1,859
Views
13
CrossRef citations to date
0
Altmetric
Research Paper

Dissecting protein domain variability in the core RNA interference machinery of five insect orders

ORCID Icon, ORCID Icon, , , , , , ORCID Icon, , , ORCID Icon & show all
Pages 1653-1681 | Received 27 Jul 2020, Accepted 02 Dec 2020, Published online: 31 Dec 2020

References

  • Fire A, Xu S, Montgomery MK, et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998 Feb;391(6669):806–811.
  • Olsen PH, The AV. lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol. 1999 Dec;216(2):671–680.
  • Napoli C, Lemieux C, Jorgensen R. Introduction of a chimeric chalcone synthase gene into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell. 1990 Apr;2(4):279–289.
  • Kavi HH, Fernandez H, Xie W, et al. Genetics and biochemistry of RNAi in Drosophila. Curr Top Microbiol Immunol. 2008;320:37–75.
  • Li H, Li WX, Ding SW. Induction and suppression of RNA silencing by an animal virus. Science. 2002 May;296(5571):1319–1321.
  • Chow J, Kagan JC. The fly way of antiviral resistance and disease tolerance. Adv Immunol. 2018 Sep;140:59–93.
  • Leggewie M, Schnettler E. RNAi-mediated antiviral immunity in insects and their possible application. Curr Opin Virol. 2018 Nov;32:108–114.
  • Swevers L, Liu J, Smagghe G. Defense mechanisms against viral infection in Drosophila: rNAi and non-rNAi. Viruses. 2018 May;10(5):230.
  • Sempere LF, Freemantle S, Pitha-Rowe I, et al. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 2004 Feb;5:R13.
  • Mallory A, Vaucheret H. Form, function, and regulation of Argonaute proteins. Plant Cell. 2010 Dec;22(12):3879–3889.
  • Okamura K, Lai EC. Endogenous small interfering RNAs in animals. Nat Rev Mol Cell Biol. 2008 Sep;9(9):673–678.
  • Lin H, Spradling AC. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development. 1997 Jun;124:2463–2476.
  • Brennecke J, Aravin AA, Stark A, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007 Mar;128(6):1089–1103.
  • Joga MR, Zotti MJ, Smagghe G, et al. RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Front Physiol. 2016 Nov;7:553.
  • Airs PM, Bartholomay LC. RNA interference for mosquito and mosquito-borne disease control. Insects. 2017 Jan;8(1): 4.
  • Mamta B, Rajam MV. RNAi technology: a new platform for crop pest control. Physiol Mol Biol Plants. 2017 Jul;23(3):487–501.
  • Zhang J, Khan SA, Heckel DG, et al. Next-generation insect-resistant plants: rNAi-mediated crop protection. Trends Biotechnol. 2017 Jul;35(9):871–882.
  • Yu N, Christiaens O, Liu J, et al. Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Sci. 2013 Feb;20(1):4–14.
  • Agrawal A, Rajamani V, Reddy VS, et al. Transgenic plants over-expressing insect-specific microRNA acquire insecticidal activity against Helicoverpa armigera: an alternative to Bt-toxin technology. Transgenic Res. 2015 Oct;24(5):791–801.
  • Yogindran S, Rajam MV. Artificial miRNA-mediated silencing of ecdysone receptor (EcR) affects larval development and oogenesis in Helicoverpa armigera. Insect Biochem Mol Biol. 2016 Jul;77:21–30.
  • Saini RP, Raman V, Dhandapani G, et al. Silencing of HaAce1 gene by host-delivered artificial microRNA disrupts growth and development of Helicoverpa armigera. PLoS One. 2018 Mar;13(3):e0194150.
  • Sharath Chandra G, Asokan R, Manamohan M, et al. Enhancing RNAi by using concatemerized double-stranded RNA. Pest Manag Sci. 2019 Feb;75:506–514.
  • Whitten MM. Novel RNAi delivery systems in the control of medical and veterinary pests. Curr Opin Insect Sci. 2019 Feb;34:1–6.
  • Ulvila J, Parikka M, Kleino A, et al. Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J Biol Chem. 2006 May;281(20):14370–14375.
  • Jin S, Singh ND, Li L, et al. Engineered chloroplast dsRNA silences cytochrome p450 monooxygenase, V-ATPase and chitin synthase genes in the insect gut and disrupts Helicoverpa zea larval development and pupation. Plant Biotechnol J. 2015 Mar;13(3):435–446.
  • Bally J, Fishilevich E, Bowling AJ, et al. Improved insect-proofing: expressing double-stranded RNA in chloroplasts. Pest Manag Sci. 2018 Aug;74(8):1751–1758.
  • Wang K, Peng Y, Fu W, et al. Key factors determining variations in RNA interference efficacy mediated by different double-stranded RNA lengths in Tribolium castaneum. Insect Mol Biol. 2019;28(2):235–245.
  • Liu J, Swevers L, Iatrou K, et al. Bombyx mori DNA/RNA non-specific nuclease: expression of isoforms in insect culture cells, subcellular localization and functional assays. J Insect Physiol. 2012 Aug;58(8):1166–1176.
  • Wynant N, Santos D, Verdonck R, et al. Identification. Schistocerca gregaria. Insect Biochem. Mol. Biol: functional characterization and phylogenetic analysis of double stranded RNA degrading enzymes present in the gut of the desert locust; 2014 Jan.
  • Almeida Garcia R, Lima Pepino Macedo L, Cabral Do Nascimento D, et al. Nucleases as a barrier to gene silencing in the cotton boll weevil. PLoS One. Anthonomus Grandis. 2017 Dec;12:e0189600.
  • Spit J, Philips A, Wynant N, et al. 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. 2017 Jan;81:103–116.
  • Peng Y, Wang K, Fu W, et al. Biochemical comparison of dsRNA degrading nucleases in four different insects. Front Physiol. 2018 May;9:624.
  • Prentice K, Smagghe G, Gheysen G, et al. Nuclease activity decreases the RNAi response in the sweetpotato weevil Cylas puncticollis. Insect Biochem Mol Biol. 2019 Jul;110:80–89.
  • Song H, Fan Y, Zhang J, et al. Contributions of dsRNases to differential RNAi efficiencies between the injection and oral delivery of dsRNA Locusta migratoria. Pest Manag Sci. 2019 Jun;75(6):1707–1717.
  • Guan R-B, Li H-C, Fan Y-J, et al. A nuclease specific to lepidopteran insects suppresses RNAi. J Biol Chem. 2018 Apr;293(16):6011–6021.
  • Winston WM, Molodowitch C, Hunter CP. Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science. 2002 Mar;295:2456–2459.
  • McEwan DL, Weisman AS, Hunter CP. Uptake of extracellular double-stranded RNA by SID-2. Mol Cell. 2012 Sep;47(5):746–754.
  • Tomoyasu Y, Miller SC, Tomita S, et al. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol. 2008 Jan;9(1):R10.
  • Méndez-Acevedo KM, Valdes VJ, Asanov A, et al. A novel family of mammalian transmembrane proteins involved in cholesterol transport. Sci Rep. 2017 Aug;7(1):7450.
  • Vélez AM, Fishilevich E. The mysteries of insect RNAi: a focus on dsRNA uptake and transport. Pestic Biochem Physiol. 2018 Oct;151:25–31.
  • Xiao D, Gao X, Xu J, et al. Clathrin-dependent endocytosis plays a predominant role in cellular uptake of double-stranded RNA in the red flour beetle. Insect Biochem Mol Biol. 2015 May;60:68–77.
  • Dominska M, Dykxhoorn DM. Breaking down the barriers: siRNA delivery and endosome escape. J Cell Sci. 2010 Apr;123(8):1183–1189.
  • Yoon JS, Gurusamy D, Palli SR. Accumulation of dsRNA in endosomes contributes to inefficient RNA interference in the fall armyworm, Spodoptera frugiperda. Insect Biochem Mol Biol. 2017 Sep;90:53–60.
  • Waterhouse RM, Seppey M, Simão FA, et al. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol. 2018 Mar;35(3):543–548.
  • Altschul SF, Madden TL, Schäffer AA, et al. PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep;25(17):3389–3402.
  • Zhang M, Leong HW. Bidirectional best hit r-window gene clusters. BMC Bioinf. 2010 Jan;11(Suppl 1):S63.
  • Li Z, Tiley GP, Galuska SR, et al. Multiple large-scale gene and genome duplications during the evolution of hexapods. Proc Natl Acad Sci USA. 2018 May;115(18):4713–4718.
  • Dalquen DA, Dessimoz C. Bidirectional best hits miss many orthologs in duplication-rich clades such as plants and animals. Genome Biol Evol. 2013;5(10):1800–1806.
  • Ward N, Moreno-Hagelsieb G. Quickly finding orthologs as reciprocal best hits with BLAT, LAST, and UBLAST: how much do we miss? PLoS One. 2014 Jul;9(7):e101850.
  • Gertz EM, Yu Y-K, Agarwala R, et al. Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol. 2006 Dec;4(1):41.
  • Rombel IT, Sykes KF, Rayner S, et al. FINDER: a vector for high-throughput gene identification. Gene. 2002 Jan;282(1–2):33–41.
  • Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Inform. 2009 Oct;23:205–211.
  • Letunic I, Bork P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res. 2018 Jan;46(D1):D493–D496.
  • Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013 Apr;30(4):772–780.
  • Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009 Aug;25(15):1972–1973.
  • Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014 May;30(9):1312–1313.
  • Letunic I, Bork P. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019 Jul;47(W1):W256–W259.
  • Sydykova DK, Jack BR, Spielman SJ, et al. Measuring evolutionary rates of proteins in a structural context. [version 2; peer review: 4 approved]. F1000Res. 2017 Oct;6:1845.
  • Spielman SJ, Kosakovsky Pond SL. Relative evolutionary rate inference in HyPhy with LEISR. PeerJ. 2018 Feb;6:e4339.
  • Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008 Jul;25(7):1307–1320.
  • Huang Y, Niu B, Gao Y, et al. a web server for clustering and comparing biological sequences. Bioinformatics. 2010 Mar;26(5):680–682.
  • Milburn D, Laskowski RA, Thornton JM. Sequences annotated by structure: a tool to facilitate the use of structural information in sequence analysis. Protein Eng. 1998 Oct;11(10):855–859.
  • Wu S, Zhang Y. LOMETS: a local meta-threading-server for protein structure prediction. Nucleic Acids Res. 2007 May;35(10):3375–3382.
  • Jaroszewski L, Li Z, Cai X, et al. FFAS server: novel features and applications. Nucleic Acids Res. 2011 Jul;39(suppl):W38–44.
  • Kurowski MA, Bujnicki JM. GeneSilico protein structure prediction meta-server. Nucleic Acids Res. 2003 Jul;31(13):3305–3307.
  • Mirdita M, Steinegger M, Söding J. MMseqs2 desktop and local web server app for fast, interactive sequence searches. Bioinformatics. 2019 Aug;35(16):2856–2858.
  • Li Z, Natarajan P, Ye Y, et al. POSA: a user-driven, interactive multiple protein structure alignment server. Nucleic Acids Res. 2014 Jul;42(W1):W240–5.
  • Shatsky M, Nussinov R, Wolfson HJ. Optimization of multiple-sequence alignment based on multiple-structure alignment. Proteins. 2006 Jan;62(1):209–217.
  • Katoh K, Frith MC. Adding unaligned sequences into an existing alignment using MAFFT and LAST. Bioinformatics. 2012 Dec;28(23):3144–3146.
  • Okonechnikov K, Golosova O, Fursov M. UGENE team. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics. 2012 Apr;28(8):1166–1167.
  • Waterhouse A, Bertoni M, Bienert S, et al. MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018 Jul;46(W1):W296–W303.
  • Armougom F, Moretti S, Poirot O, et al. Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucleic Acids Res. 2006 Jul;34(Web Server):W604–8.
  • Bailey TL, Boden M, Buske FA, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009 Jul;37(Web Server):W202–8.
  • Wallot S, Leonardi G. Deriving inferential statistics from recurrence plots: a recurrence-based test of differences between sample distributions and its comparison to the two-sample Kolmogorov-Smirnov test. Chaos. 2018 Aug;28(8):085712.
  • Burley SK, Berman HM, Bhikadiya C, et al. RCSB Protein Data Bank: biological macromolecular structures enabling research and education in fundamental biology, biomedicine, biotechnology and energy. Nucleic Acids Res. 2019 Jan;47(D1):D464–D474.
  • Rubio M, Maestro JL, Piulachs M-D BX. Conserved association of Argonaute 1 and 2 proteins with miRNA and siRNA pathways throughout insect evolution, from cockroaches to flies. Biochim Biophys Acta Gene Regul Mech. 2018 Apr;1861(6):554–560.
  • Misof B, Liu S, Meusemann K, et al. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014 Nov;346(6210):763–767.
  • Wynant N, Santos D, Vanden Broeck J. The evolution of animal Argonautes: evidence for the absence of antiviral AGO Argonautes in vertebrates. Sci Rep. 2017 Aug;7(1):9230.
  • Cerutti H, Casas-Mollano JA. On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet. 2006 Aug;50(2):81–99.
  • Kwon SC, Nguyen TA, Choi Y-G, et al. Structure of human DROSHA. Cell. 2016 Jan;164(1–2):81–90.
  • Moran Y, Agron M, Praher D, et al. The evolutionary origin of plant and animal microRNAs. Nat Ecol Evol. 2017 Feb;1(3):27.
  • de Jong D, Eitel M, Jakob W, et al. Multiple dicer genes in the early-diverging metazoa. Mol Biol Evol. 2009 Jun;26(6):1333–1340.
  • Kosik KS. MicroRNAs and cellular phenotypy. Cell. 2010 Oct;143(1):21–26.
  • Mukherjee K, Campos H, Kolaczkowski B. Evolution of animal and plant dicers: early parallel duplications and recurrent adaptation of antiviral RNA binding in plants. Mol Biol Evol. 2013 Mar;30(3):627–641.
  • Murphy D, Dancis B, Brown JR. The evolution of core proteins involved in microRNA biogenesis. BMC Evol Biol. 2008 Mar;8(1):92.
  • St Johnston D, Brown NH, Gall JG, et al. A conserved double-stranded RNA-binding domain. Proc Natl Acad Sci USA. 1992 Nov;89(22):10979–10983.
  • Wickham L, Duchaîne T, Luo M, et al. Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol Cell Biol. 1999 Mar;19:2220–2230.
  • Dowling D, Pauli T, Donath A, et al. Phylogenetic origin and diversification of RNAi pathway genes in insects. Genome Biol Evol. 2016 Dec;8:3784–3793.
  • Senturia R, Faller M, Yin S, et al. Structure of the dimerization domain of DiGeorge critical region 8. Protein Sci. 2010 Jul;19(7):1354–1365.
  • Davis-Vogel C, Van Allen B, Van Hemert JL, et al. Identification and comparison of key RNA interference machinery from western corn rootworm, fall armyworm, and southern green stink bug. PLoS One. 2018 Sep;13(9):e0203160.
  • Sharma C, Mohanty D. Sequence- and structure-based analysis of proteins involved in miRNA biogenesis. J Biomol Struct Dyn. 2018;36(1):139–151.
  • Rozewicki J, Li S, Amada KM, et al. MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Res. 2019 Jul;47:W5–W10.
  • Burd CG, Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science. 1994 Jul;265(5172):615–621.
  • Cerutti L, Mian N, Bateman A. Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the Piwi domain. Trends Biochem Sci. 2000 Oct;25(10):481–482.
  • Hall TMT. Structure and function of argonaute proteins. Structure. 2005 Oct;13(10):1403–1408.
  • Kandasamy SK, Fukunaga R. Phosphate-binding pocket in Dicer 2 PAZ domain for high-fidelity siRNA production. Proc Natl Acad Sci USA. 2016 Dec;113(49):14031–14036.
  • Blaszczyk J, Tropea JE, Bubunenko M, et al. Crystallographic and modeling studies of RNase III suggest a mechanism for double-stranded RNA cleavage. Structure. 2001 Dec;9(12):1225–1236.
  • Conrad C, Ribonuclease RR. III: new sense from nuisance. Int J Biochem Cell Biol. 2002 Feb;34(2):116–129.
  • Blaszczyk J, Gan J, Tropea JE, et al. Non-catalytic assembly of ribonuclease III with double-stranded RNA. Structure. 2004 Mar;12(3):457–466.
  • Ye X, Paroo Z, Liu Q. Functional Anatomy of the Drosophila MicroRNA-generating Enzyme. J Biol Chem. 2007 Sep;282(39):28373–28378.
  • Cenik ES, Fukunaga R, Lu G, et al. Phosphate and R2D2 restrict the substrate specificity of Dicer-2, an ATP-driven ribonuclease. Mol Cell. 2011 Apr;42(2):172–184.
  • Trettin KD, Sinha NK, Eckert DM, et al. Loquacious-PD facilitates Drosophila Dicer-2 cleavage through interactions with the helicase domain and dsRNA. Proc Natl Acad Sci USA. 2017 Sep;114(38):E7939–E7948.
  • Sinha NK, Iwasa J, Shen PS, et al. Dicer uses distinct modules for recognizing dsRNA termini. Science. 2018 Jan;359(6373):329–334.
  • Kurzynska-Kokorniak A, Pokornowska M, Koralewska N, et al. Revealing a new activity of the human Dicer DUF283 domain in vitro. Sci Rep. 2016 Apr;6(1):23989.
  • Gan J, Tropea JE, Austin BP, et al. Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III. Cell. 2006 Jan;124(2):355–366.
  • Laraki G, Clerzius G, Daher A, et al. Interactions between the double-stranded RNA-binding proteins TRBP and PACT define the Medipal domain that mediates protein-protein interactions. RNA Biol. 2008 Jun;5(2):92–103.
  • Yang SW, Chen H-Y, Yang J, et al. Structure of Arabidopsis Hyponastic Leaves 1 and its molecular implications for miRNA processing. Structure. 2010 May;18(5):594–605.
  • Wilson RC, Tambe A, Kidwell MA, et al. Dicer-TRBP complex formation ensures accurate mammalian microRNA biogenesis. Mol Cell. 2015 Feb;57(3):397–407.
  • Ryter JM, Schultz SC. Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA-binding domain complexed with dsRNA. Embo J. 1998 Dec;17(24):7505–7513.
  • Vuković L, Koh HR, Myong S, et al. Substrate recognition and specificity of double-stranded RNA binding proteins. Biochemistry. 2014 Jun;53(21):3457–3466.
  • Dias R, Manny A, Kolaczkowski O, et al. Convergence of domain architecture, structure, and ligand affinity in animal and plant RNA-binding proteins. Mol Biol Evol. 2017 Jun;34(6):1429–1444.
  • Kurihara Y, Takashi Y, Watanabe Y. The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA. 2006 Feb;12(2):206–212.
  • Liu Z, Wang J, Cheng H, et al. Cryo-EM structure of human dicer and its complexes with a pre-miRNA substrate. Cell. 2018 May;173(5):1191–1203.e12.
  • Zhang X, Li P, Lin J, et al. The insertion in the double-stranded RNA binding domain of human Drosha is important for its function. Biochim Biophys Acta Gene Regul Mech. 2017 Dec;1860(12):1179–1188.
  • Tian Y, Simanshu DK, Ma J-B, et al. A phosphate-binding pocket within the platform-PAZ-connector helix cassette of human Dicer. Mol Cell. 2014 Feb;53(4):606–616.
  • Wilson KA, Holland DJ, Wetmore SD. Topology of RNA-protein nucleobase-amino acid π-π interactions and comparison to analogous DNA-protein π-π contacts. RNA. 2016 May;22:696–708.
  • Fukunaga R, Colpan C, Han BW, et al. Inorganic phosphate blocks binding of pre-miRNA to Dicer 2 via its PAZ domain. Embo J. 2014 Feb;33(4):371–384.
  • Park J-E, Heo I, Tian Y, et al. Dicer recognizes the 5ʹ end of RNA for efficient and accurate processing. Nature. 2011 Jul;475(7355):201–205.
  • Jia H, Kolaczkowski O, Rolland J, et al. Increased affinity for RNA targets evolved early in animal and plant Dicer lineages through different structural mechanisms. Mol Biol Evol. 2017 Dec;34(12):3047–3063.
  • Zhu J-K. Reconstituting plant miRNA biogenesis. Proc Natl Acad Sci USA. 2008 Jul;105(29):9851–9852.
  • Terenius O, Papanicolaou A, Garbutt JS, et al. RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol. 2011 Feb;57(2):231–245.
  • Lau P-W, Guiley KZ, De N, et al. The molecular architecture of human Dicer. Nat Struct Mol Biol. 2012 Mar;19(4):436–440.
  • MacRae IJ, Doudna JA. An unusual case of pseudo-merohedral twinning in orthorhombic crystals of Dicer. Acta Crystallogr Sect D, Biol Crystallogr. 2007 Sep;63:993–999.
  • Sasaki T, Shimizu N. Evolutionary conservation of a unique amino acid sequence in human DICER protein essential for binding to Argonaute family proteins. Gene. 2007 Jul;396(2):312–320.
  • Maillard PV, van der Veen AG, Poirier EZ, et al. Slicing and dicing viruses: antiviral RNA interference in mammals. Embo J. 2019 Apr;38(8):e100941.
  • MacRae IJ, Zhou K, Doudna JA. Structural determinants of RNA recognition and cleavage by Dicer. Nat Struct Mol Biol. 2007 Oct;14(10):934–940.
  • Oliver D, Sheehan B, South H, et al. The chromosomal association/dissociation of the chromatin insulator protein Cp190 of Drosophila melanogaster is mediated by the BTB/POZ domain and two acidic regions. BMC Cell Biol. 2010 Dec;11(1):101.
  • Kumar A, Lualdi M, Loncarek J, et al. Loss of function of mouse Pax-Interacting Protein 1-associated glutamate rich protein 1a (Pagr1a) leads to reduced Bmp2 expression and defects in chorion and amnion development. Dev Dyn. 2014 Jul;243(7):937–947.
  • Hsu TI, Lin SC, Lu PS, et al. MMP7-mediated cleavage of nucleolin at Asp255 induces MMP9 expression to promote tumor malignancy. Oncogene. 2015 Feb;34(7):826–837.
  • Putnam CD, Tainer JA. Protein mimicry of DNA and pathway regulation. DNA Repair (Amst). 2005 Dec;4(12):1410–1420.
  • Wang H-C, Ho C-H, Hsu K-C, et al. DNA mimic proteins: functions, structures, and bioinformatic analysis. Biochemistry. 2014 May;53(18):2865–2874.
  • Kinoshita S, Katsumi E, Yamamoto H, et al. Molecular and functional analyses of aspolin, a fish-specific protein extremely rich in aspartic acid. Mar Biotechnol. 2011 Jun;13(3):517–526.
  • Scartezzini P, Egeo A, Colella S, et al. Cloning a new human gene from chromosome 21q22.3 encoding a glutamic acid-rich protein expressed in heart and skeletal muscle. Hum Genet. 1997 Mar;99:387–392.
  • Kumar P, Bansal M. Structural and functional analyses of PolyProline-II helices in globular proteins. J Struct Biol. 2016 Sep;196(3):414–425.
  • Adzhubei AA, Sternberg MJE, Makarov AA. Polyproline-II helix in proteins: structure and function. J Mol Biol. 2013 Jun;425(12):2100–2132.
  • Morgan AA, Rubenstein E. Proline: the distribution, frequency, positioning, and common functional roles of proline and polyproline sequences in the human proteome. PLoS One. 2013 Jan;8(1):e53785.
  • Jankowsky E, Fairman-Williams ME. Chapter 1. an introduction to RNA helicases: superfamilies, families, and major themes. In: Jankowsky E, editor. RNA Helicases. Cambridge: Royal Society of Chemistry; 2010. p. 1–31.
  • Mastrangelo E, Bolognesi M, Milani M. Flaviviral helicase: insights into the mechanism of action of a motor protein. Biochem Biophys Res Commun. 2012 Jan;417(1):84–87.
  • Du Pont KE, Davidson RB, McCullagh M, et al. Motif V regulates energy transduction between the flavivirus NS3 ATPase and RNA-binding cleft. J Biol Chem. 2020 Feb;295(6):1551–1564.
  • Caruthers JM, McKay DB. Helicase structure and mechanism. Curr Opin Struct Biol. 2002 Feb;12(1):123–133.
  • Papanikou E, Karamanou S, Baud C, et al. Helicase Motif III in SecA is essential for coupling preprotein binding to translocation ATPase. EMBO Rep. 2004 Aug;5(8):807–811.
  • Deddouche S, Matt N, Budd A, et al. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nat Immunol. 2008 Dec;9:1425–1432.
  • Swevers L, Vanden Broeck J, Smagghe G. The possible impact of persistent virus infection on the function of the RNAi machinery in insects: a hypothesis. Front Physiol. 2013 Nov;4:319.
  • Dias NP, Cagliari D, Dos Santos EA, et al. Insecticidal gene silencing by RNAi in the neotropical region. Neotrop Entomol. 2020 Feb;49(1):1–11.
  • Cooper AM, Silver K, Zhang J, et al. Molecular mechanisms influencing efficiency of RNA interference in insects. Pest Manag Sci. 2019 Jan;75(1):18–28.
  • Claycomb JM. Ancient endo-siRNA pathways reveal new tricks. Curr Biol. 2014 Aug;24(15):R703–15.
  • Trobaugh DW, Klimstra WB. MicroRNA regulation of RNA virus replication and pathogenesis. Trends Mol Med. 2017;23(1):80–93.
  • Shapiro JS. Processing of virus-derived cytoplasmic primary-microRNAs. Wiley Interdiscip Rev RNA. 2013 Aug;4(4):463–471.
  • Masliah G, Barraud P, Allain FH-T. RNA recognition by double-stranded RNA binding domains: a matter of shape and sequence. Cell Mol Life Sci. 2013 Jun;70:1875–1895.
  • Song -J-J, Liu J, Tolia NH, et al. The crystal structure of the Argonaute 2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat Struct Biol. 2003 Dec;10:1026–1032.
  • Drezen J-M, Josse T, Bézier A, et al. Impact of lateral transfers on the genomes of Lepidoptera. Genes (Basel). 2017 Nov;8(11):315.
  • Vignuzzi M, López CB. Defective viral genomes are key drivers of the virus-host interaction. Nat Microbiol. 2019 Jun;4:1075–1087.
  • Guo Z, Li Y, Ding S-W, et al. A-based antimicrobial immunity. Nat Rev Immunol. 2019;19(1):31–44.
  • Kolliopoulou A, Santos D, Taning CNT, et al. PIWI pathway against viruses in insects. Wiley Interdiscip Rev RNA. 2019 Jun;10(6):e1555.
  • Ter Horst AM, Nigg JC, Dekker FM, et al. Endogenous viral elements are widespread in arthropod genomes and commonly give rise to PIWI-interacting RNAs. J Virol. 2019 Mar;93(6):e02124-18.
  • Cui J, Holmes EC. Endogenous RNA viruses of plants in insect genomes. Virology. 2012 Jun;427(2):77–79.
  • Powell JA. Lepidoptera: moths, butterflies. In: Resh V, Cardé R, editors. Encyclopedia of Insects. 2nd ed ed. USA: Elsevier; 2009. p. 559–587.
  • Zografidis A, Van Nieuwerburgh F, Kolliopoulou A, et al. Viral small-RNA analysis of Bombyx mori larval midgut during persistent and pathogenic cytoplasmic polyhedrosis virus infection. J Virol. 2015 Nov;89(22):11473–11486.
  • Lavialle C, Cornelis G, Dupressoir A, et al. Paleovirology of ‘ syncytins’, retroviral env genes exapted for a role in placentation. Philos Trans R Soc Lond B, Biol Sci. 2013 Sep;368(1626):20120507.
  • Ryabov EV. Invertebrate RNA virus diversity from a taxonomic point of view. J Invertebr Pathol. 2017;147:37–50.
  • Mongelli V, Saleh M-C. Bugs are not to be silenced: small RNA pathways and antiviral responses in insects. Annu Rev Virol. 2016 Sep;3(1):573–589.
  • Berry B, Deddouche S, Kirschner D, et al. Viral suppressors of RNA silencing hinder exogenous and endogenous small RNA pathways in Drosophila. PLoS One. 2009 Jun;4(6):e5866.
  • Yoon J-S, Mogilicherla K, Gurusamy D, et al. Double-stranded RNA binding protein, Staufen, is required for the initiation of RNAi in coleopteran insects. Proc Natl Acad Sci USA. 2018 Aug;115(33):8334–8339.
  • Kingsolver MB, Huang Z, Hardy RW. Insect antiviral innate immunity: pathways, effectors, and connections. J Mol Biol. 2013 Dec;425(24):4921–4936.
  • Brown S, Hu N, Hombría JC. Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Curr Biol. 2001 Oct;11(21):1700–1705.
  • Gottar M, Gobert V, Michel T, et al. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature. 2002 Apr;416(6881):640–644.
  • Paradkar PN, Duchemin J-B, Voysey R, et al. Dicer-2-dependent activation of Culex Vago occurs via the TRAF-Rel2 signaling pathway. PLoS Negl Trop Dis. 2014 Apr;8(4):e2823.
  • Cheng G, Liu Y, Wang P, et al. Mosquito defense strategies against viral infection. Trends Parasitol. 2016 Mar;32(3):177–186.
  • Paradkar PN, Trinidad L, Voysey R, et al. Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway. Proc Natl Acad Sci USA. 2012 Nov;109(46):18915–18920.
  • Sim S, Jupatanakul N, Dimopoulos G. Mosquito immunity against arboviruses. Viruses. 2014 Nov;6(11):4479–4504.
  • Poirier EZ, Goic B, Tomé-Poderti L, et al. Dicer-2-dependent generation of viral DNA from defective genomes of RNA viruses modulates antiviral immunity in insects. Cell Host Microbe. 2018 Mar;23(3):353–365.e8.
  • Santos D, Wynant N, Van den Brande S, et al. Insights into RNAi-based antiviral immunity in Lepidoptera: acute and persistent infections in Bombyx mori and Trichoplusia ni cell lines. Sci Rep. 2018 Feb;8(1):2423.
  • Spellberg MJ, Marr MT. FOXO regulates RNA interference in Drosophila and protects from RNA virus infection. Proc Natl Acad Sci USA. 2015 Nov;112(47):14587–14592.
  • Ahlers LRH, Trammell CE, Carrell GF, et al. Insulin potentiates JAK/STAT signaling to broadly inhibit flavivirus replication in insect vectors. Cell Rep. 2019 Nov;29(7):1946–1960.e5.
  • Guan R, Hu S, Li H, et al. in vivo dsRNA cleavage has sequence preference in insects. Front Physiol. 2018 Dec;9:1768.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.