and Scholze H. Identification of EhICP1, a chagasin-like cysteine protease inhibitor of Entamoeba histolytica. FEBS Lett 579 (2005) 1573-1578
17. Pandey K., Singh N., Arastu-Kapur S., Bogyo M., Rosenthal P.J., and Falstatin. a cysteine protease inhibitor of Plasmodium falciparum, facilitates erythrocyte invasion. PLoS Pathogens 2 (2006) 1031-1041
18. Rigden D.J., Mosolov V.V., and Galperin M.Y. Sequence conservation in the chagasin family suggests a common trend in cytsteine proteinase binding by unrelated protein inhibitors. Protein Sci 11 (2002) 1971-1977
19. Sanderson S.J., Westrop G.D., Scharfstein J., Mottram J.C., and Coombs G.H. Functional conservation of a natural cysteine peptidase inhibitor in protozoan and bacterial pathogens. FEBS Lett 542 (2003) 12-16
20. Ljunggren A., Redzynia I., Alvarez-Fernandez M., et al. Crystal structure of the parasite protease inhibitor chagasin in complex with a host target cysteine protease. J Mol Biol 371 (2007) 137-153
21. Wang S.X., Pandey K.C., Scharfstein J., et al. The structure of chagasin in complex with a cysteine protease clarifies the binding mode and evolution of an inhibitor family. Structure 15 (2007) 535-543
22. Hansner T., Freyer B., Mehlhorn H., and Ruger W. Isolation and characterization of a cDNA clone encoding a thiol proteinase of Sarcocystis muris cyst merozoites (Apicomplexa). Parasitol Res 85 (1999) 749-757
23. Reed S.L., Bouvier J., Pollack A.S., et al. Cloning of a virulence factor of Entamoeba histolytica: pathogenic strains possess a unique cysteine proteinase gene. J Clin Invest 91 (1993) 1532-1540
24. Que X., Kim S.H., Sajid M., et al. A surface amebic cysteine proteinase inactivates Interleukin-18. Infect Immun 71 (2003) 1274-1280
25. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 (1994) 4673-4680
26. Sali A., and Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234 (1993) 779-815
27. Peters P.J. Cryo-immunogold electron microscopy. Curr Protocols Cell Biol (1999) 4.7.1-4.7.12
28. Emanuelsson O., Nielsen H., Brunak S., and von H.G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300 (2000) 1005-1016
29. McGrath M.E., Eakin A.E., Engel J.C., McKerrow J.H., Craik C.S., and Fletterick R.J. The crystal structure of cruzain: a therapeutic target for Chagas disease. J Mol Biol 247 (1995) 251-259
30. Brinen L.S., Hansell E., Cheng J., Roush W.R., McKerrow J.H., and Fletterick R.J. A target within the target: probing cruzain's P1'site to define structural determinants for the Chagas' disease protease. Structure 8 (2000) 831-840
31. Fuller A.L., and McDougald L.R. Reduction in cell entry of Eimeria tenella (Coccidia) sporozoites by protease inhibitors, and partial characterization of proteolytic activity associated with intact sporozoites and merozoites. J Parasitol 76 (1990) 464-467
32. Sijwali P.S., Koo J., Singh N., and Rosenthal P.J. Gene disruptions demonstrate independent roles for the four falcipain cysteine proteases of Plasmodium falciparum. Mol Biochem Parasitol 150 (2006) 96-106
33. Sijwali P.S., and Rosenthal P.J. Gene disruption confirms a critical role for the cysteine protease falcipain-2 hemoglobin hydrolysis by Plasmodium falciparum. Proc Natl Acad Sci USA 101 (2004) 4384-4389
34. Chauhan S.S., Ray D., Kane S.E., Willingham M.C., and Gottesman M.M. Involvement of carboxy-terminal amino acids in secretion of human lysosomal protease cathepsin L. Biochemistry 37 (1998) 8584-8594
35. Zhou X.W., Kafsack B.F., Cole R.N., Beckett P., Shen R.F., and Carruthers V.B. The opportunistic pathogen Toxoplasma gondii deploys a diverse legion of invasion and survival proteins. J Biol Chem 280 (2005) 34233-34244
36. Hirokawa T., Boon-Chieng S., and Mitaku S. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14 (1998) 378-383
37. Subramanian S., Sijwali P.S., and Rosenthal P.J. Falcipain cysteine proteases require bipartite motifs for trafficking to the Plasmodium falciparum food vacuole. J Biol Chem 282 (2007) 24961-24969
38. Tam S.W., Cote-Paulino L.R., Peak D.A., Sheahan K., and Murnane M.J. Human cathepsin B-encoding cDNAs: sequence variations in the 3′-untranslated region. Gene 139 (1994) 171-176
39. Oguariri R.M., Dunn J.M., and Golightly L.M. 3′ gene regulatory elements required for expression of the Plasmodium falciparum developmental protein, Pfs25. Mol Biochem Parasitol 146 (2006) 163-172
40. Ullu E., Tschudi C., and Chakraborty T. RNA interference in protozoan parasites. Cell Microbiol 6 (2004) 509-519
41. Kibe M.K., Coppin A., Dendouga N., et al. Transcriptional regulation of two stage-specifically expressed genes in the protozoan parasite Toxoplasma gondii. Nucleic Acids Res 33 (2005) 1722-1736
42. Nakaar V., Bermudes D., Peck K.R., and Joiner K.A. Upstream elements required for expression of nucleoside triphosphate hydrolase genes of Toxoplasma gondii. Mol Biochem Parasitol 92 (1998) 229-239
43. Teo C.F., Zhou X.W., Bogyo M., and Carruthers V.B. Cysteine protease inhibitors block Toxoplasma gondii microneme secretion and cell invasion. Antimicrob Agents Chemother 51 (2007) 679-688
44. Sajid M., and McKerrow J.H. Cysteine proteases of parasitic organisms. Mol Biochem Parasitol 120 (2002) 1-21
45. dos Reis F.C.G., Smith B.P., Santos C.C., et al. The role of conserved residues of chagasin in the inhibition of cysteine peptidases. FEBS Lett 582 (2008) 485-490
46. Smith B.O., Picken N.M.C., Westrop G.D., et al. The structure of Leishmania mexicana ICP provides evidence for convergent evolution of cysteine peptidase inhibitors. J Biol Chem 281 (2006) 5821-5828
47. Santos C.C., Sant'Anna C., Terres A., Cunha-e Silva N.L., Scharfstein J., and Lima A.P.C. Chagasin, the endogenous cysteine protease inhibitor of Trypanosoma cruzi, modulates parasite differentiation and invasion of mammalian cells. J Cell Sci 118 (2005) 901-915