Midgut cysteine protease-inhibiting activity in Trichoplusia ni protects the peritrophic membrane from degradation by plant cysteine proteases

Insect Biochemistry and Molecular Biology

Volumn 39, Issue 10, 2009, Pages 726-734

  Li, Changyou ^a,b   Song, Xiaozhao ^a   Li, Guoxun ^b   Wang, Ping ^a  

^a New York State Agricultural Experiment Station   (United States)

^b QINGDAO AGRICULTURAL UNIVERSITY   (China)

Author keywords

Bromelain; Cysteine protease; Cysteine protease inhibition; Midgut; Papain; Peritrophic membrane; Trichoplusia ni

Indexed keywords

CYSTEINE PROTEINASE; CYSTEINE PROTEINASE INHIBITOR; INSECT PROTEIN; VEGETABLE PROTEIN;

ANIMAL; ARTICLE; BRASSICA; CHEMISTRY; DIGESTIVE SYSTEM; ENZYMOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MOTH;

ANIMALS; BRASSICA; CYSTEINE PROTEASES; CYSTEINE PROTEINASE INHIBITORS; DIGESTIVE SYSTEM; INSECT PROTEINS; MOTHS; PLANT PROTEINS;

HELICOVERPA ZEA; HELIOTHIS VIRESCENS; HEXAPODA; LEPIDOPTERA; TRICHOPLUSIA NI;

EID: 70349733407     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2009.08.008     Document Type: Article

References (50)

1. Abedi Z.H., and Brown A.W.A. Peritrophic membrane as a vehicle for DDT and DDE excretion in Aedes aegypti larvae. Ann. Entomol. Soc. Am. 54 (1961) 539-542
2. Barbehenn R.V. Roles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals. Arch. Insect Biochem. Physiol. 47 (2001) 86-99
3. Bell R.A., Owens C.D., Shapiro M., and Tardif J.R. Development of mass-rearing technology. In: Doane C.C., and McManus M.L. (Eds). The Gypsy Moth: Research Toward Integrated Pest Management (1981), US Department of Agriculture, Washington, DC 599-633
4. Berenbaum M. Adaptive significance of midgut pH in larval Lepidoptera. Am. Nat. 115 (1980) 138-146
5. Blum H., Beier H., and Gross H.J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8 (1987) 93-99
6. Broadway R.M. The response of insects to dietary protease inhibitors. In: Michaud D. (Ed). Recombinant Protease Inhibitors in Plants (2000), Eurekah.com, Georgetown, Texas 80-88
7. Brzin J., Rogelj B., Popovic T., Strukelj B., and Ritonja A. Clitocypin, a new type of cysteine protease inhibitor from fruit bodies of mushroom Cliocybe nebularis. J. Biol. Chem. 275 (2000) 20104-20109
8. Clark T.M. Evolution and adaptive significance of larval midgut alkalinization in the insect superorder Mecopterida. J. Chem. Ecol. 25 (1999) 1945-1960
9. Duffey S.S., and Stout M.J. Antinutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32 (1996) 3-37
10. Ehrlich P.R., and Raven P.H. Butterflies and plants: a study in coevolution. Evolution 18 (1964) 586-608
11. Felton G.W., and Gatehouse J.A. Antinutritive plant defence mechanisms. In: Lehane M.J., and Billlingsley P.F. (Eds). Biology of the Insect Midgut (1996), Chapman & Hall, London, New York 373-418
12. Glazer A.N., and Smith E.L. Papain and other plant sulfhydryl proteolytic enzymes. In: Boyer P.D. (Ed). The Enzymes. third ed. vol. 3 (1971), Academic Press, London 501-546
13. Gringorten J.L., Crawford D.N., and Harvey W.R. High pH in the ectoperitrophic space of the larval lepidoteran midgut. J. Exp. Biol. 183 (1993) 353-359
14. Harborne J.B. Introduction of Ecological Biochemistry (1993), Academic Press, San Diego
15. Hegedus D., Baldwin D., O'Grady M., Braun L., Gleddie S., Sharpe A., Lydiate D., and Erlandson M. Midgut proteases from Mamestra configurata (Lepidoptera: Noctuidae) larvae: characterization, cDNA cloning, and expressed sequence tag analysis. Arch. Insect Biochem. Physiol. 53 (2003) 30-47
16. van der Hoorn R.A.L. Plant proteases: from phenotypes to molecular mechanisms. Ann. Rev. Plant Biol. 59 (2008) 191-223
17. Huber M., Cabib E., and Miller L.H. Malaria parasite chitinase and penetration of the mosquito peritrophic membrane. Proc. Natl. Acad. Sci. USA 88 (1991) 2807-2810
18. Jongsma M.A., Bakker P.L., Peters J., Bosch D., and 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
19. Jongsma M.A., Stiekema W.J., and Bosch D. Combating inhibitor-insensitive proteases of insect pests. Trends Biotechnol. 14 (1996) 331-333
20. Koiwa H., Bressan R.A., and Hasegawa P.M. Regulation of protease inhibitors and plant defense. TIPS 2 (1997) 379-384
21. Konno K., Hirayama C., Nakamura M., Tateishi K., Tamura Y., Hattori M., and Kohno K. Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J. 37 (2005) 370-378
22. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
23. Lopez L., Camas A., Shivaji R., Ankala A., Williams P., and Luthe D. Mir1-CP, a novel defense cysteine protease accumulates in maize vascular tissues in response to herbivory. Planta 226 (2007) 517-527
24. Mazumdar-Leighton S., and Broadway R.M. Transcriptional induction of diverse midgut trypsins in larval Agrotis ipsilon and Helicoverpa zea feeding on the soybean trypsin inhibitor. Insect Biochem. Mol. Biol. 31 (2001) 645-657
25. Michaud D. Protease/inhibitor interactions in plant-pest systems. In: Michaud D. (Ed). Recombinant Protease Inhibitors in Plants (2000), Eurekah.com, Georgetown, Texas 1-8
26. Mohan S., Ma P.W., Pechan T., Bassford E.R., Williams W.P., and Luthe D.S. Degradation of the S. frugiperda peritrophic matrix by an inducible maize cysteine protease. J. Insect Physiol. 52 (2006) 21-28
27. Mohan W., Ma P.W., Williams W.P., and Luthe D.S. A naturally occurring plant cysteine protease possesses remarkable toxicity against insect pests and synergizes Bacillus thuringiensis toxin. PLoS One 3 (2008) e1786
28. Monteiro A.C.S., Abrahamson M., Lima A.P.C.A., 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) 3933-3944
29. Pechan T., Ye L., Chang Y., Mitra A., Lin L., Davis F.M., Williams W.P., and Luthe D.S. A unique 33-kD cysteine protease accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other Lepidoptera. Plant Cell 12 (2000) 1031-1040
30. Pechan T., Cohen A., Williams W.P., and Luthe D.S. Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proc. Natl. Acad. Sci. USA 99 (2002) 13319-13323
31. Peters W. Peritrophic Membranes (1992), Springer, New York
32. Reeck G.R., Kramer K.J., Baker J.E., Kanost M.R., Fabrick J.A., and Behnke C.A. Proteinase inhibitors and resistance of transgenic plants to insects. In: Carozzi N., and Koziel M. (Eds). Advances in Insect Control: the Role of Transgenic Plants (1997), Taylor & Francis, London 157-183
33. Rosenthal G.A., and Berenbaum M.R. Herbivores: Their Interactions with Secondary Plant Metabolites (1991), Academic Press, San Diego, London
34. Ryan C.A. Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Ann. Rev. Phytopathol 28 (1990) 425-449
35. Ryan C.A. The systemin signaling pathway: differential activation of plant defensive genes. Biochim. Biophys. Acta 1477 (2000) 112-121
36. Sadaf Z., Shahid P.B., and Bilqees B. Isolation, characterization and kinetics of goat cystatins. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 142 (2005) 361-368
37. Schoonhoven L.M., van Loon J.J.A., and Dicke M. Insect-Plant Biology (2005), Oxford University Press, Oxford
38. Shindo T., and van der Hoorn R.A.L. Papain-like cysteine proteases: key players at molecular battlefields employed by both plants and their invaders. Mol. Plant Pathol. 9 (2008) 119-125
39. Summers C.B., and Felton G.W. Peritrophic envelope as a functional antioxidant. Arch. Insect Biochem. Physiol. 32 (1996) 131-142
40. Sutherland, D.W., Greene, G.L., 1984. Cultivated and wild host plants. In: USDA-ARS Technical Bulletin No. 1684, Suppression and Management of Cabbage Looper Populations. U.S. Dept. Agric., Washington, DC, pp. 1-13.
41. Terra W.R. The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch. Insect Biochem. Physiol. 47 (2001) 47-61
42. Wang P., Hammer D.A., and Granados R.R. Interaction of Trichoplusia ni granulosis virus-encoded enhancin with the midgut epithelium and peritrophic membrane of four lepidopteran insects. J. Gen. Virol. 75 (1994) 1961-1967
43. Wang P., Li G., and Granados R.R. Identification of two new peritrophic membrane proteins from larval Trichoplusia ni: structural characteristics and their functions in the protease rich insect gut. Insect Biochem. Mol. Biol. 34 (2004) 215-227
44. Wang P., and Granados R.R. An intestinal mucin is the target substrate for a baculovirus enhancin. Proc. Natl. Acad. Sci. USA 94 (1997) 6977-6982
45. Wang P., and Granados R.R. Molecular cloning and sequencing of a novel invertebrate intestinal mucin cDNA. J. Biol. Chem. 272 (1997) 16663-16669
46. Wang P., and Granados R.R. Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch. Insect Biochem. Physiol. 47 (2001) 110-118
47. Wittstock U., and Gershenzon J. Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr. Plant Biol. 5 (2002) 300-307
48. Zhu-Salzman K., Koiwa H., Salzman R.A., Shade R.E., and Ahn J.-E. Cowpea bruchid Callosobruchus maculates uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Mol. Biol. 12 (2003) 135-145
49. Zhu-Salzman K., Bi J.L., and Liu T.-X. Molecular strategies of plant defense and insect counter-defense. Insect Sci. 12 (2005) 3-15
50. Zhu-Salzman K., Luthe D.S., and Felton G.W. Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol. 146 (2008) 852-858