Global Analysis of Small Non-Coding RNA Populations across Tissues in the Malaria Vector, Anopheles gambiae
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals and Tissues
2.2. Quantitative PCR
2.3. Annotation of Small ncRNA Groups
2.4. Other Data Resource
2.5. Data Availability
3. Results
3.1. Diversity of Small ncRNA Groups Across Mosquito Tissues
3.2. miRNA Annotation Update
3.3. tRNA- and rRNA-Fragment Annotation
3.4. TE-piRNA Annotation
3.5. mRNA-Derived Small RNA Annotation
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- World Health Organization. World Malaria Report 2018; World Health Organization: Geneva, Switzerland, 2018. [Google Scholar]
- Aalto, A.P.; Pasquinelli, A.E. Small non-coding RNAs mount a silent revolution in gene expression. Curr. Opin. Cell. Biol. 2012, 24, 333–340. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirakata, S.; Siomi, M.C. piRNA biogenesis in the germline: From transcription of piRNA genomic sources to piRNA maturation. Biochim. Biophys. Acta 2016, 1859, 82–92. [Google Scholar] [PubMed]
- Saito, K.; Siomi, M.C. Small RNA-mediated quiescence of transposable elements in animals. Dev. Cell 2010, 19, 687–697. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aravin, A.A.; Hannon, G.J.; Brennecke, J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 2007, 318, 761–764. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Han, B.W.; Zamore, P.D. piRNAs. Curr. Biol. 2014, 24, R730–R733. [Google Scholar] [CrossRef] [Green Version]
- Senti, K.A.; Brennecke, J. The piRNA pathway: A fly’s perspective on the guardian of the genome. Trends Genet. 2010, 26, 499–509. [Google Scholar] [CrossRef] [Green Version]
- Lucas, K.; Raikhel, A.S. Insect microRNAs: Biogenesis, expression profiling and biological functions. Insect Biochem. Mol. Biol. 2013, 43, 24–38. [Google Scholar] [CrossRef] [Green Version]
- Lucas, K.J.; Myles, K.M.; Raikhel, A.S. Small RNAs: A new frontier in mosquito biology. Trends Parasitol. 2013, 29, 295–303. [Google Scholar] [CrossRef] [Green Version]
- Lampe, L.; Levashina, E.A. The role of microRNAs in Anopheles biology-an emerging research field. Parasite Immunol. 2017, 39, e12405. [Google Scholar] [CrossRef]
- Bryant, W.B.; Mills, M.K.; Olson, B.J.S.C.; Michel, K. Small RNA-Seq Analysis Reveals miRNA Expression Dynamics Across Tissues in the Malaria Vector, Anopheles gambiae. G3 (Bethesda) 2019, 9, 1507–1517. [Google Scholar]
- Bryant, B.; Macdonald, W.; Raikhel, A.S. microRNA miR-275 is indispensable for blood digestion and egg development in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. USA 2010, 107, 22391–22398. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schmittgen, T.D.; Livak, K.J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 2008, 3, 1101–1108. [Google Scholar] [CrossRef] [PubMed]
- Giraldo-Calderon, G.I.; Emrich, S.J.; MacCallum, R.M.; Maslen, G.; Dialynas, E.; Topalis, P.; Ho, N.; Gesing, S.; Consortium, V.; Madey, G.; et al. VectorBase: An updated bioinformatics resource for invertebrate vectors and other organisms related with human diseases. Nucleic Acids Res. 2015, 43, D707–D713. [Google Scholar] [CrossRef] [PubMed]
- Fu, X.; Dimopoulos, G.; Zhu, J. Association of microRNAs with Argonaute proteins in the malaria mosquito Anopheles gambiae after blood ingestion. Sci. Rep. 2017, 7, 6493. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reynolds, J.A.; Peyton, J.T.; Denlinger, D.L. Changes in microRNA abundance may regulate diapause in the flesh fly, Sarcophaga bullata. Insect Biochem. Mol. Biol. 2017, 84, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Su, J.; Li, C.; Zhang, Y.; Yan, T.; Zhu, X.; Zhao, M.; Xing, D.; De Dong, Y.-; Guo, X.-X.; Zhao, T. Identification of microRNAs expressed in the midgut of Aedes albopictus during dengue infection. Parasit. Vectors 2017, 10, 63. [Google Scholar] [CrossRef] [Green Version]
- Jain, S.; Rana, V.; Shrinet, J.; Sharma, A.; Tridibes, A.; Sunil, S.; Bhatnagar, R.K. Blood feeding and Plasmodium infection alters the miRNome of Anopheles stephensi. PLoS ONE 2014, 9, e98402. [Google Scholar]
- Dou, S.; Wang, Y.; Lu, J. Metazoan tsRNAs: Biogenesis, Evolution and Regulatory Functions. Noncoding RNA 2019, 5, 18. [Google Scholar] [CrossRef] [Green Version]
- Lambert, M.; Benmoussa, A.; Provost, P. Small Non-Coding RNAs derived from eukaryotic ribosomal RNA. Noncoding RNA 2019, 5, 16. [Google Scholar] [CrossRef] [Green Version]
- Babski, J.; Maier, L.-K.; Heyer, R.; Jaschinski, K.; Prasse, D.; Jäger, M.; Randau, L.; A Schmitz, R.; Marchfelder, A.; Soppa, J. Small regulatory RNAs in Archaea. RNA Biol. 2014, 11, 484–493. [Google Scholar] [CrossRef] [Green Version]
- Eng, M.W.; Clemons, A.; Hill, C.; Engel, R.; Severson, D.W.; Behura, S.K. Multifaceted functional implications of an endogenously expressed tRNA fragment in the vector mosquito Aedes aegypti. PLoS Negl. Trop. Dis. 2018, 12, e0006186. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arca, B.; Colantoni, A.; Fiorillo, C.; Severini, F.; Benes, V.; Di Luca, M.; Calogero, R.A.; Lombardo, F. MicroRNAs from saliva of anopheline mosquitoes mimic human endogenous miRNAs and may contribute to vector-host-pathogen interactions. Sci. Rep. 2019, 9, 2955. [Google Scholar] [CrossRef] [PubMed]
- Castellano, L.; Rizzi, E.; Krell, J.; Di Cristina, M.; Galizi, R.; Mori, A.; Tam, J.; De Bellis, G.; Stebbing, J.; Crisanti, A.; et al. The germline of the malaria mosquito produces abundant miRNAs, endo-siRNAs, piRNAs and 29-nt small RNAs. BMC Genom. 2015, 16, 100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Biryukova, I.; Ye, T. Endogenous siRNAs and piRNAs derived from transposable elements and genes in the malaria vector mosquito Anopheles gambiae. BMC Genom. 2015, 16, 278. [Google Scholar] [CrossRef] [Green Version]
- George, P.; Jensen, S.; Pogorelcnik, R.; Lee, J.; Xing, Y.; Brasset, E.; Vaury, C.; Sharakhov, I.V. Increased production of piRNAs from euchromatic clusters and genes in Anopheles gambiae compared with Drosophila melanogaster. Epigenetics Chromatin 2015, 8, 50. [Google Scholar] [CrossRef] [Green Version]
- Serrato-Capuchina, A.; Matute, D.R. The Role of Transposable Elements in Speciation. Genes 2018, 9, 254. [Google Scholar] [CrossRef] [Green Version]
- Lau, N.C.; Robine, N.; Martín, R.; Chung, W.-J.; Niki, Y.; Berezikov, E.; Lai, E.C. Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. Genome Res. 2009, 19, 1776–1785. [Google Scholar] [CrossRef] [Green Version]
- Malone, C.D.; Brennecke, J.; Dus, M.; Stark, A.; McCombie, W.R.; Sachidanandam, R.; Hannon, G.J. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 2009, 137, 522–535. [Google Scholar] [CrossRef] [Green Version]
- Li, C.; Vagin, V.V.; Lee, S.; Xu, J.; Ma, S.; Xi, H.; Seitz, H.; Horwich, M.D.; Syrzycka, M.; Honda, B.M.; et al. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 2009, 137, 509–521. [Google Scholar] [CrossRef] [Green Version]
- Brennecke, J.; Aravin, A.A.; Stark, A.; Dus, M.; Kellis, M.; Sachidanandam, R.; Hannon, G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128, 1089–1103. [Google Scholar] [CrossRef] [Green Version]
- Wen, J.; Mohammed, J.; Bortolamiol-Becet, D.; Tsai, H.; Robine, N.; Westholm, J.; Ladewig, E.; Dai, Q.; Okamura, K.; Flynt, A.S.; et al. Diversity of miRNAs, siRNAs, and piRNAs across 25 Drosophila cell lines. Genome Res. 2014, 24, 1236–1250. [Google Scholar] [CrossRef] [Green Version]
- Rouget, C.; Papin, C.; Boureux, A.; Meunier, A.-C.; Franco, B.; Robine, N.; Lai, E.C.; Pélisson, A.; Simonelig, M. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 2010, 467, 1128–1132. [Google Scholar] [CrossRef] [Green Version]
- Klein, J.D.; Qu, C.; Yang, X.; Fan, Y.; Tang, C.; Peng, J.C. c-Fos Repression by Piwi regulates Drosophila ovarian germline formation and tissue morphogenesis. PLoS Genet. 2016, 12, e1006281. [Google Scholar] [CrossRef] [Green Version]
- Robine, N.; Lau, N.C.; Balla, S.; Jin, Z.; Okamura, K.; Kuramochi-Miyagawa, S.; Blower, M.D.; Lai, E.C. A broadly conserved pathway generates 3’UTR-directed primary piRNAs. Curr. Biol. 2009, 19, 2066–2076. [Google Scholar] [CrossRef] [Green Version]
- Saito, K.; Inagaki, S.; Mituyama, T.; Kawamura, Y.; Ono, Y.; Sakota, E.; Kotani, H.; Asai, K.; Siomi, H.; Siomi, M.C. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 2009, 461, 1296–1299. [Google Scholar] [CrossRef]
- Hirakata, S.; Ishizu, H.; Fujita, A.; Tomoe, Y.; Siomi, M.C. Requirements for multivalent Yb body assembly in transposon silencing in Drosophila. EMBO Rep. 2019, 20, e47708. [Google Scholar] [CrossRef]
- Girardi, E.; Miesen, P.; Pennings, B.; Frangeul, L.; Saleh, M.C.; Van Rij, R.P. Histone-derived piRNA biogenesis depends on the ping-pong partners Piwi5 and Ago3 in Aedes aegypti. Nucleic Acids Res. 2017, 45, 4881–4892. [Google Scholar]
- Adelman, Z.N.; Anderson, M.A.E.; Liu, M.; Zhang, L.; Myles, K.M. Sindbis virus induces the production of a novel class of endogenous siRNAs in Aedes aegypti mosquitoes. Insect Mol. Biol. 2012, 21, 357–368. [Google Scholar] [CrossRef] [Green Version]
- Liu, S.; Lucas, K.J.; Roy, S.; Ha, J.; Raikhel, A.S. Mosquito-specific microRNA-1174 targets serine hydroxymethyltransferase to control key functions in the gut. Proc. Natl. Acad. Sci. USA 2014, 111, 14460–14465. [Google Scholar] [CrossRef] [Green Version]
- Lampe, L.; Levashina, E.A. MicroRNA tissue atlas of the malaria mosquito Anopheles gambiae. G3 (Bethesda) 2018, 8, 185–193. [Google Scholar] [CrossRef] [Green Version]
- Mead, E.A.; Tu, Z. Cloning, characterization, and expression of microRNAs from the Asian malaria mosquito, Anopheles stephensi. BMC Genom. 2008, 9, 244. [Google Scholar] [CrossRef] [Green Version]
- Jain, S.; Rana, V.; Adak, T.; Sunil, S.; Bhatnagar, R.K. Dynamic expression of miRNAs across immature and adult stages of the malaria mosquito Anopheles stephensi. Parasit. Vectors 2015, 8, 179. [Google Scholar] [CrossRef] [Green Version]
- Ruby, J.G.; Stark, A.; Johnston, W.K.; Kellis, M.; Bartel, B.; Lai, E.C. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res. 2007, 17, 1850–1864. [Google Scholar] [CrossRef] [Green Version]
- Goodwin, P.R.; Meng, A.; Moore, J.; Hobin, M.; Fulga, T.A.; Van Vactor, D.; Griffith, L.C. MicroRNAs Regulate Sleep and Sleep Homeostasis in Drosophila. Cell Rep. 2018, 23, 3776–3786. [Google Scholar] [CrossRef]
- Monsanto-Hearne, V.; Tham, A.L.; Wong, Z.S.; Asgari, S.; Johnson, K. Drosophila miR-956 suppression modulates Ectoderm-expressed 4 and inhibits viral replication. Virology 2017, 502, 20–27. [Google Scholar] [CrossRef]
- Curtis, C.F.; Graves, P.M. Methods for replacement of malaria vector populations. J. Trop. Med. Hyg. 1988, 91, 43–48. [Google Scholar]
- Pircher, A.; Bąkowska-Żywicka, K.; Schneider, L.; Żywicki, M.; Polacek, N. An mRNA-derived noncoding RNA targets and regulates the ribosome. Mol. Cell 2014, 54, 147–155. [Google Scholar] [CrossRef] [Green Version]
Tissue | miRNA | tRNA/rRNA | TE-piRNAs | mRNA-Derived | Unannotated | Unmapped |
---|---|---|---|---|---|---|
Fat Body-Ab | 13.43 | 49.89 | 2.21 | 15.56 | 18.63 | 0.29 |
Midgut | 22.62 | 52.80 | 0.94 | 11.45 | 13.09 | 1.35 |
Ovary | 2.07 | 6.24 | 34.72 | 6.47 | 54.33 | 0.26 |
Remainder | 3.71 | 77.24 | 0.76 | 9.07 | 10.38 | 0.45 |
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Bryant, W.B.; Ray, S.; Mills, M.K. Global Analysis of Small Non-Coding RNA Populations across Tissues in the Malaria Vector, Anopheles gambiae. Insects 2020, 11, 406. https://doi.org/10.3390/insects11070406
Bryant WB, Ray S, Mills MK. Global Analysis of Small Non-Coding RNA Populations across Tissues in the Malaria Vector, Anopheles gambiae. Insects. 2020; 11(7):406. https://doi.org/10.3390/insects11070406
Chicago/Turabian StyleBryant, William Bart, Savanna Ray, and Mary Katherine Mills. 2020. "Global Analysis of Small Non-Coding RNA Populations across Tissues in the Malaria Vector, Anopheles gambiae" Insects 11, no. 7: 406. https://doi.org/10.3390/insects11070406