NMR structure and dynamics of inhibitory repeat domain variant 12, a plant protease inhibitor from Capsicum annuum, and its structural relationship to other plant protease inhibitors

References

• Aggarwal, N., Brar, D., & Basedow, T. (2006). Insecticide resistance management of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) and its effect on pests and yield of cotton in North India. Journal of Plant Diseases and Protection, 113(3), 120–127. doi:10.1007/BF03356168
   Web of Science ®Google Scholar
• Anangi, R., Rash, L. D., Mobli, M., & King, G. F. (2012). Functional expression in Escherichia coli of the disulfide-rich sea anemone peptide APETx2, a potent blocker of acid-sensing ion channel 3. Marine Drugs, 10(12), 1605–1618. doi:10.3390/md10071605
   PubMedGoogle Scholar
• Antcheva, N., Pintar, A., Patthy, A., Simoncsits, A., Barta, E., Tchorbanov, B., & Pongor, S. (2008). Proteins of circularly permuted sequence present within the same organism: The major serine proteinase inhibitor from Capsicum annuum seeds. Protein Science, 10(11), 2280–2290. doi:10.1110/ps.21701
   Google Scholar
• Arantes, P. R., Perez-Sanchez, H., & Verli, H. (2018). Antithrombin conformational modulation by D-myo-inositol 3,4,5,6-tetrakisphosphate (TMI), a novel scaffold for the development of antithrombotic agents. Journal of Biomolecular Structure and Dynamics, 36(15), 4045–4056. doi:10.1080/07391102.2017.1407259
   PubMed Web of Science ®Google Scholar
• Atkinson, A. H., Heath, R. L., Simpson, R. J., Clarke, A. E., & Anderson, M. A. (1993). Proteinase inhibitors in Nicotiana alata stigmas are derived from a precursor protein which is processed into five homologous inhibitors. The Plant Cell Online, 5(2), 203–213. doi:10.1105/tpc.5.2.203
   PubMed Web of Science ®Google Scholar
• Atreya, H., Chary, K., & Govil, G. (2002). Automated NMR assignments of proteins for high throughput structure determination: TATAPRO II. Current Science, 83(11), 1372–1376. Available from https://www.currentscience.ac.in/Downloads/article_id_083_11_1372_1376_0.pdf
   Web of Science ®Google Scholar
• Barnwal, R. P., Agarwal, G., & Chary, K. V. (2012). Guanidine-HCl dependent structural unfolding of M-crystallin: Fluctuating native state like topologies and intermolecular association. PLoS One, 7(12), e42948. doi:10.1371/journal.pone.0042948
   PubMed Web of Science ®Google Scholar
• Barnwal, R. P., Devi, K. M., Agarwal, G., Sharma, Y., & Chary, K. V. (2011). Temperature-dependent oligomerization in M-crystallin: Lead or lag toward cataract, an NMR perspective. Proteins, 79(2), 569–580. doi:10.1002/prot.22905
   PubMed Web of Science ®Google Scholar
• Barnwal, R. P., Jobby, M. K., Devi, K. M., Sharma, Y., & Chary, K. V. (2009). Solution structure and calcium-binding properties of M-crystallin, a primordial betagamma-crystallin from archaea. Journal of Molecular Biology, 386(3), 675–689. doi:10.1016/j.jmb.2008.12.058
   PubMed Web of Science ®Google Scholar
• Barnwal, R. P., Rout, A. K., Chary, K. V., & Atreya, H. S. (2007). Rapid measurement of 3J(H N-H alpha) and 3J(N-H beta) coupling constants in polypeptides. Journal of Biomolecular NMR, 39(4), 259–263. doi:10.1007/s10858-007-9200-8
   PubMed Web of Science ®Google Scholar
• Barnwal, R. P., Rout, A. K., Chary, K. V. R., & Atreya, H. S. (2008). Rapid measurement of pseudocontact shifts in paramagnetic proteins by GFT NMR spectroscopy. The Open Magnetic Resonance Journal, 1, 13. doi:10.2174/1874769800801010016
   Google Scholar
• Bass, C., & Field, L. M. (2011). Gene amplification and insecticide resistance. Pest Management Science, 67(8), 886–890. doi:10.1002/ps.2189
   PubMed Web of Science ®Google Scholar
• Bevington, P. R., Robinson, D. K., Blair, J. M., Mallinckrodt, A. J., & McKay, S. (1993). Data reduction and error analysis for the physical sciences. Computers in Physics, 7(4), 415–416. doi:10.1063/1.4823194
   Google Scholar
• Bhattacharya, A., Tejero, R., & Montelione, G. T. (2006). Evaluating protein structures determined by structural genomics consortia. Proteins: Structure, Function, and Bioinformatics, 66(4), 778–795. doi:10.1002/prot.21165
   Web of Science ®Google Scholar
• Bloom, D. E. (2011). 7 billion and counting. Science (New York, N.Y.), 333(6042), 562–569. doi:10.1126/science.1209290
   PubMed Web of Science ®Google Scholar
• Bode, W., & Huber, R. (1992). Natural protein proteinase inhibitors and their interaction with proteinases. European Journal of Biochemistry, 204(2), 433–451. doi:10.1111/j.1432-1033.1992.tb16654.x
   PubMedGoogle Scholar
• Boulter, D. (1993). Insect pest control by copying nature using genetically engineered crops. Phytochemistry, 34(6), 1453–1466. doi:10.1016/S0031-9422(00)90828-8
   PubMed Web of Science ®Google Scholar
• Bown, D. P., Wilkinson, H. S., & Gatehouse, J. A. (1997). Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochemistry and Molecular Biology, 27(7), 625–638. doi:10.1016/S0965-1748(97)00043-X
   PubMed Web of Science ®Google Scholar
• Boyer, S., Zhang, H., & Lemperiere, G. (2012). A review of control methods and resistance mechanisms in stored-product insects. Bulletin of Entomological Research, 102(02), 213–229. doi:10.1017/S0007485311000654
   PubMedGoogle Scholar
• Cai, M., Gong, Y. X., Wen, L., & Krishnamoorthi, R. (2002). Correlation of binding-loop internal dynamics with stability and function in potato I inhibitor family: Relative contributions of Arg(50) and Arg(52) in Cucurbita maxima trypsin inhibitor-V as studied by site-directed mutagenesis and NMR spectroscopy. Biochemistry, 41(30), 9572–9579. doi:10.1021/bi0258952
   PubMed Web of Science ®Google Scholar
• Chary, K. V., & Govil, G. (2008). NMR in Biological Systems: From Molecules to Humans. Berlin, Germany: Springer. doi:10.1007/978-1-4020-6680-1, Retrieved from https://www.springer.com/in/book/9781402066795
   Google Scholar
• Chaturvedi, I. (2007). Status of insecticide resistance in the cotton bollworm, Helicoverpa armigera (Hubner). Journal of Central European Agriculture, 8, 171–182.
   Google Scholar
• Chougule, N. P., Giri, A. P., Sainani, M. N., & Gupta, V. S. (2005). Gene expression patterns of Helicoverpa armigera gut proteases. Insect Biochemistry and Molecular Biology, 35(4), 355–367. doi:10.1016/j.ibmb.2005.01.006
   PubMed Web of Science ®Google Scholar
• Christeller, J., & Laing, W. (2005). Plant serine proteinase inhibitors. Protein and Peptide Letters, 12(5), 439–447.
   PubMed Web of Science ®Google Scholar
• Cornilescu, G., Delaglio, F., & Bax, A. (1999). Protein backbone angle restraints from searching a database for chemical shift and sequence homology. Journal of Biomolecular NMR, 13(3), 289–302.
   PubMed Web of Science ®Google Scholar
• Crooks, G. E., Hon, G., Chandonia, J. M., & Brenner, S. E. (2004). WebLogo: A sequence logo generator. Genome Research, 14(6), 1188–1190. doi:10.1101/gr.849004
   PubMed Web of Science ®Google Scholar
• Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., & Bax, A. (1995). NMRPipe: A multidimensional spectral processing system based on UNIX pipes. Journal of Biomolecular NMR, 6, 277–293.
   PubMed Web of Science ®Google Scholar
• Gassmann, A. J., Petzold-Maxwell, J. L., Clifton, E. H., Dunbar, M. W., Hoffmann, A. M., Ingber, D. A., & Keweshan, R. S. (2014). Field-evolved resistance by western corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize. Proceedings of the National Academy of Sciences USA, 111(14), 5141–5146. doi:10.1073/pnas.1317179111
   PubMed Web of Science ®Google Scholar
• Giri, A. P., Harsulkar, A. M., Deshpande, V. V., Sainani, M. N., Gupta, V. S., & Ranjekar, P. K. (1998). Chickpea defensive proteinase inhibitors can be inactivated by podborer gut proteinases. Plant Physiology, 116(1), 393–401. doi:10.1104/pp.116.1.393
   Web of Science ®Google Scholar
• Green, T. R., & Ryan, C. A. (1972). Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects. Science, 175(4023), 776–777. doi:10.1126/science.175.4023.776
   PubMed Web of Science ®Google Scholar
• Güntert, P., Mumenthaler, C., & Wüthrich, K. (1997). Torsion angle dynamics for NMR structure calculation with the new program Dyana1. Journal of Molecular Biology, 273(1), 283–298. doi:10.1006/jmbi.1997.1284
   PubMed Web of Science ®Google Scholar
• Harsulkar, A. M., Giri, A. P., Patankar, A. G., Gupta, V. S., Sainani, M. N., Ranjekar, P. K., & Deshpande, V. V. (1999). Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth. Plant Physiology, 121(2), 497–506. doi:10.1104/pp.121.2.497
   PubMed Web of Science ®Google Scholar
• Imai, K., & Mitaku, S. (2005). Mechanisms of secondary structure breakers in soluble proteins. Biophysics, 1, 55–65.
   Google Scholar
• Jain, S., Amin, S. A., Adhikari, N., Jha, T., & Gayen, S. (2019). Good and bad molecular fingerprints for human rhinovirus 3C protease inhibition: Identification, validation, and application in designing of new inhibitors through Monte Carlo-based QSAR study. Journal of Biomolecular Structure and Dynamics, 1–12. doi:10.1080/07391102.2019.1566093
   PubMed Web of Science ®Google Scholar
• Jin, C., & Liao, X. (1999). Backbone dynamics of a winged helix protein and its DNA complex at different temperatures: Changes of internal motions in genesis upon binding to DNA. Journal of Molecular Biology, 292(3), 641–651. doi:10.1006/jmbi.1999.3106
   PubMed Web of Science ®Google Scholar
• Joshi, R. S., Gupta, V. S., & Giri, A. P. (2014). Differential antibiosis against Helicoverpa armigera exerted by distinct inhibitory repeat domains of Capsicum annuum proteinase inhibitors. Phytochemistry, 101, 16–22. doi:10.1016/j.phytochem.2014.01.011
   PubMed Web of Science ®Google Scholar
• Kay, L. E., Torchia, D. A., & Bax, A. (1989). Backbone dynamics of proteins as studied by nitrogen-15 inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry, 28(23), 8972–8979. doi:10.1021/bi00449a003
   PubMed Web of Science ®Google Scholar
• Keller, R., & Wuthrich, K. (2004). Computer-aided resonance assignment (CARA). Verl Goldau Cantina Switz. Retrieved from http://cara.nmr-software.org/portal/
   Google Scholar
• King, G. F., & Hardy, M. C. (2013). Spider-venom peptides: Structure, pharmacology, and potential for control of insect pests. Annual Review of Entomology, 58(1), 475–496. doi:10.1146/annurev-ento-120811-153650
   PubMedGoogle Scholar
• Klint, J. K., Senff, S., Saez, N. J., Seshadri, R., Lau, H. Y., Bende, N. S., … King, G. F. (2013). Production of recombinant disulfide-rich venom peptides for structural and functional analysis via expression in the periplasm of E. coli. PLoS One, 8(5), e63865. doi:10.1371/journal.pone.0063865
   PubMed Web of Science ®Google Scholar
• Koundal, K., & Rajendran, P. (2003). Plant insecticidal proteins and their potential for developing transgenics resistant to insect pests. Indian Journal of Biotechnology, 2, 110–120. Retrieved from http://nopr.niscair.res.in/handle/123456789/11293
   Google Scholar
• Krizova, H., Zidek, L., Stone, M. J., Novotny, M. V., & Sklenar, V. (2004). Temperature-dependent spectral density analysis applied to monitoring backbone dynamics of major urinary protein-I complexed with the pheromone 2- sec-butyl-4,5-dihydrothiazole. Journal of Biomolecular NMR, 28, 369–384. doi:10.1023/B:JNMR.0000015404.61574.65
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., Moss, D. S., & Thornton, J. M. (1993). Main-chain bond lengths and bond angles in protein structures. Journal of Molecular Biology, 231(4), 1049–1067. doi:10.1006/jmbi.1993.1351
   PubMed Web of Science ®Google Scholar
• Lefevre, J. F., Dayie, K. T., Peng, J. W., & Wagner, G. (1996). Internal mobility in the partially folded DNA binding and dimerization domains of GAL4: NMR analysis of the N–H spectral density functions. Biochemistry, 35, 2674–2686. doi:10.1021/bi9526802
   PubMed Web of Science ®Google Scholar
• Marques, J. R. F., Da Fonseca, R. R., Drury, B., & Melo, A. (2010). Conformational characterization of disulfide bonds: A tool for protein classification. Journal of Theoretical Biology, 267(3), 388–395. doi:10.1016/j.jtbi.2010.09.012
   PubMed Web of Science ®Google Scholar
• Oerke, E. C. (2006). Crop losses to pests. The Journal of Agricultural Science, 144(1), 31–43. doi:10.1017/S0021859605005708
   Web of Science ®Google Scholar
• Patankar, A. G., Giri, A. P., Harsulkar, A. M., Sainani, M. N., Deshpande, V. V., Ranjekar, P. K., & Gupta, V. S. (2001). Complexity in specificities and expression of Helicoverpa armigera gut proteinases explains polyphagous nature of the insect pest. Insect Biochemistry and Molecular Biology, 31(4/5), 453–464. doi:10.1016/S0965-1748(00)00150-8
   PubMed Web of Science ®Google Scholar
• Peng, J. W., & Wagner, G. (1992). Mapping of spectral density-functions using heteronuclear NMR relaxation measurements. Journal of Magnetic Resonance, 98, 308–332. doi:10.1016/0022-2364(92)90135-T
   Web of Science ®Google Scholar
• Que, Q., Chilton, M. D., de Fontes, C. M., He, C., Nuccio, M., Zhu, T., … Shi, L. (2010). Trait stacking in transgenic crops: Challenges and opportunities. GM Crops, 1(4), 220–229. doi:10.4161/gmcr.1.4.13439
   PubMedGoogle Scholar
• Renner, C., Baumgartner, R., Noegel, A. A., & Holak, T. A. (1998). Backbone dynamics of the CDK inhibitor p19(INK4d) studied by 15N NMR relaxation experiments at two field strengths. Journal of Molecular Biology, 283(1), 221–229. doi:10.1006/jmbi.1998.2079
   PubMed Web of Science ®Google Scholar
• Ryan, C. A. (1990). Protease inhibitors in plants: Genes for improving defenses against insects and pathogens. Annual Review of Phytopathology, 28(1), 425–449.
   Web of Science ®Google Scholar
• Sattler, M., Schleucher, J., & Griesinger, C. (1999). Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Progress in Nuclear Magnetic Resonance Spectroscopy, 34(2), 93–158. doi:10.1016/S0079-6565(98)00025-9
   Web of Science ®Google Scholar
• Savage, G. P., & Morrison, S. C. (2003). Trypsin inhibitors. Encyclopedia of Food Sciences and Nutrition. Cambridge, MA: Academic Press. doi:10.1016/B0-12-227055-X/00934-2
   Google Scholar
• Schirra, H. J., Guarino, R. F., Anderson, M. A., & Craik, D. J. (2010). Selective removal of individual disulfide bonds within a potato type II serine proteinase inhibitor from Nicotiana alata reveals differential stabilization of the reactive-site loop. Journal of Molecular Biology, 395(3), 609–626. doi:10.1016/j.jmb.2009.11.031
   PubMed Web of Science ®Google Scholar
• Schirra, H. J., Scanlon, M. J., Lee, M. C., Anderson, M. A., & Craik, D. J. (2001). The solution structure of C1–T1, a two-domain proteinase inhibitor derived from a circular precursor protein from Nicotiana alata. Journal of Molecular Biology, 306(1), 69–79.
   PubMed Web of Science ®Google Scholar
• Schmidt, B., Ho, L., & Hogg, P. J. (2006). Allosteric disulfide bonds. Biochemistry, 45(24), 7429–7433. doi:10.1021/bi0603064
   PubMed Web of Science ®Google Scholar
• Shen, Y., Delaglio, F., Cornilescu, G., & Bax, A. (2009). TALOS+: A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. Journal of Biomolecular NMR, 44(4), 213–223. doi:10.1007/s10858-009-9333-z
   PubMed Web of Science ®Google Scholar
• Srivastava, A. K., Sharma, Y., & Chary, K. V. (2010). A natively unfolded betagamma-crystallin domain from Hahella chejuensis. Biochemistry, 49(45), 9746–9755. doi:10.1021/bi101000m
   PubMed Web of Science ®Google Scholar
• Su, C. T., Kwoh, C. K., Verma, C. S., & Gan, S. K. (2018). Modeling the full length HIV-1 Gag polyprotein reveals the role of its p6 subunit in viral maturation and the effect of non-cleavage site mutations in protease drug resistance. Journal of Biomolecular Structure and Dynamics, 36(16), 4366–4377. doi:10.1080/07391102.2017.1417160
   PubMed Web of Science ®Google Scholar
• Tabashnik, B. E., Brevault, T., & Carriere, Y. (2013). Insect resistance to Bt crops: Lessons from the first billion acres. Nature Biotechnology, 31(6), 510–521.
   PubMed Web of Science ®Google Scholar
• Tamhane, V. A., Chougule, N. P., Giri, A. P., Dixit, A. R., Sainani, M. N., & Gupta, V. S. (2005). In vivo and in vitro effect of Capsicum annum proteinase inhibitors on Helicoverpa armigera gut proteinases. Biochimica Et Biophysica Acta-General Subjects, 1722(2), 156–167. doi:10.1016/j.bbagen.2004.12.017
   PubMed Web of Science ®Google Scholar
• Tamhane, V. A., Giri, A. P., & Gupta, V. S. (2007). Helicoverpa armigera: Ecology and control using novel biotechnological approaches. Encyclopedia of Pest Management, 2, 232–236. doi: 10.1201/9781420068467 and 10.1081/E-EPM-120041174, Retrieved from https://www.crcpress.com/Encyclopedia-of-Pest-Management-Volume-II/Pimentel-PhD/p/book/9781420053616
   Google Scholar
• Tamhane, V. A., Giri, A. P., Sainani, M. N., & Gupta, V. S. (2007). Diverse forms of Pin-II family proteinase inhibitors from Capsicum annuum adversely affect the growth and development of Helicoverpa armigera. Gene, 403(1-2), 29–38. doi:10.1016/j.gene.2007.07.024
   PubMed Web of Science ®Google Scholar
• Tay, W. T., Soria, M. F., Walsh, T., Thomazoni, D., Silvie, P., Behere, G. T., … Downes, S. (2013). A brave new world for an old world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS One, 8, e80134. doi:10.1371/journal.pone.0080134
   Web of Science ®Google Scholar
• Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., … Laue, E. D. (2005). The CCPN data model for NMR spectroscopy: Development of a software pipeline. Proteins: Structure, Function, and Bioinformatics, 59(4), 687–696. doi:10.1002/prot.20449
   PubMed Web of Science ®Google Scholar
• Wishart, D. S., Bigam, C. G., Yao, J., Abildgaard, F., Dyson, H. J., Oldfield, E., … Sykes, B. D. (1995). 1H, 13C and 15N chemical shift referencing in biomolecular NMR. Journal of Biomolecular NMR, 6(2), 135–140.
   PubMed Web of Science ®Google Scholar