Stage-specific gut proteinases of the cotton stainer bug Dysdercus peruvianus: Role in the release of entomotoxic peptides from Canavalia ensiformis urease

Insect Biochemistry and Molecular Biology

Volumn 38, Issue 11, 2008, Pages 1023-1032

  Piovesan, Angela R ^a   Stanisçuaski, Fernanda ^a   Marco Salvadori, Juliana ^a   Real Guerra, Rafael ^a   Defferrari, Marina S ^a   Carlini, Célia R ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Dysdercus peruvianus; Enzyme inhibitor; Insecticidal peptide; Proteolytic enzyme; Urease

Indexed keywords

AZOCASEIN; CASEIN; INSECT PROTEIN; PEPTIDE HYDROLASE; TOXIN; UREASE;

ANIMAL; ARTICLE; CANAVALIA; ELECTROSPRAY MASS SPECTROMETRY; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; HETEROPTERA; HYDROLYSIS; LIQUID CHROMATOGRAPHY; METABOLISM; NYMPH; PHYSIOLOGY;

ANIMALS; CANAVALIA; CASEINS; CHROMATOGRAPHY, LIQUID; HETEROPTERA; HYDROLYSIS; INSECT PROTEINS; NYMPH; PEPTIDE HYDROLASES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TOXINS, BIOLOGICAL; UREASE;

CANAVALIA; CANAVALIA ENSIFORMIS; DYSDERCUS PERUVIANUS; GOSSYPIUM HIRSUTUM; HEXAPODA; WUPATKIUS SEMO;

EID: 55749099956     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2008.09.004     Document Type: Article

References (41)

1. Barret A.J., Rawlings N.D., and Woessner J.F. Handbook of Proteolytic Enzymes (1998), Academic Press, San Diego 1666 pp.
2. Brinkworth R.I., Provic P., Loukas A., and Brindley P.J. Hemoglobin-degrading, aspartic proteases of blood-feeding parasites. J. Biol. Chem. 276 (2001) 38844-38851
3. Carlini C.R., and Guimarães J.A. Isolation and characterization of a toxic protein from Canavalia ensiformis (jack bean) seeds, distinct from concanavalin A. Toxicon 19 (1981) 667-676
4. Carlini C.R., Oliveira A.E., Azambuja P., Xavier-Filho J., and Wells M.A. Biological effects of canatoxin in different insect models. Evidence for a proteolytic activation of the toxin by insect cathepsinlike enzymes. J. Econ. Entomol. 90 (1997) 340-348
5. Cristofoletti P.T., Ribeiro A.F., Deraison C., Rahbé Y., and Terra W.R. Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J. Insect Physiol. 49 (2003) 11-24
6. Dahl S.W., Halkier T., Lauritzen C., Dolenc I., Pedersen J., Turk V., and Turk B. Human recombinant pro-dipeptidyl peptidase I (cathepsin C) can be activated by cathepsins L and S but not by autocatalytic processing. Biochemistry 40 (2001) 1671-1678
7. Di{dotless}az-Mendoza M., Ortego F., Garci{dotless}a de Lacoba M., Magana C., de la Poza M., Farinos G.P., Castanera P., and Hernadez-Crespo P. Diversity of trypsins in the Mediterranean corn borer Sesamia nonagrioides (Lepidoptera: Noctuidae), revealed by nucleic acid sequences and enzyme purification. Insect Biochem. Mol. Biol. 35 (2005) 1005-1020
8. Drapeau G.R. Substrate specificity of a proteolytic enzyme isolated from a mutant of Pseudomonas fragi. J. Biol. Chem. 255 (1980) 839-840
9. Eggleson K.K., Duffin K.L., and 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
10. Ferreira-DaSilva C.T., Gombarovits M.E., Masuda H., Oliveira C.M., and Carlini C.R. Proteolytic activation of canatoxin, a plant toxic protein, by insect cathepsin-like enzymes. Arch. Insect Biochem. Physiol. 44 (2000) 162-171
11. Follmer C. Insights into the role and structure of plant ureases. Phytochemistry 69 (2008) 18-28
12. Follmer C., Barcellos G.B.S., Zingali R.B., Machado O.L.T., Alves E.W., Barja-Fidalgo C., Guimarães J.A., and Carlini C.R. Canatoxin, a toxic protein from jack beans (Canavalia ensiformis), is a variant from of urease (EC. 3.5.1.5): biological effects of urease independent of its ureolytic activity. Biochem. J. 360 (2001) 217-224
13. Follmer C., Real-Guerra R., Wassermann G.E., Olivera-Severo D., and Carlini C.R. Jackbean, soybean and Bacillus pasteurii ureases: biological effects unrelated to ureolytic activity. Eur. J. Biochem. 271 (2004) 1357-1363
14. Follmer C., Wassermann G., and Carlini C.R. Separation of Jack bean (Canavalia ensiformis) urease isoforms by immobilized metal affinity chromatography and characterization of insecticidal properties unrelated to ureolytic activity. Plant Sci. 167 (2004) 241-246
15. Gallo D. Manual de Entomologia Agrícola. second ed. (1988), CERES, São Paulo 649 pp.
16. Hagmann M.L. Peptidyl-Asp Metalloendopeptidase. Handbook of Proteolytic Enzymes. second ed. (2004), Elsevier, London 1037-1039
17. Hawkins C.J., Yoo S.J., Peterson E.P., Wang S.L., Vernooy S.Y., and Hay B.A. The Drosophila caspase DRONC cleaves following glutamate or aspartate and is regulated by DIAP1, HID, and GRIM. J. Biol. Chem. 275 (2000) 27084-27093
18. Keller M., Sneh B., Strizhov N., Prudovsky E., Regev A., Koncz C., Schell J., and Zilberstein A. Digestion of delta-endotoxin by gut proteases may explain reduced sensitivity of advanced instar larvae of Spodoptera littoralis to CryIC. Insect Biochem. Mol. Biol. 26 (1996) 365-373
19. MEROPS, http://merops.sanger.ac.uk/.
20. Miller C.G. Dipeptidase E. Handbook of Proteolytic Enzymes. second ed. (2004), Elsevier, London 2033-2035
21. Mobley H.L., Island M.D., and Hausinger R.P. Molecular biology of microbial ureases. Microbiol. Rev. 59 (1995) 451-480
22. Mulinari, F., Freitas-Silva, M.A., Grossi-De-Sa, M.F., Moraes, M.G., Kurtenbach, E., Carlini, C.R., 2004. Toxina Praguicida, Construção Gênica e Método de Controle de Pragas. Patent registered at National Institute for Intellectual Property (INPI). Brazil; 08/04/2004 [protocol BRPI0403435A].
23. Mulinari F., Stanisçuaski F., Bertholdo-Vargas L.R., Postal M., Oliveira-Neto O.B., Ridgen D.J., Grossi-de-Sá M.F., and Carlini C.R. Jaburetox-2Ec: an insecticidal peptide derived from an isoform of urease from the plant Canavalia ensiformis. Peptides 28 (2007) 2042-2050
24. Nemoto T., Sato N., Iwanari H., Yamashita H., and Takagii T. Domain structures and immunogenic regions of the 90-kDa heat-shock protein (HSP90). J. Biol. Chem. 272 (1997) 26179-26187
25. Peumans W.J., and Van Damme E.J. Lectin as plant defense proteins. Plant Physiol. 109 (1995) 347-352
26. Polacco J.C., and Holland M.A. Roles of urease in plant cells. Int. Rev. Cytol. 145 (1993) 65-103
27. Renard G., Garcia J.F., Cardoso F.C., Richter M.F., Sakanari J.A., Ozaki L.S., Termignoni C., and Masuda A. Cloning and functional expression of a Boophilus microplus cathepsin L-like enzyme. Insect Biochem. Mol. Biol. 30 (2000) 1017-1026
28. Silva C.P., and Terra W.R. Digestive and absorptive sites along the midgut of the cotton seed sucker bug Dysdercus peruvianus (Hemiptera: Pyrrhocoridae). Insect Biochem. Mol. Biol. 24 (1994) 493-505
29. Silva C.P., Ribeiro A.F., and Terra W.R. Enzyme markers and isolation of the microvillar and perimicrovillar membranes of Dysdercus peruvianus (Hemiptera: Pyrrhocoridae) midgut cells. Insect Biochem. Mol. Biol. 26 (1996) 1011-1018
30. Sirko A., and Brodzik R. Plant ureases: role and regulation. Acta Biochim. Pol. 47 (2000) 1189-1195
31. Sorgine M.H., Logullo C., Zingali R.B., Paiva-Silva G.O., Juliano L., and Oliveira P.L. A heme-binding aspartic proteinase from the eggs of the hard tick Boophilus microplus. J. Biol. Chem. 275 (2000) 28659-28665
32. Stanisçuaski F., Ferreira-Dasilva C.T., Mulinari F., Pires-Alves M., and Carlini C.R. Insecticidal effects of canatoxin on the cotton stainer bug Dysdercus peruvianus (Hemiptera: Pyrrhocoridae). Toxicon 45 (2005) 753-760
33. Terra W.R., and Ferreira C. Insect digestive enzymes: properties, compartmentalization and function. Comp. Biochem. Physiol. 109 (1994) 1-62
34. Terra W.R., Ferreira C., Jordão B.P., and Dillon R.J. Digestive Enzymes. Biology of the Insect Midgut (1996), Chapman & Hall, London 153-194
35. Tomazzeto G., Mulinari F., Staniscuaski F., Settembrini B.P., Carlini C.R., and Ayub M.A.Z. Expression kinetics and plasmid stability of recombinant E. coli encoding urease-derived peptide with bioinsecticide activity. Enzyme Microb. Technol. 41 (2007) 821-827
36. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76 (1979) 4350-4354
37. Weber K., and Osborn M. The reliability of molecular weight determinations by dodecyl sulfate polyacrylamide gel electrophoresis. J. Biol. Chem. 244 (1969) 4406-4412
38. Whitaker J.R., and Perez-Villasenor J. Chemical modification of papain. 1. Reaction with the chloromethyl ketones of phenylalanine and lysine and with phenylmethylsulphonyl fluoride. Arch. Biochem. Biophys. 124 (1968) 70-78
39. Wilhite S.E., Elden T.C., Brzin J., and Smigocki A.C. Inhibition of cysteine and aspartyl proteinases in the alfalfa weevil midgut with biochemical and plant-derived proteinase inhibitors. Insect Biochem. Mol. Biol. 30 (2000) 1181-1188
40. Wilk S. Beta-aspartyl peptidase. Handbook of Proteolytic Enzymes. second ed (2004), Elsevier, London 2115-2116
41. Wright M.K., Brandt S.L., Coudron T.A., Wagner R.M., Habibi J., Backus E.A., and Huesing J.E. Characterization of digestive proteolytic activity in Lygus hesperus knight (Hemiptera: Miridae). J. Insect Physiol. 52 (2006) 717-728