Increased RNAi efficacy in Spodoptera exigua via the formulation of dsRNA with guanylated polymers

Frontiers in Physiology

Volumn 9, Issue APR, 2018, Pages

  Christiaens, Olivier ^a   Tardajos, Myriam G ^a   Reyna, Zarel L Martinez ^a   Dash, Mamoni ^a,b   Dubruel, Peter ^a   Smagghe, Guy ^a  

^a GHENT UNIVERSITY   (Belgium)

^b INSTITUTE OF LIFE SCIENCES   (India)

Author keywords

Crop protection; DsRNA degradation; DsRNA polymer nanocarriers; Lepidoptera; RNA interference; Spodoptera exigua

Indexed keywords

CHITIN SYNTHASE; GUANIDINE; NANOPARTICLE; POLYMER; RNA;

ARTICLE; CELL TRANSPORT; CONTROLLED STUDY; EX VIVO STUDY; IN VIVO STUDY; INTESTINAL SECRETION; MORTALITY RATE; NONHUMAN; RNA DEGRADATION; RNA INTERFERENCE; RNA SYNTHESIS; SPODOPTERA EXIGUA;

EID: 85045047416     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2018.00316     Document Type: Article

References (50)

1. Allen, M. L., and Walker, W. B. III. (2012). Saliva of Lygus lineolaris digests double stranded ribonucleic acids. J. Insect Physiol. 58, 391-396. doi: 10.1016/j.jinsphys.2011.12.014
2. Arimatsu, Y., Furuno, T., Sugimura, Y., Togoh, M., Ishihara, R., Tokizane, M., et al. (2007). Purification and properties of double-stranded RNA-degrading nuclease, dsRNase, from the digestive juice of the silkworm, Bombyx mori. J. Insect Biotechnol. Sericol. 76, 57-62. doi: 10.1016/j.ibmb.2006.11.004
3. Bachman, P. M., Bolognesi, R., Moar, W. J., Mueller, G. M., Paradise, M. S., Ramaseshadri, P., et al. (2013). Characterization of the spectrum of insecticidal activity of a double-stranded RNA with targeted activity against Western Corn Rootworm (Diabrotica virgifera virgifera LeConte). Transgenic Res. 22, 1207-1222. doi: 10.1007/s11248-013-9716-5
4. Baum, J. A., Bogaert, T., Clinton, W., Heck, G. R., Feldmann, P., Ilagan, O., et al. (2007). Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25, 1322-1326. doi: 10.1038/nbt1359
5. Bolognesi, R., Ramaseshadri, P., Anderson, J., Bachman, P., Clinton, W., Flannagan, R., et al. (2012). Characterizing the mechanism of action of double-stranded RNA activity against Western Corn Rootworm (Diabrotica virgifera virgifera LeConte). PLoS ONE 7:e47534. doi: 10.1371/journal.pone.0047534
6. Cappelle, K., de Oliveira, C. F. R., Van Eynde, B., Christiaens, O., and Smagghe, G. (2016). The involvement of clathrin-mediated endocytosis and two Sid-1-like transmembrane proteins in doublestranded RNA uptake in the Colorado potato beetle midgut. Insect Mol. Biol. 25, 315-323. doi: 10.1111/imb.12222
7. Cavallaro, G., Sardo, C., Craparo, E. F., Porsio, B., and Giammona, G. (2017). Polymeric nanoparticles for siRNA delivery: Production and applications. Int. J. Pharm. 525, 313-333. doi: 10.1016/j.ijpharm.2017.04.008
8. Choi, J. L., Tan, J.-K. Y., Sellers, D. L., Wei, H., Horner, P. J., and Pun, S. H. (2015). Guanidinylated block copolymers for gene transfer: a comparison with amine-based materials for in vitro and in vivo gene transfer efficiency. Biomaterials 54, 87-96. doi: 10.1016/j.biomaterials.2015.03.008
9. Christiaens, B., Dubruel, P., Grooten, J., Goethals, M., Vandekerckhove, J., Schacht, E., et al. (2005). Enhancement of polymethacrylate-mediated gene delivery by Penetratin. Eur. J. Pharm. Sci. 24, 525-537. doi: 10.1016/j.ejps.2005.01.004
10. Christiaens, O., and Smagghe, G. (2014). The challenge of RNAi-mediated control of hemipterans. Curr. Opin. Insect Sci. 6, 15-21. doi: 10.1016/j.cois.2014.09.012
11. Christiaens, O., Swevers, L., and Smagghe, G. (2014). DsRNA degradation in the pea aphid (Acyrthosiphon pisum) associated with lack of response in RNAi feeding and injection assay. Peptides 53, 307-314. doi: 10.1016/j.peptides.2013.12.014
12. De Wolf, H. K., De Raad, M., Snel, C., Van Steenbergen, M. J., Fens, M. H., Storm, G., et al. (2007). Biodegradable poly (2-dimethylamino ethylamino) phosphazene for in vivo gene delivery to tumor cells. Effect of polymer molecular weight. Pharm. Res. 24, 1572-1580. doi: 10.1007/s11095-007-9299-z
13. Dubelman, S., Fischer, J., Zapata, F., Huizinga, K., Jiang, C., Uffman, J., et al. (2014). Environmental fate of double-stranded RNA in agricultural soils. PLoS ONE 9:e93155. doi: 10.1371/journal.pone.0093155
14. Feinberg, E. H., and Hunter, C. P. (2003). Transport of dsRNA into cells by the transmembrane protein SID-1. Science 301, 1545-1547. doi: 10.1126/science.1087117
15. Funhoff, A. M., Van Nostrum, C. F., Lok, M. C., Fretz, M. M., Crommelin, D. J., and Hennink, W. E. (2004). Poly (3-guanidinopropyl methacrylate): a novel cationic polymer for gene delivery. Bioconj. Chem. 15, 1212-1220. doi: 10.1021/bc049864q
16. Garbutt, J. S., Bellés, X., Richards, E. H., and Reynolds, S. E. (2013). Persistence of double-stranded RNA in insect hemolymph as a potential determiner of RNA interference success: evidence from Manduca sexta and Blattella germanica. J. Insect Physiol. 59, 171-178. doi: 10.1016/j.jinsphys.2012.05.013
17. Gong, L., Chen, Y., Hu, Z., and Hu, M. (2013). Testing insecticidal activity of novel chemically synthesized siRNA against Plutella xylostella under laboratory and field conditions. PLoS ONE 8:e62990. doi: 10.1371/journal.pone.0062990
18. Guo, P., Gu, W., Chen, Q., Lu, H., Han, X., Li, W., et al. (2015). Dual functionalized amino poly (glycerol methacrylate) with guanidine and Schiff-base linked imidazole for enhanced gene transfection and minimized cytotoxicity. J. Mater. Chem. B 3, 6911-6918. doi: 10.1039/C5TB01291K
19. He, B., Chu, Y., Yin, M., Müellen, K., An, C., and Shen, J. (2013). Fluorescent nanoparticle delivered dsRNA toward genetic control of insect pests. Adv. Mater. Weinheim. 25, 4580-4584. doi: 10.1002/adma.201301201
20. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F., and Vandesompele, J. (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8:R19. doi: 10.1186/gb-2007-8-2-r19
21. Huvenne, H., and Smagghe, G. (2010). Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J. Insect Physiol. 56, 227-235. doi: 10.1016/j.jinsphys.2009.10.004
22. Ji, W., Panus, D., Palumbo, R. N., Tang, R., and Wang, C. (2011). Poly (2-aminoethyl methacrylate) with well-defined chain length for DNA vaccine delivery to dendritic cells. Biomacromolecules 12, 4373-4385. doi: 10.1021/bm201360v
23. Joga, M. R., Zotti, M. J., Smagghe, G., and Christiaens, O. (2016). RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Front. Physiol. 7:553. doi: 10.3389/fphys.2016.00553
24. Jones, S. K., Sarkar, A., Feldmann, D. P., Hoffmann, P., and Merkel, O. (2017). Revisiting the value of competition assays in folate receptor-mediated drug delivery. Biomaterials 138, 35-45. doi: 10.1016/j.biomaterials.2017.05.034
25. Kumar, D. R., Kumar, P. S., Gandhi, M. R., Al-Dhabi, N. A., Paulraj, M. G., and Ignacimuthu, S. (2016). Delivery of chitosan/dsRNA nanoparticles for silencing of wing development vestigial (vg) gene in Aedes aegypti mosquitoes. Int. J. Biol. Macromol. 86, 89-95. doi: 10.1016/j.ijbiomac.2016.01.030
26. Kwon, D. H., Park, J. H., and Lee, S. H. (2013). Screening of lethal genes for feeding RNAi by leaf disc-mediated systematic delivery of dsRNA in Tetranychus urticae. Pestic. Biochem. Physiol. 105, 69-75. doi: 10.1016/j.pestbp.2012.12.001
27. Lin, D., Jiang, Q., Cheng, Q., Huang, Y., Huang, P., Han, S., et al. (2013). Polycation-detachable nanoparticles self-assembled from mPEG-PCL-g-SS-PDMAEMA for in vitro and in vivo siRNA delivery. Acta Biomater. 9, 7746-7757. doi: 10.1016/j.actbio.2013.04.031
28. Liu, J., Swevers, L., Iatrou, K., Huvenne, H., and Smagghe, G. (2012). Bombyx mori DNA/RNA non-specific nuclease: expression of isoforms in insect culture cells, subcellular localization and functional assays. J. Insect Physiol. 58, 1166-1176. doi: 10.1016/j.jinsphys.2012.05.016
29. Luo, Y., Wang, X., Wang, X., Yu, D., Chen, B., and Kang, L. (2013). Differential responses of migratory locusts to systemic RNA interference via double-stranded RNA injection and feeding. Insect Mol. Biol. 22, 574-583. doi: 10.1111/imb.12046
30. Mattheis, C., Wang, H., Meister, C., and Agarwal, S. (2013). Effect of guanidinylation on the properties of poly (2-aminoethylmethacrylate)-based antibacterial materials. Macromol. Biosci. 13, 242-255. doi: 10.1002/mabi.201200217
31. McEwan, D. L., Weisman, A. S., and Hunter, C. P. (2012). Uptake of extracellular double-stranded RNA by SID-2. Mol. Cell 47, 746-754. doi: 10.1016/j.molcel.2012.07.014
32. Miller, S. C., Brown, S. J., and Tomoyasu, Y. (2008). Larval RNAi in Drosophila? Dev. Genes Evol. 218, 505-510. doi: 10.1007/s00427-008-0238-8
33. Price, D. R. G., and Gatehouse, J. A. (2008). RNAi-mediated crop protection against insects. Trends Biotechnol. 26, 393-400. doi: 10.1016/j.tibtech.2008.04.004
34. Saleh, M.-C., van Rij, R. P., Hekele, A., Gillis, A., Foley, E., O'Farrell, P. H., et al. (2006). The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat. Cell Biol. 8, 793-802. doi: 10.1038/ncb1439
35. Smagghe, G., and Degheele, D. (1994). Action of a novel nonsteroidal ecdysteroid mimic, tebufenozide (RH-5992), on insects of different orders. Pest Manage. Sci. 42, 85-92. doi: 10.1002/ps.2780420204
36. Song, H., and Chu, C. (2012). Synthesis and characterization of a new family of cationic amino acid-based poly (ester amide) s and their biological properties. J. Appl. Polym. Sci. 124, 3840-3853. doi: 10.1002/app.35512
37. Synatschke, C. V., Schallon, A., Jérôme, V. R., Freitag, R., and Müller, A. H. (2011). Influence of polymer architecture and molecular weight of poly (2-(dimethylamino) ethyl methacrylate) polycations on transfection efficiency and cell viability in gene delivery. Biomacromolecules 12, 4247-4255. doi: 10.1021/bm201111d
38. Taning, C. N. T., Christiaens, O., Berkvens, N., Casteels, H., Maes, M., and Smagghe, G. (2016). Oral RNAi to control Drosophila suzukii: laboratory testing against larval and adult stages. J. Pest Sci. 89, 803-814. doi: 10.1007/s10340-016-0736-9
39. Terenius, O., Papanicolaou, A., Garbutt, J. S., Eleftherianos, I., Huvenne, H., Kanginakudru, S., et al. (2011). RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design. J. Insect Physiol. 57, 231-245. doi: 10.1016/j.jinsphys.2010.11.006
40. Timin, A. S., Muslimov, A. R., Lepik, K. V., Epifanovskaya, O. S., Shakirova, A. I., Mock, U., et al. (2018). Efficient gene editing via non-viral delivery of CRISPR-Cas9 system using polymeric and hybrid microcarriers. Nanomedicine 14, 97-108. doi: 10.1016/j.nano.2017.09.001
41. Tomoyasu, Y., Miller, S. C., Tomita, S., Schoppmeier, M., Grossmann, D., and Bucher, G. (2008). Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol. 9:R10. doi: 10.1186/gb-2008-9-1-r10
42. Treat, N. J., Smith, D., Teng, C., Flores, J. D., Abel, B. A., York, A. W., et al. (2011). Guanidine-containing methacrylamide (Co) polymers via a RAFT: toward a cell-penetrating peptide mimic. ACS Macro Lett. 1, 100-104. doi: 10.1021/mz200012p
43. Ulvila, J., Parikka, M., Kleino, A., Sormunen, R., Ezekowitz, R. A., Kocks, C., et al. (2006). Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J. Biol. Chem. 281, 14370-14375. doi: 10.1074/jbc. M513868200
44. Whyard, S., Singh, A. D., and Wong, S. (2009). Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem. Mol. Biol. 39, 824-832. doi: 10.1016/j.ibmb.2009.09.007
45. Winston, W. M., Molodowitch, C., and Hunter, C. P. (2002). Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295, 2456-2459. doi: 10.1126/science.1068836
46. Winston, W. M., Sutherlin, M., Wright, A. J., Feinberg, E. H., and Hunter, C. P. (2007). Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc. Natl. Acad. Sci. U.S.A. 104, 10565-10570. doi: 10.1073/pnas.0611282104
47. Wynant, N., Santos, D., Verdonck, R., Spit, J., Van Wielendaele, P., and Vanden Broeck, J. (2014). Identification, functional characterization and phylogenetic analysis of double stranded RNA degrading enzymes present in the gut of the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol. 46, 1-8. doi: 10.1016/j.ibmb.2013.12.008
48. Zhang, X., Mysore, K., Flannery, E., Michel, K., Severson, D. W., Zhu, K. Y., et al. (2015). Chitosan/interfering RNA nanoparticle mediated gene silencing in disease vector mosquito larvae. J. Vis. Exp. 2015:e52523. doi: 10.3791/52523
49. Zhang, X., Zhang, J., and Zhu, K. Y. (2010). Chitosan/double-stranded RNA nanoparticle-mediated RNA interference to silence chitin synthase genes through larval feeding in the African malaria mosquito (Anopheles gambiae). Insect Mol. Biol. 19, 683-693. doi: 10.1111/j.1365-2583.2010.01029.x
50. Zhu, F., Xu, J., Palli, R., Ferguson, J., and Palli, S. R. (2011). Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manage. Sci. 67, 175-182. doi: 10.1002/ps.2048