Purification and characterization of the western spruce budworm larval midgut proteinases and comparison of gut activities of laboratory-reared and field-collected insects

Insect Biochemistry and Molecular Biology

Volumn 29, Issue 5, 1999, Pages 405-415

  Valaitis, Algimantas P ^a   Augustin, Sylvie ^b   Clancy, Karen M ^a  

^a USDA FOREST SERVICE   (United States)

^b Inst Natl de la Rech Agronom   (France)

Author keywords

Aminopeptidase; Carboxypeptidase; Choristoneura occidentalis; Chymotrypsin; Laboratory and field collected western spruce budworm; Trypsin

Indexed keywords

CHYMOTRYPSIN; ENZYME INHIBITOR; MICROSOMAL AMINOPEPTIDASE; PROTEINASE; TRYPSIN; TRYPSIN INHIBITOR;

AMINO TERMINAL SEQUENCE; ANIMAL; ARTICLE; DIGESTIVE SYSTEM; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYMOLOGY; INSECT; ISOLATION AND PURIFICATION; LARVA; METABOLISM; MIDGUT; MOTH; NONHUMAN; PEST CONTROL;

ANIMALS; ANTIGENS, CD13; CHYMOTRYPSIN; DIGESTIVE SYSTEM; ENZYME INHIBITORS; LARVA; MOTHS; TRYPSIN; TRYPSIN INHIBITORS;

ANIMALIA; CHORISTONEURA FUMIFERANA; CHORISTONEURA OCCIDENTALIS; HEXAPODA; INSECTA; INVERTEBRATA; LEPIDOPTERA; PICEA;

EID: 0033137068     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0965-1748(99)00017-X     Document Type: Article

References (53)

1. Amarant T., Burkhart W., LeVine H., Arocha-Pinango C.L., Parikh I. Isolation and complete amino acid sequence of two fibrinolytic proteinases from the toxic Saturnid caterpillar Lonomia achelous. Biochem. Biophys. Acta. 1079:1991;214-221.
2. Applebaum S.W. Biochemistry of digestion. Kerkut G.A., Gilbert L.I. Comprehensive Insect Physiology, Biochemistry and Pharmacology, vol. 4. 1985;279-311 Pergamon Press, Oxford.
3. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
4. Broadway R.M. Characterization and ecological implications of midgut proteolytic activity in Pieris rapae and Trichoplusia ni. J. Chem. Ecol. 15:1989;2101-2113.
5. Broadway R.M. Are insects resistant to plant proteinase inhibitors? J. Insect Physiol. 41:1995;107-116.
6. Casu R.E., Pearson R.D., Jarmey J.M., Cadogan L.C., Riding G.A., Tellman R.L. Excretory/secretory chymotrypsin from Lucilia cuprina: purification, enzymatic specificity and amino acid sequence deduced from mRNA. Insect Molec. Biol. 3:1994;201-211.
7. Christeller J.T., Laing W.A., Markwick N.P., Burgess E.P.J. Midgut protease activities in 12 phytophagous lepidopteran larvae: dietary and protease inhibitor interactions. Insect Biochem. Molec. Biol. 22:1992;735-746.
8. Christeller J.T., Gatehouse A.M.R., Laing W.A. The interaction of the elastase inhibitor, Eglin c, with insect digestive endopeptidases: effect of pH on the dissociation constants. Insect Biochem. Molec. Biol. 24:1994;103-109.
9. Clancy K.M. Multiple-generation bioassay for investigating western spruce budworm (Lepidoptera: Tortricidae) Nutritional Ecology. Environ. Entomol. 20:1991;1363-1374.
10. Del Mar E.G., Largman C., Brodick J.W., Geokas M.C. A sensitive new substrate for chymotrypsin. Anal. Biochem. 99:1979;316-320.
11. Del Mar E.G., Largman C., Brodick J.W., Fassett M., Geokas M.C. Substrate specificity of human pancreatic elastase 2. Biochemistry. 19:1980;271-278.
12. Erlanger B.F., Kokowsky N., Cohen W. The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 95:1961;271-278.
13. Euguchi M., Iwamoto A. Alkaline proteases in the midgut tissue and digestive fluid of the silkworm, Bombyx mori. Insect Biochem. 6:1976;491-496.
14. Ferreira C., Ribeiro A.F., Terra W.R. Fine structure of the larval midgut of the fly Rhynchosciara and its physiological implications. J. Insect Physiol. 27:1981;559-570.
15. Ferreira C., Capella A.N., Sitnik R., Terra W.R. Properties of the digestive enzymes and the permeability of the peritrophic membrane of Spodoptera frugiperda (Lepidoptera) larvae. Comp. Biochem. Physiol. 107A:1994;631-640.
16. Garczynski S.F., Adang M.J. Bacillus thuringiensis CryIA(c) δ-endotoxin binding aminopeptidase in the Manduca sexta midgut has a glycosyl-phophatidylinositol anchor. Insect Biochem. Molec. Biol. 25:1995;409-415.
17. Gatehouse A.M.R., Gatehouse J.A., Boulter J.A. Isolation and characterization of trypsin inhibitors from cowpea (Vigna unquiculata). Phytochemistry. 19:1980;751-756.
18. Houck E.J., Arcus Y.M., Hardy J.L. Isolation and characterization of brush border fragments from mosquito mesenterons. Arch. Insect Biochem. Physiol. 3:1986;135-146.
19. Johnston K.A., Lee M.J., Brough C., Hilder V.A., Gatehouse A.M.R., Gatehouse J.A. Protease activities in the larval midgut of Heliothis virescens: Evidence for trypsin and chymotrypsin-like enzymes. Insect Biochem. Molec. Biol. 25:1995;375-383.
20. Jongsma M.A., Bakker P.L., Peters J., Bosch D., Stiekema W.J. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc. Natl. Acad. Sci. USA. 92:1995;8041-8045.
21. Keller M., Sneh B., Strizhov N., Prudovsky E., Regev A., Koncz C., Schell J., Zilberstein A. Digestion of δ-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.
22. Klimova O.A., Borukhov S.I., Solovyena N.I., Balaevskaya T.O., Strongin A.Y. The isolation and properties of collagenolytic proteases from crab hepatopancreas. Biochem. Biophys. Res. Commun. 166:1990;1411-1420.
23. Klopenstein N.B., Allen K.K., Avila F.J., Heuchelin S.A., Martinez J., Carman R.C., Hall R.B., Hart E.R., McNabb H.S. Jr. Proteinase inhibitor II gene in transgenic poplar: chemical and biological assays. Biomass and Bioenergy. 12:1997;299-311.
24. Knight P.J.K., Crickmore N., Ellar D.J. The receptor for Bacillus thuringiensis CryIA(c) delta-endotoxin in the brush border membrane of the lepidopteran Manduca sexta is aminopeptidase N. Mol. Microbiol. 11:1994;429-436.
25. Laemmli U.K. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
26. Lecadet M.M., Martouret D. Enzymatic hydrolysis of the crystals of Bacillus thuringiensis by the proteases of Pieris brassicae. J. Invertebr. Pathol. 9:1967;322-330.
27. Lee M.J., Anstee J.H. Endoproteases from the midgut of larval Spodoptera littoralis include a chymotrypsin-like enzyme with an extended binding site. Insect Biochem. Molec. Biol. 25:1995;49-61.
28. Luo K., Sangadala S., Masson L., Mazza A., Brousseau R., Adang M.J. The Heliothis virescens 170 kDa aminopeptidase functions as "Receptor A" by mediating specific Bacillus thuringiensis Cry1A δ-endotoxin binding and pore formation. Insect Biochem. Molec. Biol. 27:1997;735-743.
29. Maneervik B., Guthenberg C. Gluthathione transferase (Human Placenta). Methods Enzymol. 77:1981;231-235.
30. McManus M.T., White D.W.R., McGregor P.G. Accumulation of chymotrypsin inhibitor in transgenic tobacco can effect the growth of insect pests. Transgenic Research. 3:1994;50-58.
31. McMorran A. A synthetic diet for the spruce budworm, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae). Can. Entomol. 97:1965;58-62.
32. Miller J.W., Kramer K.J., Law J.H. Isolation and partial characterization of the larval midgut trypsin from the tobacco hornworm, Manduca sexta, Johannson (Lepidoptera: Sphingidae). Comp. Biochem. Physiol. 48B:1974;117-129.
33. Milne R., Kaplan H. Purification and characterization of a trypsin-like digestive enzyme from spruce budworm (Choristoneura fumiferana) responsible for the activation of δ-endotoxin from Bacillus thuringiensis. Insect Biochem. Molec. Biol. 23:1993;663-673.
34. Oppert B., Kramer K.J., Johnson D.E., MacIntosh S.C., McGaughey W.H. Altered protoxin activation by midgut enzymes from a Bacillus thuringiensis resistant strain of Plodia interpuntella. Biochem. Biophys. Res. Comm. 198:1994;940-947.
35. Oppert B., Kramer K.J., Johnson D., Upton S.J., McGaughey W.H. Luminal proteinases from Plodia interpunctella and the hydrolysis of Bacillus thuringiensis Cry1A(c) protoxin. Insect Biochem. Molec. Biol. 26:1996;571-583.
36. Peterson A.M., Barillas-Mury C.V., Wells M.A. Sequence of three cDNAs encoding an alkaline midgut trypsin from Manduca sexta. Insect Biochem. Molec. Biol. 24:1994;463-471.
37. Peterson A.M., Fernando G.J.P., Wells M.A. Purification, characterization and cDNA sequence of an alkaline chymotrypsin from the midgut of Manduca sexta. Insect Biochem. Molec. Biol. 25:1995;765-774.
38. + efflux in vitro. J. Biol. Chem. 269:1994;10088-10092.
39. Santos C.D., Terra W.R. Plasma membrane-associated amylase and trypsin. Insect Biochem. 14:1984;587-594.
40. Santos C.D., Ribeiro A.F., Terra W.R. Differential centrifugation, calcium precipitation, and ultrasonic disruption of midgut cells of Erinnyis ello caterpillars. Purification of cell microvilli and inferences concerning secretory mechanisms. Can. J. Zool. 64:1986;490-500.
41. Shwert G.W., Takenaka Y. A spectrophotometric determination of trypsin and chymotrypsin. Biochim. Biophys. Acta. 16:1955;570-575.
42. Takesue S., Yokota K., Miyajima S., Taguchi R., Ikezawa H., Takesue Y. Partial release of aminopeptidase N from larval midgut cell membranes of the silkworm, Bombyx mori, by phosphatidylinositol-specific phopholipase C. Comp. Biochem. Physiol. 102:1992;7-11.
43. Terra W.R. Evolution of digestive systems of insects. Ann. Rev. Entomol. 35:1990;181-200.
44. Terriere L.C. Induction of detoxification enzymes in insects. Ann. Rev. Entomol. 29:1984;71-88.
45. Tomita M., Obara H., Takesue Y., Tamura H., Miyajima S., Taguchi R., Ikezawa H. Glycosylphophatidylinositol-anchoring aminopeptidase N from the plasma membrane of larval midgut epithelial cells of the silkworm, Bombyx mori. Int. J. Biochem. 26:1994;977-986.
46. Tsai I.-H., Chuang K.-L., Chuang J.L. Chymotrypsins in digestive tracts of crustacean decapods (Shrimps). Comp. Biochem. Physiol. 85:1986;235-239.
47. Valaitis A.P. Gypsy moth midgut proteinases: purification and characterization of luminal trypsin, elastase and the brush border membrane leucine aminopeptidase. Insect Biochem. Molec. Biol. 25:1995;139-149.
48. Valaitis A.P., Lee Mi K., Rajamohan F., Dean D.H. Brush border membrane aminopeptidase-N in the midgut of the gypsy moth serves as the receptor for the cryIA(c) δ-endotoxin of Bacillus thuringiensis. Insect Biochem. Molec. Biol. 25:1995;1143-1151.
49. Wang S., Magoulas C., Hickey D.A. Isolation and characterization of a full-length trypsin-encoding cDNA clone from the lepidopteran insect, Choristoneura fumiferana. Gene. 136:1993;375-376.
50. Wolfersberger M.G. Enzymology of plasma membranes of insect intestinal cells. Am. Zool. 24:1984;187-197.
51. Wolfersberger M., Luethy P., Maurer A., Parenti P., Sacchi F.V., Giordana B., Hanozet G.M. Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly (Pierris brassicae). Comp. Biochem. Physiol. 86A:1987;301-308.
52. Yun Y., Davis R.L. Levels of RNA from a family of putative serine protease genes are reduced in Drosophila melanogaster dunce mutants and are regulated by cyclic AMP. Mol. Cell. Biol. 9:1989;692-700.
53. Zhu Y.-C., Oppert B., Kramer K.J., McGaughey W.H., Dowdy A.K. cDNAs for a chymotrypsinogen-like protein from two strains of Plodia interpunctella. Insect Biochem. Molec. Biol. 27:1997;1027-1037.