A nuclease specific to lepidopteran insects suppresses RNAi

Journal of Biological Chemistry

Volumn 293, Issue 16, 2018, Pages 6011-6021

  Guan, Ruo Bing ^a   Li, Hai Chao ^a   Fan, Yu Jie ^a   Hu, Shao Ru ^a,b   Christiaens, Olivier ^c   Smagghe, Guy ^c   Miao, Xue Xia ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ENCODING (SYMBOLS); GENE ENCODING; PROTEINS;

AGRICULTURAL PESTS; DROSOPHILA MELANOGASTER; HOMOLOGOUS SEQUENCES; LEPIDOPTERAN INSECTS; SINGLE STRANDED RNA; STRUCTURAL SIMILARITY; THREE-DIMENSIONAL STRUCTURE; TRANSCRIPTOME ANALYSIS;

EFFICIENCY;

DICER; DOUBLE STRANDED DNA; DOUBLE STRANDED RNA; EXONUCLEASE; EXONUCLEASE I; NUCLEASE; RNAI EFFICIENCY RELATED NUCLEASE; SINGLE STRANDED RNA; UNCLASSIFIED DRUG; DEOXYRIBONUCLEASE; INSECT PROTEIN; RIBONUCLEASE; TRANSCRIPTOME;

ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE KNOCKDOWN; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LEPIDOPTERA; NONHUMAN; OSTRINIA; OSTRINIA FURNACALIS; PRIORITY JOURNAL; RNA DEGRADATION; RNA INTERFERENCE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY; THREE DIMENSIONAL IMAGING; UP56 GENE; UPREGULATION; VALIDATION PROCESS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENE; GENETICS; METABOLISM; MOLECULAR MODEL; PHYLOGENY; RNA STABILITY; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; DEOXYRIBONUCLEASES; GENES, INSECT; INSECT PROTEINS; LEPIDOPTERA; MODELS, MOLECULAR; PHYLOGENY; RIBONUCLEASES; RNA INTERFERENCE; RNA STABILITY; SEQUENCE ALIGNMENT; TRANSCRIPTOME;

EID: 85045847808     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.RA117.001553     Document Type: Article

References (41)

1. Mao, Y. B., Cai, W. J., Wang, J. W., Hong, G. J., Tao, X. Y., Wang, L. J., Huang, Y. P., and Chen, X. Y. (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 25, 1307-1313 CrossRef Medline
2. Baum, J. A., Bogaert, T., Clinton, W., Heck, G. R., Feldmann, P., Ilagan, O., Johnson, S., Plaetinck, G., Munyikwa, T., Pleau, M., Vaughn, T., and Roberts, J. (2007) Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25, 1322-1326 CrossRef Medline
3. Wang, Y., Zhang, H., Li, H., and Miao, X. (2011) Second-generation sequencing supply an effective way to screen RNAi targets in large scale for potential application in pest insect control. PLoS ONE 6, e18644 CrossRef Medline
4. Zhang, H., Li, H. C., and Miao, X. X. (2013) Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control. Insect Sci. 20, 15-30 CrossRef Medline
5. Terenius, O., Papanicolaou, A., Garbutt, J. S., Eleftherianos, I., Huvenne, H., Kanginakudru, S., Albrechtsen, M., An, C., Aymeric, J. L., Barthel, A., Bebas, P., Bitra, K., Bravo, A., Chevalier, F., Collinge, D. P., 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 CrossRef Medline
6. 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 Medline
7. Santos, D., Broeck, J. V., and Wynant, N. (2014) Systemic RNA interference in locusts: reverse genetics and possibilities for locust pest control. Curr. Opin. Insect Sci. 6, 9 -14 CrossRef
8. Spit, J., Philips, A., Wynant, N., Santos, D., Plaetinck, G., and Vanden Broeck, J. (2017) Knockdown of nuclease activity in the gut enhances RNAi efficiency in the Colorado potato beetle, Leptinotarsa decemlineata, but not in the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol. 81, 103-116 CrossRef Medline
9. Ding, S. W. (2010) RNA-based antiviral immunity. Nat. Rev. Immunol. 10, 632- 644 CrossRef Medline
10. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806 - 811 CrossRef Medline
11. Tijsterman, M., and Plasterk, R. H. (2004) Dicers at RISC: the mechanism of RNAi. Cell 117, 1-3 CrossRef Medline
12. Li, H., Li, W. X., and Ding, S. W. (2002) Induction and suppression of RNA silencing by an animal virus. Science 296, 1319 -1321 CrossRef Medline
13. Hannon, G. J. (2002) RNA interference. Nature 418, 244-251 CrossRef Medline
14. 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 CrossRef Medline
15. Dowling, D., Pauli, T., Donath, A., Meusemann, K., Podsiadlowski, L., Petersen, M., Peters, R. S., Mayer, C., Liu, S., Zhou, X., Misof, B., and Niehuis, O. (2016) Phylogenetic origin and diversification of RNAi pathway genes in insects. Genome Biol. Evol. 8, 3784 -3793 Medline
16. Shukla, J. N., Kalsi, M., Sethi, A., Narva, K. E., Fishilevich, E., Singh, S., Mogilicherla, K., and Palli, S. R. (2016) Reduced stability and intracellular transport of dsRNA contribute to poor RNAi response in lepidopteran insects. RNA Biol. 13, 656 - 669 CrossRef Medline
17. Allen, M. L., and Walker, W. B., 3rd. (2012) Saliva of Lygus lineolaris digests double stranded ribonucleic acids. J. Insect Physiol. 58, 391-396 CrossRef Medline
18. 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 CrossRef Medline
19. 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 CrossRef Medline
20. 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 CrossRef Medline
21. Ivashuta, S., Zhang, Y., Wiggins, B. E., Ramaseshadri, P., Segers, G. C., Johnson, S., Meyer, S. E., Kerstetter, R. A., McNulty, B. C., Bolognesi, R., and Heck, G. R. (2015) Environmental RNAi in herbivorous insects. RNA 21, 840 - 850 CrossRef Medline
22. Christiaens, O., Prentice, K., Pertry, I., Ghislain, M., Bailey, A., Niblett, C., Gheysen, G., and Smagghe, G. (2016) RNA interference: a promising biopesticide strategy against the African sweetpotato weevil Cylas brun-neus. Sci. Rep. 6, 38836 CrossRef Medline
23. Prentice, K., Christiaens, O., Pertry, I., Bailey, A., Niblett, C., Ghislain, M., Gheysen, G., and Smagghe, G. (2017) RNAi-based gene silencing through dsRNA injection or ingestion against the African sweet potato weevil Cylas puncticollis (Coleoptera: Brentidae). Pest Management Science 73, 44 -52 CrossRef Medline
24. Arimatsu, Y., Kotani, E., Sugimura, Y., and Furusawa, T. (2007) Molecular characterization of a cDNA encoding extracellular dsRNase and its expression in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 37, 176 -183 CrossRef Medline
25. 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 CrossRef Medline
26. Meiss, G., Gast, F. U., and Pingoud, A. M. (1999) The DNA RNA nonspecific Serratia nuclease prefers double-stranded A-form nucleic acids as substrates. J. Mol. Biol. 288, 377-390 CrossRef Medline
27. Kennedy, S., Wang, D., and Ruvkun, G. (2004) A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427, 640 - 645
28. Lu, R., Yigit, E., Li, W. X., and Ding, S. W. (2009) An RIG-I-like RNA helicase mediates antiviral RNAi downstream of viral siRNA biogenesis in Caenorhabditis elegans. PLoS Pathog. 5, e1000286 CrossRef Medline
29. Weinheimer, I., Jiu, Y., Rajamäki, M. L., Matilainen, O., Kallijärvi, J., Cuel-lar, W. J., Lu, R., Saarma, M., Holmberg, C. I., Jäntti, J., and Valkonen, J. P. (2015) Suppression of RNAi by dsRNA-degrading RNaseIII enzymes of viruses in animals and plants. PLoS Pathog. 11, e1004711 CrossRef Medline
30. Guan, R. B., Li, H. C., and Miao, X. X. (2017) Prediction of effective RNA interference targets and pathway-related genes in lepidopteran insects by RNA sequencing analysis. Insect Sci. 10.1111/1744 -7917.12437
31. Arcus, V. L., McKenzie, J. L., Robson, J., and Cook, G. M. (2011) The PIN-domain ribonucleases and the prokaryotic VapBC toxin-antitoxin array. Protein Eng. Des. Sel. 24, 33- 40 CrossRef Medline
32. Glavan, F., Behm-Ansmant, I., Izaurralde, E., and Conti, E. (2006) Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J. 25, 5117-5125 CrossRef Medline
33. Burand, J. P., and Hunter, W. B. (2013) RNAi: future in insect management. J. Invertebr. Pathol. 112, S68 -S74 CrossRef Medline
34. Gerdes, K., Christensen, S. K., and Løbner-Olesen, A. (2005) Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3, 371-382 CrossRef Medline
35. Page, M. F., Carr, B., Anders, K. R., Grimson, A., and Anderson, P. (1999) SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell Biol. 19, 5943-5951 CrossRef Medline
36. Domeier, M. E., Morse, D. P., Knight, S. W., Portereiko, M., Bass, B. L., and Mango, S. E. (2000) A link between RNA interference and nonsense-mediated decay in Caenorhabditis elegans. Science 289, 1928 -1931 CrossRef Medline
37. Clissold, P. M., and Ponting, C. P. (2000) PIN domains in nonsense-mediated mRNA decay and RNAi. Curr. Biol. 10, R888 - 890 CrossRef Medline
38. Mourrain, P., Béclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J. B., Jouette, D., Lacombe, A. M., Nikic, S., Picault, N., Remoue, K., Sanial, M., Vo, T. A., and Vaucheret, H. (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101, 533-542 CrossRef Medline
39. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H., and Fire, A. (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107, 465- 476 CrossRef Medline
40. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 ( C(T)) method. Methods 25, 402- 408 CrossRef Medline
41. Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., and Wittwer, C. T. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611- 622 CrossRef Medline