Evaluation of the inhibitory potential of pro-peptide region as the inhibitor of the digestive chymotrypsin of cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae), based on in silico studies

Document Type : Paper, Persian

Authors

Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran

Abstract

The cotton bollworm, Helicoverpa armigera (Hübner),is a wide host range pest that causes severe economic damages to agricultural crops in Iran and all around the world. During recent years, chemical insecticides have been used as the most effective strategy in control of this pest, but due to their hazardous effects, most of the researches are being conducted to offer an alternative approach for chemical control. In this regard, digestive systems, in particular inhibition of insect digestive enzymes, are considered as a target for pest control. Here, we used the original pro-region of H. armigera chymotrypsin as a potent and specific inhibitor of the pest enzyme. The structural model of the insect chymotrypsin was predicted based on homology modeling and the crystal structure of Bos taurus L. as template. The reliability of the model was assessed using VERIFY_3D, ERRAT, PROCHECK, WHAT-IF and Z-scores, and the results confirmed that the predicted structural model has an appropriate quality. Moreover, molecular docking simulations between the predicted structural model of enzyme and designed peptide showed that the inhibitor peptide has the most appropriate docking score and total binding energy for interactions with the insect chymotrypsin’s active site. However, it showed a weak potential for interaction with Sus scrofa L. chymotrypsin, as a representative of the mammalian enzyme. The results of this report indicate the importance of computational studies in design and selection of the favored inhibitor pro-peptides against the target enzymes. Such inhibitors can be further suggested as a replacement of chemical pesticides for controlling of H. armigera as well as the other pests in future.

Keywords


Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic acids research 25, 3389–3402
Applebaum, S. W. (1985) Biochemistry of digestion. Comprehensive insect physiology, biochemistry and pharmacology 4, 279–311
Colovos, C. & Yeates, T. O. (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Science 2, 1511–1519
De Beer, T. A. P., Berka, K., Thornton, J. M. & Laskowski, R. A. (2014) PDBsum additions. Nucleic acids research 42, 292–296
De Vries, S. J., van Dijk, M. & Bonvin, A. M. J. J. (2010) The HADDOCK web server for data-driven biomolecular docking. Nature protocols 5,883–897
Dominguez, C., Boelens, R. & Bonvin, A. M. J. J. (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. Journal of the American Chemical Society 125, 1731–1737
Eisenberg, D., Lüthy, R. & Bowie, J. U. (1997) [20] VERIFY3D: assessment of protein models with three-dimensional profiles. pp. 396–404 in Charles, W., Carter, Jr. & Robert, M. Sweet (Eds) Methods in Enzymology. 696 pp. Academic Press.
Fitt, G. P. (1989) The ecology of Heliothis species in relation to agroecosystems. Annual Review of Entomology 34, 17–52
Franco, O. L., Rigden, D. J., Melo, F. R. & GrossideSá, M. F. (2002) Plant α‐amylase inhibitors and their interaction with insect α‐amylases. European Journal of Biochemistry 269, 397–412
Gouet, P., Courcelle, E., Stuart, D. & Metoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305–308
Groves, M. R., Taylor, M. A. J., Scott, M., Cummings, N. J., Pickersgill, R. W. & Jenkins, J. A. (1996) The prosequence of procaricain forms an α-helical domain that prevents access to the substrate-binding cleft. Structure 4, 1193–1203
Hemati, S. A., Naseri, B., Ganbalani, G. N., Dastjerdi, H. R. & Golizadeh, A. (2012) Digestive proteolytic and amylolytic activities and feeding responses of Helicoverpa armigera (Noctuidae: Lepidoptera) on different host plants. Journal of Economic Entomology 105, 1439–1446
Hemmati, S. A., Sajedi, R. H., Moharramipour, S., Taghdir, M., Rahmani, H., Etezad, S. M. & Mehrabadi, M. (2017a) Biochemical characterization and structural analysis of trypsin from Plodia interpunctella midgut: implication of determinants in extremely alkaline pH activity profile. Physiological Entomology 42, 307–318
Hemmati, S. A., Sajedi, R. H., Moharramipour, S., Taghdir, M., Rahmani, H., Etezad, S. M. & Mehrabadi, M. (2017b) Directed design of peptide inhibitor based on zymogen structure of trypsin to assess of inhibitory and insecticidal effects on Plodia interpunctella.2nd International Iranian Peptide Conference & Humboldt-Kolleg, Tehran, Iran. p. 72
Houseman, J. G., Philogene, B. J. R. & Downe, A. E. R. (1989) Partial characterization of proteinase activity in the larval midgut of the European corn borer, Ostrinia nubilalis Hübner (Lepidoptera: Pyralidae). Canadian Journal of Zoology 67, 864–868
Ingale, A. G. & Chikhale, N. J. (2010) Prediction of 3D Structure of Paralytic Insecticidal Toxin (ITX-1) of Tegenaria agrestis (Hobo Spider). Journal Data Mining Genomics Proteomics 1, 102–104
Isman, M. B. (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology 51, 45–66
Jitonnom, J., Lomthaisong, K. & Lee, V. S. (2012) Computational design of peptide inhibitor based on modifications of proregion from Plutella xylostella midgut trypsin. Chemical biology & drug design 79, 583–593
Kalman, T. I. (1981) Enzyme inhibition as a source of new drugs. Drug Development Research 4, 311–328
Karahroodi, Z. R., Moharramipour, S. & Rahbarpour, A. (2009) Investigated repellency effect of some essential oils of 17 native medicinal plants on adults Plodia interpunctella. American-Eurasian journal of sustainable agriculture 3, 181–184
Karthik, M. & Shukla, P. (2012) Computational strategies towards improved protein function prophecy of Xylanases from Thermomyces lanuginosus. 1st ed. 44 pp. Springer Science & Business.
Kunitz, M. J. & Northrop, J. H. (1936) Isolation from beef pancreas of crystalline trypsinogen, trypsin, a trypsin inhibitor, and an inhibitor-trypsin compound. The Journal of general physiology 19, 991–1007
Kunitz, M. (1945) Crystallization of a trypsin inhibitor from soybean. Science 101, 668–669
Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography 26, 283–291
Lazure, C. (2002) The peptidase zymogen proregions: nature’s way of preventing undesired activation and proteolysis. Current pharmaceutical design 8, 511–531
Leuck, D. B. & Perkins, W. D. (1972) A method of estimating fall armyworm progeny reduction when evaluating control achieved by host-plant resistance. Journal of Economic Entomology 65, 482–483
Mehrabadi, M., Bandani, A. R., Saadati, F. & Ravan, S. (2009) Sunn pest, Eurygaster integriceps Putton (Hemiptera: Scutelleridae), digestive α-amylase, α-glucosidase and β-glucosidase. Journal of Asia-Pacific Entomology 12, 79–83
Mehrabadi, M., Bandani, A. R. & Franco, O. L. (2012) Plant proteinaceous alpha-amylase and proteinase inhibitors and their use in insect pest control. pp. 229-246 in Bandani, A. R.(Ed.) New Perspectives in Plant Protection. 246 pp.InTech.
Perona, J. J. & Craik, C. S. (1997) Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. Journal of Biological Chemistry 272, 29987–29990
Phillips, T. W., Berberet, R. C. & Cuperus, G. W. (2000) Post-harvest integrated pest management. pp. 2690–2701 in Francis, F. J. (Ed.) Encyclopedia of food science and technology. 3130 pp. Wiley.
Platzer, K. E., Momany, F. A. & Scheraga, H. A. (1972) Conformational energy calculations of enzyme‐substrate interactions. II. Computation of the binding energy for substrates in the active site of α‐chymotrypsin. International journal of peptide and protein research 4, 201–219
Prasad, E. R., Dutta- Gupta, A. & Padmasree, K. (2010) Insecticidal potential of Bowman–Birk proteinase inhibitors from red gram (Cajanus cajan) and black gram (Vigna mungo) against lepidopteran insect pests. Pesticide Biochemistry and Physiology 98, 80–88
Rafiee- Dastjerdi, H., Hejazi, M. J., Nouri- Ganbalani, G. & Saber, M. (2008) Toxicity of some biorational and conventional insecticides to cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae) and its ectoparasitoid, Habrobracon hebetor (Hymenoptera: Braconidae). Journal of Entomological Society of Iran 28, 27–37
Rodriguez, R., Chinea, G., Lopez, N., Pons, T. & Vriend, G. (1998) Homology modeling, model and software evaluation: three related resources. Bioinformatics 14, 523–528
Roy, A., Kucukural, A. & Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols 5, 725–738
Ryan, C. A. (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annual review of phytopathology 28, 425–449
Shukle, R. H. & Murdock, L. L. (1983) Lipoxygenase trypsin inhibitor, and lectin from soybeans: effects on larval growth of Manduca sexta (Lepidoptera: Sphingidae). Environmental Entomology 12, 787–791
Silva, F. B., Monteiro, A. C. S., Del Sarto, R. P., Marra, B. M., Dias, S. C., Figueira, E. L. Z., Oliveira, G. R., Rocha, T. L., Souza, D. S. L., da Silva, M. C. M. & Franco, O. L. (2007) Proregion of Acanthoscelides obtectus cysteine proteinase: A novel peptide with enhanced selectivity toward endogenous enzymes. Peptides 28, 1292–1298
Sudbrink, J. D. L. & Grant, J. F. (1995) Wild host plants of Helicoverpa armigera and Helicoverpa zea (Lepidoptera: Noctuidae) in eastern Tennessee. Environmental Entomology 24, 1080–1085
Talekar, N. S., Opena, R. T. & Hanson, P. (2006) Helicoverpa armigera management: A review of AVRDC’s research on host plant resistance in tomato. Crop Protection 25, 461–467
Taylor, M. A. J. & Lee, M. J. (1997) Trypsin isolated from the midgut of the Tobacco hornworm, Manduca sexta, is inhibited by synthetic pro-peptides in vitro. Biochemical and Biophysical Research Communications 235, 606–609
Terra, W. R. & Ferreira, C. (1994) Insect digestive enzymes: properties, compartmentalization and function. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 109, 1–62
Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680
Visal, S., Taylor, M. A. J. & Michaud, D. (1998) The proregion of papaya proteinase IV inhibits Colorado potato beetle digestive cysteine proteinases. FEBS Lett 434, 401–405
Walsh, K. A. & Wilcox, P. E. (1970) Serine proteases. Methods in Enzymology 19, 31–41
Yildirim, A., Mavi, A. & Kara, A. A. (2001) Determination of antioxidant and antimicrobial activities of Rumex crispus L. extracts. Journal of agricultural and food chemistry 49, 4083–4089
Zhang, L. & Skolnick, J. (1998) What should the Z-score of native protein structures be?. Protein Science 7, 1201–1207.