Cruzipain, the major cysteine proteinase from the protozoan parasite Trypanosoma cruzi

Biological Chemistry

Volumn 378, Issue 1, 1997, Pages 1-10

  Cazzulo, Juan José ^a   Stoka, Veronika ^b   Turk, Vito ^b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

Chagas disease; Cruzipain; Cysteine proteinase; Trypanosoma cruzi

Indexed keywords

CRUZIPAIN; CYSTEINE PROTEINASE; CYSTEINE PROTEINASE INHIBITOR; EPITOPE; HYDROLASE INHIBITOR;

CARBOXY TERMINAL SEQUENCE; CHAGAS DISEASE; HUMAN; NONHUMAN; PARASITE SURVIVAL; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTOZOON; REVIEW; TRYPANOSOMA CRUZI;

AMINO ACID SEQUENCE; ANIMALS; CATALYSIS; CYSTEINE ENDOPEPTIDASES; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; TRYPANOSOMA CRUZI;

PROTOZOA; TRYPANOSOMA; TRYPANOSOMA CRUZI; TRYPANOSOMATIDAE;

EID: 0031049020     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (73)

1. Agarwal, S.K. (1990). Proteases cathepsins - A view. Biochemical Education 18, 67-72.
2. Ashall, F. (1990). Characterization of an alkaline peptidase of Trypanosoma cruzi. Mol. Biochem. Parasitol. 38, 77-88.
3. Ashall, R, Harris, D., Roberts, H., Healy, N., and Shaw, E. (1990). Substrate specificity and inhibitor sensitivity of a trypanosomatid alkaline peptidase. Biochim. Biophys. Acta 1035, 293-299.
4. Åslund, L., Henriksson, J., Campetella, O., Frasch, A.C.C., Pettersson, U., and Cazzulo, J.J. (1991). The C-terminal extension of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi Mol. Biochem. Parasitol. 45, 345-348.
5. Avila, J.L., Casanova, M.A., Avila, A., and Bretaňa, A. (1979). Acid and neutral hydrolases in Trypanosoma cruzi. Characterization and assay. J. Protozool. 26, 304-311.
6. Berti, P.J., and Storer, A.C. (1995). Alignment/phylogeny of the papain superfamily of cysteine proteases. J. Mol. Biol. 246, 273-283.
7. Bonaldo, M.C., D'Escoffier, L.N., Salles, J.M., and Goldenberg, S. (1991). Characterization and expression of proteases during Trypanosoma cruzi metacyclogenesis. Exp. Parasitol. 73, 44-51.
8. Bongertz, V., and Hungerer, K.D. (1978). Trypanosoma cruzi: Isolation and characterization of a protease. Exp. Parasitol. 45, 8-18.
9. Bontempi, E., and Cazzulo, J.J. (1990). Digestion of human immunoglobulin G by the major cysteine proteinase (cruzipain) from Trypanosoma cruzi. FEMS Microbiol. Lett. 70, 337-342.
10. Bontempi, E., Franke de Cazzulo, B.M., Ruiz, A.M., and Cazzulo, J.J. (1984). Purification and some properties of an acidic protease from epimastigotes of Trypanosoma cruzi. Comp. Biochem. Physiol. 77B, 599-604.
11. 2+-signaling factor for mammalian cells. J. Biol. Chem. 270, 5172-5180.
12. Campetella, O., Martínez, J., and Cazzulo, J.J. (1990). A major cysteine proteinase is developmentally regulated in Trypanosoma cruzi. FEMS Microbiol. Lett. 67, 145-150.
13. Campetella, O., Henriksson, J., Aslund, L., Frasch, A.C.C., Pettersson, U., and Cazzulo, J.J. (1992). The major cysteine proteinase (Cruzipain) from Trypanosoma cruzi is encoded by multiple polymorphic tandemly organized genes located on different chromosomes. Mol. Biochem. Parasitol. 50, 225-234.
14. Cazzulo, J.J. (1984). Protein and aminoacid catabolism in Trypanosoma cruzi. Comp. Biochem. Physiol. 79B, 309-320.
15. Cazzulo, J.J. (1991). Proteinases of Trypanosoma cruzi. In: Biochemistry of Parasitic Protozoa, G.H. Coombs and M.J. North, eds. (London, Washington D.C.: Taylor & Francis Ltd.), pp. 191-199.
16. Cazzulo, J.J., and Frasch, A.C.C. (1992). SAPA/trans-sialidase and cruzipain: two antigens from Trypanosoma cruzi contain immunodominant but enzymatically inactive domains. FASEB J. 6, 3259-3264.
17. Cazzulo, J.J., Couso, R., Raimondi, A., Wernstedt, C., and Hellman, U. (1989). Further characterization and partial amino acid sequence of a cysteine proteinase from Trypanosoma cruzi. Mol. Biochem. Parasitol. 33, 33-41.
18. Cazzulo, J.J., Cazzulo Franke, M.C., Martínez, J., and Franke de Cazzulo, B.M. (1990). Some kinetic properties of a cysteine proteinase (Cruzipain) from Trypanosoma cruzi. Biochim. Biophys. Acta 1037, 186-191.
19. Cazzulo, J.J., Martínez, J., Parodi, A.J.A., Wernstedt, C., and Hellman, U. (1992). On the post-translational modifications at the C-terminal domain of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi. FEMS Microbiol. Lett. 700, 411-416.
20. Cazzulo, J.J., Labriola, C., Parussini, F., Duschak, V., Martínez, J., and Franke de Cazzulo, B.M. (1995). Cysteine proteinases in Trypanosoma cruzi and other Trypanosomatid parasites. Acta Chim. Slovenica 42, 409-418.
21. Cazzulo, J.J., Bravo, M., Raimondi, A., Engström, U., Lindeberg, G., and Hellman, U. (1996). Hydrolysis of synthetic peptides by cruzipain, the major cysteine proteinase from Trypanosoma cruzi, provides evidence for self-processing and the possibility of more specific substrates for the enzyme. Cell. Mol. Biol. 42, 691-696.
22. Coombs, G.H., Robertson, C.D., and Mottram, J.C. (1991). Cysteine proteinases of leishmanias. In: Biochemistry of Parasitic Protozoa, G.H. Coombs and M.J. North, eds. (London, Washington D.C.: Taylor & Francis Ltd.), pp. 208-220.
23. Eakin, A.E., Bouvier, J., Sakanari, J.A., Craik, C.S., and McKerrow, J.H. (1990). Amplification and sequencing of genomic DNA fragments encoding cysteine proteinases from protozoan parasites. Mol. Biochem. Parasitol. 39, 1-8.
24. Eakin, A.E., Mills, A.A., Harth, G., McKerrow, J.H., and Craik, C.S. (1992). The sequence, organization, and expression of the major cysteine proteinase (cruzain) from Trypanosoma cruzi. J. Biol. Chem. 267, 7411-7420.
25. Eakin, A.E., McGrath, M.E., McKerrow, J.H., Fletterick, R.J., and Craik, C.S. (1993). Production of crystallizable cruzain, the major cysteine proteinase from Trypanosoma cruzi. J. Biol. Chem. 268, 6115-6118.
26. Etges, R., and Bouvier, J. (1991). The promastigote surface proteinase of Leishmania. In: Biochemistry of Parasitic Protozoa, G.H. Coombs and M.J. North, eds. (London, Washington D.C.: Taylor & Francis Ltd.), pp. 221-233.
27. Franke de Cazzulo, B.M., Martínez, M., North, M.J., Coombs, G.H., and Cazzulo, J.J. (1994). Effect of proteinase inhibitors on growth and differentiation of Trypanosoma cruzi. FEMS Microbiol. Lett. 124, 81-86.
28. Fresno, M., Hernández-Munaín, C., de-Diego, J., Rivas, L., Scharfstein, J., and Bonay, P. (1994). Trypanosoma cruzi: identification of a membrane cysteine proteinase linked through a GPI anchor. Brazilian J. Med. Biol. Res. 27, 431-437.
29. Greig, S., and Ashall, F. (1990). Electrophoretic detection of Trypanosoma cruzi peptidases. Mol. Biochem. Parasitol. 39, 31-38.
30. Harth, G., Andrews, N., Mills, A.A., Engel, J.C., Smith, R., and McKerrow, J.H. (1993). Peptidefluoromethyl ketones arrest intracellular replication and intercellular transmission of Trypanosoma cruzi. Mol. Biochem. Parasitol. 58, 17-24.
31. Healy, N., Greig, S., Enahoro, H., Roberts, H., Drake, L., Shaw, E., and Ashall, F. (1992). Detection of peptidases in Trypanosoma cruzi epimastigotes using chromogenic and fluorogenic substrates. Parasitology 104, 315-322.
32. Hellman, U., Wernstedt, C., and Cazzulo, J.J. (1991). Self-proteolysis of the cysteine proteinase, cruzipain, from Trypanosoma cruzi gives a major fragment corresponding to its C-terminal domain. Mol. Biochem. Parasitol. 44, 15-22.
33. Itw, S., and Camargo, E.P. (1977). Proteolytic activities in cell extracts of Trypanosoma cruzi. J. Protozool. 24, 591-595.
34. Khamphuis, I.G., Kalk, K.H., Swarte, M.B.A., and Drenth, J. (1984). Structure of papain refined at 1.65 Å resolution. J. Mol. Biol. 179, 233-256.
35. Khouri, H.E., Vernet, T., Ménard, R., Parlati, F., Laflamme, P., Tessier, D.C., Gour-Salin, B., Thomas, D.Y., and Storer, A.C. (1991). Engineering of papain: Selective alteration of substrate specificity by site-directed mutagenesis. Biochemistry 30, 8929-8936.
36. Kos, J., Arbanas, V., Turk, V., and Maksimenko, A.V. (1986). Chicken egg white cystatin as a ligand for affinity chromatography. In: Cysteine Proteinases and Their Inhibitors, V. Turk, ed. (Berlin, New York: Walter de Gruyter), pp. 569-575.
37. Krettli, A., Thomas, N., and Eisen, H. (1980). Escape mechanisms of Trypanosoma cruzi from the host immune system. In: Les Colloques de l'INSERM. Cancer Immunology and Parasite Immunology, Vol. 97, L. Israel, P. Lagrange and J.C. Salomon, eds. (Paris: INSERM), pp. 553-558.
38. Labriola, C., and Cazzulo, J.J. (1995). Purification and partial characterization of a cysteine proteinase from Trypanosoma rangeli. FEMS Microbiol. Lett., 129, 143-148.
39. Labriola, C., Sousa, M., and Cazzulo, J.J. (1993). Purification of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi by affinity chromatography. Biological Res. 26, 101-107.
40. Labriola, C., Cazzulo, J.J., and Parodi, A.J. (1995). Retention of glucose units added by the UDPGLC: Glycoprotein glucosyltransferase delays exit of glycoproteins from the endoplasmic reticulum. J. Cell Biol. 130, 771-779.
41. Lima, A.P.C.A., Scharfstein, J., Storer, A.C., and Ménard, R. (1992). Temperature-dependent substrate inhibition of the cysteine proteinase (GP 57/51) from Trypanosoma cruzi. Mol. Biochem. Parasitol. 56, 335-338.
42. Lima, A.P.C.A., Tessier, D.C., Thomas, D.Y., Scharfstein, J., Storer, A.C., and Vernet, T. (1994). Identification of new cysteine protease gene isoforms in Trypanosoma cruzi. Mol. Biochem. Parasitol. 67, 333-338.
43. Lonsdale-Eccles, J.D. (1991). Proteinases of African Trypanosomes. In: Biochemistry of Parasitic Protozoa, G.H. Coombs and M.J. North, eds. (London, Washington D.C.: Taylor & Francis Ltd.), pp. 200-207.
44. Malchiodi, E.L., Chiaramonte, M.G., Martínez, J.A., Zwirner, N.W., Margni, R.A., and Cazzulo, J.J. (1993). Identity of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi and an antigen (Ag163B6) isolated with a monoclonal antibody. Immunol. Lett. 35, 59-62.
45. Martínez, J. (1995). Study of structural aspects and antigenic properties of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi. Ph. D. Thesis, Universidad de Buenos Aires.
46. Martínez, J., and Cazzulo, J.J. (1992). Anomalous electrophoretic behaviour of the major cysteine proteinase (cruzipain) from Trypanosoma cruzi in relation to its apparent molecular weight. FEMS Microbiol. Lett. 95, 225-230.
47. Martínez, J., Silberstein, E., and Cazzulo, J.J. (1989). Cysteine proteinase activities in epimastigotes of Trypanosoma cruzi: an electrophoretic study. Anales Asoc. Quím. Argentina 77, 113-117.
48. Martínez, J., Campetella, O., Frasch, A.C.C., and Cazzulo, J.J. (1991). The major cysteine proteinase (Cruzipain) from Trypanosoma cruzi is antigenic in human infections. Infect. Immun. 59, 4275-4277.
49. Martínez, J., Campetella, O., Frasch, A.C.C., and Cazzulo, J.J. (1993). The reactivity of sera from chagasic patients against different fragments of cruzipain, the major cysteine proteinase from Trypanosoma cruzi, suggests the presence of defined antigenic and catalytic domains. Immunol. Lett. 35, 191-196.
50. McGrath, M.E., Eakin, A.E., Engel, J.C., McKerrow, J.H., Craik, C.S., and Fletterick, R.J. (1995). The crystal structure of cruzain: a therapeutic target for Chagas' disease. J. Mol. Biol. 247, 251-259.
51. McKerrow, J.H., McGrath, M.E., and Engel, J.C. (1995). The cysteine protease of Trypanosoma cruzi as a model for antiparasite drug design. Parasitol. Today 11, 279-282.
52. Meirelles, M.N.L., Juliano, L., Carmona, E., Silva, S.G., Costa, E.M., Murta, A.C.M., and Scharfstein, J. (1992). Inhibitors of the major cysteinyl proteinase (GP57/51) impair host cell invasion and arrest the intracellular development of Trypanosoma cruzi in vitro. Mol. Biochem. Parasitol. 52, 175-184.
53. Metzner, S.I., Sousa, M.C., Hellman, U., Cazzulo, J.J., and Parodi, A.J. (1996). The use of UDP-Glc: glycoprotein glucosyltransferase for radiolabeling protein-linked high mannose-type oligosaccharides. Cell. Mol. Biol. 42, 631-635.
54. Mottram, J.C., North, M.J., Barry, J.D., and Coombs, G.H. (1989). A cysteine proteinase cDNA from Trypanosoma brucei predicts an enzyme with an unusual C-terminal extension. FEBS Lett. 258, 211-215.
55. Murta, A.C.M., Persechini, P.M., de Souto Padrón, T., de Souza, W., Guimaraes, J.A., and Scharfstein, J. (1990). Structural and functional identification of GP57/51 antigen of Trypanosoma cruzi as a cysteine proteinase. Mol. Biochem. Parasitol. 43, 27-38.
56. North, M.J., Coombs, G.H., and Barry, J.D. (1983). A comparative study of the proteolytic enzymes of Trypanosoma brucei, T. equiperdum, T. evansi, T. vivax, Leishmania tarentolae and Crithidia fasciculata. Mol. Biochem. Parasitol. 9, 19-26.
57. Parodi, A.J., Labriola, C., and Cazzulo, J.J. (1995). The presence of complex-type oligosaccharides at the C-terminal domain glycosylation site of some molecules of cruzipain. Mol. Biochem. Parasitol. 69, 247-255.
58. Piras, M.M., Henríquez, D., and Piras, R. (1985). The effect of proteolytic enzymes and protease inhibitors on the interaction Trypanosoma cruzi-fibroblasts. Mol. Biochem. Parasitol. 14, 151-163.
59. Raimondi, A., Wernstedt, C., Hellman, U., and Cazzulo, J.J. (1991). Degradation of oxidized insulin A and B chains by the major cysteine proteinase (Cruzipain) from Trypanosoma cruzi epimastigotes. Mol. Biochem. Parasitol. 49, 341-344.
60. Rangel, H.A., Araújo, P.M.F., Repka, D., and Costa, M.G. (1981). Trypanosoma cruzi: Isolation and characterization of a proteinase. Exp. Parasitol. 52, 199-209.
61. Rawlings, N.D., and Barrett, A.J. (1994). Families of cysteine peptidases. Methods Enzymol. 244, 461-486.
62. Santana, J.M., Grellier, P., Rodier, M.H., Schrevel, J., and Teixeira, A. (1992). Purification and characterization of a new 120 kda alkaline proteinase of Trypanosoma cruzi. Biochem. Biophys. Res. Commun. 187, 1466-1473.
63. Scharfstein, J., Schechter, M., Senna, M., Peralta, J.M., Mendonça-Previato, L., and Miles, M.M. (1986). Trypanosoma cruzi: characterization and isolation of a 57/51,000 m.w. surface glycoprotein (GP57/51) expressed by epimastigotes and blood-stream trypomastigotes. J. Immunol. 137, 1336-1341.
64. Serveau, C., Lalmanach, G., Juliano, M.A., Scharfstein, J., Juliano, L., and Gauthier, F. (1996). Investigation of the substrate specificity of cruzipain, the major cysteine protease of Trypanosoma cruzi, through the use of cystatin-derived substrates and inhibitors Biochem. J. 313, 951-956.
65. Soares, M.J., Souto-Padrón, T., and De Souza, W. (1992). Identification of a large pre-lysosomal compartment in the pathogenic protozoon Trypanosoma cruzi. J. Cell Sci. 102, 157-167.
66. Souto-Padrón, T. Campetella, O., Cazzulo, J.J., and de Souza, W. (1990). Cysteine proteinase in Trypanosoma cruzi: immunocytochemical localization and involvement in parasite-host cell interaction. J. Cell Sci. 96, 485-490.
67. Souza, A.E., Waugh, S., Coombs, G.H., and Mottram, J.C. (1992). Characterization of a multi-copy gene for a major stage-specific cysteine proteinase of Leishmania mexicana. FEBS Lett. 311, 124-127.
68. Stoka, V., Nycander, M., Lenarčič, B., Labriola, C., Cazzulo, J.J., Björk, I., and Turk, V. (1995). Inhibition of cruzipain, the major cysteine proteinase of the protozoan parasite, Trypanosoma cruzi, by proteinase inhibitors of the cystatin superfamily. FEBS Lett. 370, 101-104.
69. Tomas, A.M., and Kelly, J.M. (1996). Stage regulated expression of cruzipain, the major cysteine protease of Trypanosoma cruzi is independent of the level of RNA. Mol. Biochem. Parasitol. 76, 91-103.
70. Turk, B., Dolenc, I., Turk, V., and Bieth, J.G. (1993). Kinetics of the pH-induced inactivation of human cathepsin L. Biochemistry 32, 375-380.
71. Turk, B., Dolenc, I., Žerovnik, E., Turk, D., Gubenšek, F., and Turk, V. (1994). Human cathepsin B is a metastable enzyme stabilized by specific ionic interactions associated with the active site. Biochemistry 33, 14800-14806.
72. Vickerman, K. (1976). The diversity of the kinetoplastid flagellates. In: Biology of the Kinetoplastida, Vol. 1, W.H.R. Lumsden and D.A. Evans, eds. (New York: Plenum Press), pp. 1-34.
73. Yokoyama-Yasunaka, J.K.U., Pral, E.M.F., Oliveira, Jr., O.C., Alfieri, S.C., and Stolf, A.M.S. (1994). Trypanosoma cruzi: identification of proteinases in shed components of trypomastigote forms. Acta Tropica 57, 307-315.