Skip to main content
Download PDF
  • Published:

Structural and functional diversities in lepidopteran serine proteases

Cellular & Molecular Biology Letters volume 11, pages 132–154 (2006)Cite this article

Abstract

Primary protein-digestion in Lepidopteran larvae relies on serine proteases like trypsin and chymotrypsin. Efforts toward the classification and characterization of digestive proteases have unraveled a considerable diversity in the specificity and mechanistic classes of gut proteases. Though the evolutionary significance of mutations that lead to structural diversity in serine proteases has been well characterized, detailing the resultant functional diversity has continually posed a challenge to researchers. Functional diversity can be correlated to the adaptation of insects to various host-plants as well as to exposure of insects to naturally occurring antagonistic biomolecules such as plant-derived protease inhibitors (PIs) and lectins. Current research is focused on deciphering the changes in protease specificities and activities arising from altered amino acids at the active site, specificity-determining pockets and other regions, which influence activity. Some insight has been gained through in silico modeling and simulation experiments, aided by the limited availability of characterized proteases. We examine the structurally and functionally diverse Lepidopteran serine proteases, and assess their influence on larval digestive processes and on overall insect physiology.

Abbreviations

AI:

amylase inhibitor

Bt:

Bacillus thuringiensis

HGPs:

Helicoverpa armigera gut proteases

PI:

protease inhibitor

References

  1. Bown, D.P., Wilkinson, H.S. and Gatehouse, J.A. Differentially regulated inhibitor sensitive and insensitive protease genes from the phytophagous pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem. Mol. Biol. 27 (1997) 625–638.

    Article  PubMed  CAS  Google Scholar 

  2. Gatehouse, L.N., Shannon, A.L., Burgess, E.P.J. and Christeller, J.T. Characterization of major midgut proteinase cDNAs from Helicoverpa armigera larvae and changes in gene expression in response to four proteinase inhibitors in the diet. Insect Biochem. Mol. Biol. 27 (1997) 929–944.

    Article  PubMed  CAS  Google Scholar 

  3. Patankar, A.G., Giri, A.P., Harsulkar, A.M., Sainani, M.N., Deshpande, V.V., Ranjekar, P.K. and Gupta, V.S. Complexity in specificities and expression of Helicoverpa armigera gut proteinases explains polyphagous nature of the insect pest. Insect Biochem. Mol. Biol. 31 (2001) 453–464.

    Article  PubMed  CAS  Google Scholar 

  4. Browne, L.B. and Raubenheimer, D. Ontogenic changes in the rate of ingestion and estimates of food consumption in fourth and fifth instar Helicoverpa armigera caterpillars. J. Insect Physiol. 49 (2003) 63–71.

    Article  Google Scholar 

  5. Chougule, N.P., Giri, A.P., Sainani, M.N. and Gupta, V.S. Gene expression patterns of Helicoverpa armigera gut proteases. Insect Biochem. Mol. Biol. 35 (2005) 355–367.

    Article  PubMed  CAS  Google Scholar 

  6. Bown, D.P., Wilkinson, H.S. and Gatehouse, J.A. Regulation of expression of genes encoding digestive proteases in the gut of a polyphagous lepidopteran larva in response to dietary protease inhibitors. Physiol. Entomol. 29 (2004), 278–290.

    Article  CAS  Google Scholar 

  7. Huang, Y., Brown, M.R., Lee, T.D. and Crim, J.W. RF-amides isolated from the midgut of the corn earworm Helicoverpa zea, resemble pancreatic polypeptide. Insect Biochem. Mol. Biol. 28 (1998) 345–356.

    Article  PubMed  CAS  Google Scholar 

  8. Harshini, S., Nachman, R.J. and Sreekumar, S. In vitro release of digestive enzymes by FMRF amide related neuropeptides and analogues in the lepidopteran insect Opisina arenosella (Walk.) Peptides 23 (2002) 1759–1763.

    Article  PubMed  CAS  Google Scholar 

  9. Harshini, S., Nachman, R.J. and Sreekumar, S. Inhibition of digestive enzyme release by neuropeptides in larvae of Opisina arenosella (Lepidoptera: Cryptophasidae). Comp. Biochem. Physiol. — Part B 132 (2002) 353–358.

    CAS  Google Scholar 

  10. Lopes, A.R., Juliano, M.A., Juliano, L. and Terra, W.R. Coevolution of insect trypsins and inhibitors. Arch. Insect Biochem. Physiol. 55 (2004) 140–152.

    Article  PubMed  CAS  Google Scholar 

  11. Barrett, A.J. and Rawlings, N.D. Families and clans in serine peptidases. Arch. Biochem. Biophys. 318 (1995) 247–250.

    Article  PubMed  CAS  Google Scholar 

  12. Krem, M.M. and Cera E.D. Molecular markers of serine protease evolution. EMBO J. 20 (2001) 3036–3045.

    Article  PubMed  CAS  Google Scholar 

  13. 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.

    Article  PubMed  CAS  Google Scholar 

  14. Botos, I., Meyer, E., Nguyen, M., Swanson, S.M., Koomen, J.M., Russell, D.H. and Meyer, E.F., 2000. The structure of an insect chymotrypsin. J. Mol. Biol. 298 (2000) 895–901.

    Article  PubMed  CAS  Google Scholar 

  15. Iengar, P. and Ramakrishnan, C. Knowledge based modeling of the serine protease triad into non-proteases. Protein Eng. 12 (1999) 649–655.

    Article  PubMed  CAS  Google Scholar 

  16. Nishihira, J. and Tachikawa, H. Theoretical evaluation of a model of the catalytic triads of serine and cysteine proteases by an initio molecular orbital calculation. J. Theor. Biol. 196 (1999) 513–519.

    Article  PubMed  CAS  Google Scholar 

  17. Beveridge, A.J. A theoretical study of the initial stages of catalysis in the aspartic proteinases. J. Mol. Chem. (Theochem) 453 (1998) 275–291.

    Article  CAS  Google Scholar 

  18. Laskowski, M. Jr, and Qasim, M.A. What can the structures of enzyme-inhibitor complexes tell us about the structures of enzyme substrate complexes? Biochim. Biophys. Acta 1477 (2000) 324–337.

    PubMed  CAS  Google Scholar 

  19. Krowarsch, D., Zakrzewska, M., Smalas, O.A. and Otlewski, J. Structure-function relationships in serine protease-bovine pancreatic trypsin inhibitor interaction. Protein Pept. Lett. 12 (2005) 1–5.

    Article  Google Scholar 

  20. Kraut, J. Serine proteases: structure and mechanism of catalysis. Annu. Rev. Biochem. 46 (1977) 331–358.

    Article  PubMed  CAS  Google Scholar 

  21. Dodson, G. and Wlodawer, A. Catalytic triad and their relatives. Trends Biochem. Sci. 23 (1998) 347–352.

    Article  PubMed  CAS  Google Scholar 

  22. Polgar, L. The catalytic triad of serine peptidases. Cell. Mol. Life Sci. 62 (2005) 1–12.

    Article  CAS  Google Scholar 

  23. Hunkapiller, M.W., Smallcombe, S.H., Hitaker, D.R. and Richards, J.H. Ionization behaviour of the histidine residue in the catalytic triad of serine proteases. J. Biol. Chem. 248 (1973) 8306–8308.

    PubMed  CAS  Google Scholar 

  24. David, F., Bernard, A.M., Pierres, M. and Marguet, D. Identification of serine 624, aspartic acid 702 and histidine 734 as the catalytic triad residues of mouse dipeptidyl-peptidase IV (CD26): a member of the novel family of nonclassical serine hydrolases. J. Biol. Chem. 268 (1993) 17247–17252.

    PubMed  CAS  Google Scholar 

  25. Ishida, T. and Kato, S. Role of asp102 in the catalytic relay system of serine proteases: a theoretical study. J. Am. Chem. Soc. 126 (2004) 7111–7118.

    Article  PubMed  CAS  Google Scholar 

  26. Komiyama, T., VanderLugt, B., Fugere, M., Day, R., Kaufman, R.J. and Fuller, R.S. Optimization of protease-inhibitor interactions by randomizing adventitious contacts. Proc. Nat. Acad. Sci. USA 100 (2003) 8205–8210.

    Article  PubMed  CAS  Google Scholar 

  27. Marana, S.R., Lopes, A.R., Juliano, L., Juliano, M.A., Ferreira, C. and Terra, W.R. Subsites of trypsin active site favor catalysis or substrate binding. Biochem. Biophys. Res. Comm. 290 (2002) 494–497.

    Article  PubMed  CAS  Google Scholar 

  28. Fodor, K., Harmat, V., Hetenyi, C., Kardos, J., Antal, J., Perczel, A., Patthy, A., Katona, G. and Graf, L. Extended intermolecular interactions in a serine protease canonical inhibitor complex account for strong and highly specific inhibition. J. Mol. Biol. 350 (2005) 156–169.

    Article  PubMed  CAS  Google Scholar 

  29. Atassi, M.Z., Manshouri, T. Design of peptide enzymes (pepzymes): Surface-simulation synthetic peptides that mimic the chymotrypsin and trypsin active sites exhibit the activity and specificity of the respective enzyme. Proc. Natl. Acad. Sci. USA. 90 (1993) 8282–8286.

    Article  PubMed  Google Scholar 

  30. Kaiser, E.T., Lawrence, D.S. and Rokita, S.E. The chemical modification of enzyme specificity. Annu. Rev. Biochem. 54 (1985) 565–595.

    Article  PubMed  CAS  Google Scholar 

  31. El-Hawrani, A.S., Sessions, R.B., Moreton, K.M. and Holbrook, J.J. Guided evolution of enzymes with new substrate specificities. J. Mol. Biol. 264 (1996) 97–110.

    Article  PubMed  CAS  Google Scholar 

  32. Hung, S. and Hedstrom, L. Converting trypsin to elastase: substitution of the S1 site and adjacent loops reconstitutes esterase specificity but not amidase activity. Protein Eng. 11 (1998) 669–673.

    Article  PubMed  CAS  Google Scholar 

  33. Takagi, H. and Takahashi, M. A new approach for alteration of protease functions: pro-sequence engineering. Appl. Microbiol. Biotechnol. 63 (2003) 1–9.

    Article  PubMed  CAS  Google Scholar 

  34. Khamrui, S., Dasgupta, J., Dattagupta, J.K. and Sen, U. Single mutation at P1 of a chymotrypsin inhibitor changes it to a trypsin inhibitor: X-ray structural (2.15°A) and biochemical basis. Biochim. Biophys. Acta (2005) in press.

  35. Corey, D.R., Willett, W.S., Coombs, G.S. and Craik, C.S. Trypsin Specificity Increased through Substrate-Assisted Catalysis. Biochemistry 34 (1995) 11521–11527.

    Article  PubMed  CAS  Google Scholar 

  36. Higaki, J.N., Evnin, L.B. and Craik, C.S. Introduction of a Cysteine Protease Active Site into Trypsin. Biochemistry 28 (1989) 9256–9263.

    Article  PubMed  CAS  Google Scholar 

  37. Tanaka, T. and Yada, R.Y. Redesign of catalytic center of an enzyme: aspartic to serine proteinase. Biochem. Biophys. Res. Commun. 323 (2004) 947–953.

    Article  PubMed  CAS  Google Scholar 

  38. Telang, M.A., Giri, A.P., Sainani, M.N. and Gupta, V.S. Elastase-like proteinase of Helicoverpa armigera is responsible for inactivation of a proteinase inhibitor from chickpea. J. Insect Physiol. 51 (2005) 513–522.

    Article  PubMed  CAS  Google Scholar 

  39. Valaitis, A.P., Augustin, S. and Clancy, K.M. Purification and characterization of the western spruce budworm larval midgut proteinases and comparison of gut activities of laboratory-reared and field-collected insects. Insect Biochem. Mol. Biol. 29 (1999) 405–415.

    Article  PubMed  CAS  Google Scholar 

  40. Bown, D.P., Wilkinson, H.S., Jongsma, M.A. and Gatehouse, J.A. Characterization of cysteine proteinases responsible for digestive proteolysis in guts of larval western corn rootworm (Diabroticca virgifera) by expression in the yeast Pichia pastoris. Insect Biochem. Mol. Biol. 34 (2004) 305–320.

    Article  PubMed  CAS  Google Scholar 

  41. Bown, D.P., Wilkinson, H.S. and Gatehouse, J.A. Midgut carboxypeptidase from Helicoverpa armigera (Lepidoptera: Noctuidae) larvae: enzyme characterisation, cDNA cloning and expression. Insect Biochem. Mol. Biol. 28 (1998) 739–749.

    Article  PubMed  CAS  Google Scholar 

  42. Bayes, A., Sonnenschein, A., Daura, X., Vendrell, J. and Aviles, F.X. Procarboxypeptidase A from the insect pest Helicoverpa armigera and its derived enzyme. Eur. J. Biochem. 270 (2003) 3026–3035.

    Article  PubMed  CAS  Google Scholar 

  43. Estebanez-Perpina, E., Bayes, A., Vendrell, J., Jongsma, M.A., Bown, D.P., Gatehouse, J.A., Huber, R., Bode, W., Aviles, F.X. and Reverter, D. Crystal structure of a novel mid-gut procarboxypeptidase from the cotton pest Helicoverpa armigera. J. Mol. Biol. 313 (2001) 629–638.

    Article  PubMed  CAS  Google Scholar 

  44. Herrero, S., Combes, E., Van Oers, M.M., Vlak, J.M., de Maagd, R.A. and Beekwilder, J. Identification and recombinant expression of a novel chymotrypsin from Spodoptera exigua. Insect Biochem. Mol. Biol. 35 (2005) 1073–1082.

    Article  PubMed  CAS  Google Scholar 

  45. Li, J., Choo, Y.M., Lee, K.S., Je, Y.H., Woo, S.D., Kim, I., Sohn, H.D. and Jin, B.R. A serine protease gene from the firefly, Pyrocoelia rufa: gene structure, expression, and enzyme activity. Biotechnol. Lett. 27 (2005) 1051–1057.

    Article  PubMed  CAS  Google Scholar 

  46. Garcia-Olmedo, F., Salcedo, G., Sanchez-Monge, R., Gomez, L., Roys, J. and Carbonero, P. Plant proteinaceous inhibitors of proteases and amylases. Oxford Survey Plant Mol. Cell. Biol. 4 (1987) 275–334.

    CAS  Google Scholar 

  47. Ryan, C.A. Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28 (1990) 425–449.

    Article  CAS  Google Scholar 

  48. Boulter, D. Insect pest control by copying nature using genetically engineered crops. Phytochemistry 34 (1993) 1453–1466.

    Article  PubMed  CAS  Google Scholar 

  49. Carlini, C.R. and Grossi-de-Sa, M.F. Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon 40 (2002) 1515–1539.

    Article  PubMed  CAS  Google Scholar 

  50. Murdock, L.L. and Shade, R.E. Lectins and protease inhibitors as plant defenses against insects. J. Agric. Food Chem. 50 (2002) 6605–6611.

    Article  PubMed  CAS  Google Scholar 

  51. Ferry, N., Edwards, M.G., Gatehouse, J.A. and Gatehouse, A.M.R. Plant-insect interactions: molecular approaches to insect resistance. Curr. Opin. Biotechnol. 15 (2004) 155–161.

    Article  PubMed  CAS  Google Scholar 

  52. Giri, A.P., Chougule, N.P., Telang M.A. and Gupta, V.S. Engineering insect tolerant plants using plant defensive proteinase inhibitors. in: Recent Research Developments in Phytochemistry, (Pandalai, S.G. Ed) Research Signpost, India, vol. 8, 2005, 117–137.

    Google Scholar 

  53. Laskowski, M. Jr. Protein inhibitors of serine proteinases — mechanism and function. Adv. Exp. Med. Biol. 199 (1986) 1–17.

    PubMed  CAS  Google Scholar 

  54. Huntington, J.A., Read, R.J. and Carrell, R.W. Structure of a serpin-protease complex shows inhibition by deformation. Nature 407 (2000) 923–926.

    Article  PubMed  CAS  Google Scholar 

  55. Hedstrom, L. Serine protease mechanism and specificity. Chem. Rev. 102 (2000) 4501–4523.

    Article  CAS  Google Scholar 

  56. Plotnick, M.I., Mayne, L., Schechter, N.M. and Harvey, R. Distortion of the Active Site of Chymotrypsin Complexed with a Serpin. Biochemistry 35 (1996) 7586–7590.

    Article  PubMed  CAS  Google Scholar 

  57. Broadway, R.M. and Duffey, S.S. Plant proteinase inhibitors: mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J. Insect Physiol. 32 (1986) 827–833.

    Article  CAS  Google Scholar 

  58. Hilder, V.A., Gatehouse, A.M.R., Sherman, S.F., Barker, R.F. and Boulter, D. A novel mechanism of insect resistance engineered into tobacco. Nature 330 (1987) 160–163.

    Article  CAS  Google Scholar 

  59. Broadway, R.M. Plant dietary proteinase inhibitors alter complement of midgut proteases. Arch. Insect Biochem. Physiol. 32 (1996) 39–53.

    Article  CAS  Google Scholar 

  60. Srinivasan, A., Giri, A.P., Harsulkar, A.M., Gatehouse, J.A. and Gupta, V.S. A Kunitz trypsin inhibitor from chickpea (Cicer arietinum L.) that exerts anti-metabolic effect on podborer (Helicoverpa armigera) larvae. Plant Mol. Biol. 57 (2005) 359–374.

    Article  PubMed  CAS  Google Scholar 

  61. Jouanin, L., Bonade-Bottino, M., Girard, C., Morrot, G and Giband, M. Transgenic plants for insect resistance. Plant Sci. 131 (1998) 1–11.

    Article  CAS  Google Scholar 

  62. Harsulkar, A.M., Giri, A.P., Patankar, A.G., Gupta, V.S., Sainani, M.N., Ranjekar, P.K. and Deshpande, V.V. Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth. Plant Physiol. 121 (1999) 497–506.

    Article  PubMed  CAS  Google Scholar 

  63. deLeo, F. and Gallerani, R. The mustard trypsin inhibitor 2 affects the fertility of Spodoptera littoralis larvae fed on transgenic plants. Insect Biochem. Mol. Biol. 32 (2002) 489–496.

    Article  CAS  Google Scholar 

  64. Telang, M.A., Srinivasan, A., Patankar, A.G., Harsulkar, A.M., Joshi, V.V., Damle, A., Deshpande, V.V., Sainani, M.N., Ranjekar, P.K., Gupta, G.P., Birah, A., Rani, S., Kachole, M., Giri, A.P and Gupta, V.S. Bitter gourd proteinase inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochemistry 63 (2003) 643–652.

    Article  PubMed  CAS  Google Scholar 

  65. Tamhane, V.A., Chougule, N.P., Giri, A.P., Dixit, A.R., Sainani, M.N. and Gupta, V.S. In vitro and in vivo effects of Capsicum annum proteinase inhibitors on Helicoverpa armigera gut proteinases. Biochim. Biophys. Acta 1722 (2005) 155–167.

    Google Scholar 

  66. Giri, A.P., Harsulkar, A.M., Deshpande, V.V., Sainani, M.N., Gupta, V.S. and Ranjekar, P.K. Chickpea defensive proteinase inhibitors can be inactivated by podborer gut proteinases. Plant Physiol. 116 (1998) 393–401.

    Article  CAS  Google Scholar 

  67. Giri, A.P., Harsulkar, A.M., Ku, M.S.B., Gupta, V.S., Deshpande, V.V., Ranjekar, P.K. and Franceschi, V.R. Identification of potent inhibitors of Helicoverpa armigera gut proteinases from winged bean seeds. Phytochemistry 63 (2003) 523–532.

    Article  PubMed  CAS  Google Scholar 

  68. Ishimoto, M. and Chrispeels, M.J. Protective mechanism of the Mexican bean weevil against high levels of α-amylase inhibitor in the common bean. Plant Physiol. 111 (1996) 393–401.

    Article  PubMed  CAS  Google Scholar 

  69. Oppert, B., Kramer, K.J., Johnson, D., Upton, S.J. and McGaughey, W.H. Luminal proteinases from Plodia interpunctella and the hydrolysis of Bacillus thuringiensis Cry1A(c) protoxin. Insect Biochem. Mol. Biol. 26 (1996) 571–583.

    Article  PubMed  CAS  Google Scholar 

  70. Zhu, Y., Oppert, B., Kramer, K.J., McGaughey, W.H. and Dowdy, A.K. cDNAs for a chymotrypsinogen-like protein from two strains of Plodia interpunctella. Insect Biochem. Mol. Biol. 27 (1997) 1027–1037.

    Article  PubMed  CAS  Google Scholar 

  71. Zhu, Y., Kramer, K.J., Oppert, B. and Dowdy, A.K. cDNAs of aminopeptidase-like protein genes from Plodia interpunctella strains with different susceptibilities to Bacillus thuringiensis toxins. Insect Biochem. Mol. Biol. 30 (2000) 215–224.

    Article  PubMed  CAS  Google Scholar 

  72. Zhu, Y., Kramer, K.J., Dowdy, A.K. and Baker, J.E. Trypsinogen-like cDNAs and quantitative analysis of mRNA levels from the indianmeal moth, Plodia interpunctella. Insect Biochem. Mol. Biol. 30 (2000) 1027–1035.

    Article  PubMed  CAS  Google Scholar 

  73. Zhu, Y., Oppert, B., Kramer, K.J., McGaughey, W.H. and Dowdy, A.K. cDNA sequence, mRNA expression and genomic DNA of trypsinogen from the indianmeal moth Plodia interpunctella. Insect Mol. Biol. 9 (2000) 19–26.

    Article  PubMed  CAS  Google Scholar 

  74. Jongsma, M.A. and Bolter, C. The adaptation of insects to plant protease inhibitors. J. Insect Physiol. 43 (1997) 885–895.

    Article  PubMed  CAS  Google Scholar 

  75. Paulillo, L.C.M.S., Lopes, A.R., Cristofoletti, P.T., Parra, J.R.P., Terra, W.R. and Silva-Filho, M.C. Changes in midgut endopeptidase activity of Spodoptera frugiperda (Lepidoptera: Noctuidae) are responsible for adaptation to soybean proteinase inhibitors. J. Econ. Entomol. 93 (2000) 892–896.

    Article  PubMed  CAS  Google Scholar 

  76. Brito, L.O., Lopes, A.R., Parra, J.R.P., Terra, W.R. and Silva-Filho, M.C. Adaptation of tobacco budworm Heliothis virescens to proteinase inhibitors may be mediated by the synthesis of new proteinases. Comp. Biochem. Physiol. 128 (2001) 365–375.

    Article  CAS  Google Scholar 

  77. Broadway, R.M. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J. Insect Physiol. 43 (1997) 855–874.

    Article  PubMed  CAS  Google Scholar 

  78. Girard, C., Metayer, M.L., Zaccomer, B., Bartlet, E., Williams, I., Bonade-Bottino, M., Pham-Delegue, M. and Jouanin, L. Growth simulation of beetle larvae reared on a transgenic oilseed rape expressing a cysteine proteinase inhibitor. J. Insect Physiol. 44 (1998) 263–270.

    Article  PubMed  CAS  Google Scholar 

  79. 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. Nat. Acad. Sci. USA 92 (1995) 8041–8045.

    Article  PubMed  CAS  Google Scholar 

  80. Mazumdar-Leighton, S. and Broadway, R.M. Identification of six chymotrypsin cDNAs from larval midguts of Helicoverpa zea and Agrotis ipsilon feeding on the soybean (Kunitz) trypsin inhibitor. Insect Biochem. Mol. Biol. 31 (2001) 633–644.

    Article  PubMed  CAS  Google Scholar 

  81. 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.

    Article  PubMed  CAS  Google Scholar 

  82. Volpicella, M., Ceci, L.R., Cordewener, J., America, T., Gallerani, R., Bode, W., Jongsma, M.A. and Beekwilder, J. Properties of purified gut trypsin from Helicoverpa zea adapted to proteinase inhibitors. Eur. J. Biochem. 270 (2003) 10–19.

    Article  PubMed  CAS  Google Scholar 

  83. Girard, C., Metayer, M.L., Bonade-Bottino, M., Pham-Delegue, M. and Jouanin, L. High level of resistance to proteinase inhibitors may be conferred by proteolytic cleavage in beetle larvae. Insect Biochem. Mol. Biol. 28 (1998) 229–137.

    Article  PubMed  CAS  Google Scholar 

  84. Zhu-Salzman, K., Koiwa, H., Salzman, R.A., Shade, R.E. and Ahn, J.E. Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Biochem. Mol. Biol. 12 (2003) 135–145.

    Article  CAS  Google Scholar 

  85. Moon, J., Salzman, R.A., Ahn, J.E., Koiwa, H. and Zhu-Salzman, K. Transcriptional regulation in cowpea bruchid guts during adaptation to a plant defence protease inhibitor. Insect Biochem. Mol. Biol. 13 (2004) 283–291.

    Article  CAS  Google Scholar 

  86. Srinivasan, A., Chougule, N.P., Giri, A.P., Gatehouse, J.A. and Gupta, V.S. Podborer (Helicoverpa armigera Hübn.) does not show specific adaptations in gut proteinases to dietary Cicer arietinum Kunitz proteinase inhibitor. J. Insect Physiol. 51 (2005) 1268–1276.

    Article  PubMed  CAS  Google Scholar 

  87. Ehrlich, P.R. and Raven P.H. Butterflies and plants: a study in coevolution. Evolution 18 (1964) 586–608.

    Article  Google Scholar 

  88. Johnson, R., Narvaez, J., An, G. and Ryan, C.A. Expression of proteinase inhibitors I and II in transgenic tobacco plants: Effects on natural defense against Manduca sexta larvae. Proc. Natl. Acad. Sci. USA 86 (1989) 9871–9875.

    Article  PubMed  CAS  Google Scholar 

  89. Lara, P., Ortego, F., Gonzalez-Hidalgo, E., Castanera, P., Carbonero, P. and Diaz, I. Adaptation of Spodoptera exigua (Lepidoptera: Noctuidae) to barley trypsin inhibitor BTI-CMe expressed in transgenic tobacco. Transgenic Res. 9 (2000) 169–178.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant Molecular Biology Group, Division of Biochemical Sciences, National Chemical Laboratory, Pune, 411008, India

    Ajay Srinivasan, Ashok P. Giri & Vidya S. Gupta

Authors
  1. Ajay Srinivasan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ashok P. Giri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vidya S. Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vidya S. Gupta.

Additional information

Invited paper

Rights and permissions

Reprints and permissions

About this article

Cite this article

Srinivasan, A., Giri, A.P. & Gupta, V.S. Structural and functional diversities in lepidopteran serine proteases. Cell. Mol. Biol. Lett. 11, 132–154 (2006). https://doi.org/10.2478/s11658-006-0012-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11658-006-0012-8

Key words

Cellular & Molecular Biology Letters

ISSN: 1689-1392

Contact us