Hormonal regulation of microRNA expression dynamics in the gut of the yellow fever mosquito Aedes aegypti

References

• Barrett ADT, Higgs S. Yellow fever: a disease that has yet to be conquered. Annu Rev Entomol. 2007;52:209–229.
   PubMed Web of Science ®Google Scholar
• McFee RB. Selected mosquito borne illnesses - dengue. Disease-a-month. 2018;64:246–274.
   PubMedGoogle Scholar
• Tsetsarkin KA, Chen RB, Weaver SC. Interspecies transmission and chikungunya virus emergence. Curr Opin Virol. 2016;16:143–150.
   PubMed Web of Science ®Google Scholar
• Weaver SC, Costa F, Garcia-Blanco MA, et al. Zika virus: history, emergence, biology, and prospects for control. Antiviral Res. 2016;130:69–80.
   PubMed Web of Science ®Google Scholar
• Shaw WR, Catteruccia F. Vector biology meets disease control: using basic research to fight vector-borne diseases. Nat Microbiol. 2019;4:20–34.
   PubMed Web of Science ®Google Scholar
• Zou Z, Saha TT, Roy S, et al. Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression. Proc Natl Acad Sci U S A. 2013;110:E2173–2181.
   PubMed Web of Science ®Google Scholar
• Shapiro AB, Wheelock GD, Hagedorn HH, et al. Juvenile-hormone and juvenile-hormone esterase in adult females of the mosquito aedes-aegypti. J Insect Physiol. 1986;32:867–877.
   Web of Science ®Google Scholar
• Hagedorn HH, Shapiro JP, Hanaoka K. Ovarian ecdysone secretion is controlled by a brain hormone in an adult mosquito. Nature. 1979;282:92–94.
   PubMed Web of Science ®Google Scholar
• Roy S, Saha TT, Johnson L, et al. Regulation of gene expression patterns in mosquito reproduction. PLoS Genet. 2015;11:e1005450.
   PubMed Web of Science ®Google Scholar
• Attardo GM, Hansen IA, Raikhel AS. Nutritional regulation of vitellogenesis in mosquitoes: implications for anautogeny. Insect Biochem Mol Biol. 2005;35:661–675.
   PubMed Web of Science ®Google Scholar
• Salazar MI, Richardson JH, Sanchez-Vargas I, et al. Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes. BMC Microbiol. 2007;7:9.
   PubMed Web of Science ®Google Scholar
• Noriega FG, Wells MA. A molecular view of trypsin synthesis in the midgut of Aedes aegypti. J Insect Physiol. 1999;45:613–620.
   PubMed Web of Science ®Google Scholar
• Petchampai N, Scaraffia PY. Nitrogen metabolism in mosquitoes new insights into the nitrogen metabolism in blood-fed mosquitoes. Prog Mosq Res. 2016;51:363–391.
   Google Scholar
• Bartholomay LC, Michel K. Mosquito Immunobiology: the Intersection of Vector Health and Vector Competence. Annu Rev Entomol. 2018;63:145–167.
   PubMed Web of Science ®Google Scholar
• Skvortsova K, Iovino N, Bogdanovic O. Functions and mechanisms of epigenetic inheritance in animals. Nat Rev Mol Cell Biol. 2018;19:774–790.
   PubMed Web of Science ®Google Scholar
• Yu Y, Zhang YC, Chen XM, et al. Plant noncoding RNAs: hidden players in development and stress responses. Annu Rev Cell Dev Biol. 2019;35:407–431.
   PubMed Web of Science ®Google Scholar
• Bryant B, Macdonald W, Raikhel AS. microRNA miR-275 is indispensable for blood digestion and egg development in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A. 2010;107:22391–22398.
   PubMed Web of Science ®Google Scholar
• Liu S, Lucas KJ, Roy S, et al. Mosquito-specific microRNA-1174 targets serine hydroxymethyltransferase to control key functions in the gut. Proc Natl Acad Sci U S A. 2014;111:14460–14465.
   PubMed Web of Science ®Google Scholar
• Lucas KJ, Zhao B, Roy S, et al. Mosquito-specific microRNA-1890 targets the juvenile hormone-regulated serine protease JHA15 in the female mosquito gut. RNA Biol. 2015;12:1383–1390.
   PubMed Web of Science ®Google Scholar
• Zhao B, Lucas KJ, Saha TT, et al. MicroRNA-275 targets sarco/endoplasmic reticulum Ca2+ adenosine triphosphatase (SERCA) to control key functions in the mosquito gut. PLoS Genet. 2017;13:e1006943.
   PubMed Web of Science ®Google Scholar
• Samuel GH, Adelman ZN, Myles KM. Antiviral immunity and virus-mediated antagonism in disease vector mosquitoes. Trends Microbiol. 2018;26:447–461.
   PubMed Web of Science ®Google Scholar
• Feng X, Zhou S, Wang J, et al. microRNA profiles and functions in mosquitoes. PLoS Negl Trop Dis. 2018;12:e0006463.
   PubMed Web of Science ®Google Scholar
• Saldana MA, Etebari K, Hart CE, et al. Zika virus alters the microRNA expression profile and elicits an RNAi response in Aedes aegypti mosquitoes. PLoS Negl Trop Dis. 2017;11:e0005760.
   PubMed Web of Science ®Google Scholar
• Hays AR, Raikhel AS. A novel protein produced by the vitellogenic fat body and accumulated in mosquito oocytes. Roux’s Arch Dev Biol. 1990;199:114–121.
   Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–359.
   PubMed Web of Science ®Google Scholar
• Kent WJ. BLAT–the BLAST-like alignment tool. Genome Res. 2002;12:656–664.
   PubMed Web of Science ®Google Scholar
• Friedlander MR, Mackowiak SD, Li N, et al. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res. 2012;40:37–52.
   PubMed Web of Science ®Google Scholar
• Lawrence M, Huber W, Pages H, et al. Software for computing and annotating genomic ranges. PLoS Comput Biol. 2013;9:e1003118.
   PubMed Web of Science ®Google Scholar
• Velu CS, Grimes HL. Utilizing antagomiR (antisense microRNA) to knock down microRNA in murine bone marrow cells. Methods Mol Biol. 2012;928:185–195.
   PubMedGoogle Scholar
• Zhang X, Aksoy E, Girke T, et al. Transcriptome-wide microRNA and target dynamics in the fat body during the gonadotrophic cycle of Aedes aegypti. Proc Natl Acad Sci U S A. 2017;114:E1895–E1903.
   PubMed Web of Science ®Google Scholar
• Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3:1101–1108.
   PubMed Web of Science ®Google Scholar
• Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014;42:D68–D73.
   PubMed Web of Science ®Google Scholar
• Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
   PubMed Web of Science ®Google Scholar
• Biryukova I, Ye T, Levashina E. Transcriptome-wide analysis of microRNA expression in the malaria mosquito Anopheles gambiae. BMC Genomics. 2014;15:557.
   PubMed Web of Science ®Google Scholar
• Gu J, Hu W, Wu J, et al. miRNA genes of an invasive vector mosquito, Aedes albopictus. PloS One. 2013;8:e67638.
   PubMed Web of Science ®Google Scholar
• Hu W, Criscione F, Liang S, et al. MicroRNAs of two medically important mosquito species: aedes aegypti and Anopheles stephensi. Insect Mol Biol. 2015;24:240–252.
   PubMed Web of Science ®Google Scholar
• Skalsky RL, Vanlandingham DL, Scholle F, et al. Identification of microRNAs expressed in two mosquito vectors, Aedes albopictus and Culex quinquefasciatus. BMC Genomics. 2010;11:119.
   PubMed Web of Science ®Google Scholar
• Lampe L, Levashina EA. MicroRNA tissue atlas of the malaria mosquito anopheles gambiae. G3. 2018;8:185–193.
   Web of Science ®Google Scholar
• Zhou Y, Liu Y, Yan H, et al. miR-281, an abundant midgut-specific miRNA of the vector mosquito Aedes albopictus enhances dengue virus replication. Parasit Vectors. 2014;7:488.
   PubMed Web of Science ®Google Scholar
• Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140.
   PubMed Web of Science ®Google Scholar
• Li S, Mead EA, Liang S, et al. Direct sequencing and expression analysis of a large number of miRNAs in Aedes aegypti and a multi-species survey of novel mosquito miRNAs. BMC Genomics. 2009;10:581.
   PubMed Web of Science ®Google Scholar
• Akbari OS, Antoshechkin I, Amrhein H, et al. The developmental transcriptome of the mosquito Aedes aegypti, an invasive species and major arbovirus vector. G3. 2013;3:1493–1509.
   Web of Science ®Google Scholar
• Nouzova M, Etebari K, Noriega FG, et al. A comparative analysis of corpora allata-corpora cardiaca microRNA repertoires revealed significant changes during mosquito metamorphosis. Insect Biochem Mol Biol. 2018;96:10–18.
   PubMed Web of Science ®Google Scholar
• Shah AP, Patel PT, Patel BP, et al. Evaluation of microtitre plate-based Haemoglobin estimation. Int J Lab Hematol. 2018;40:196–200.
   PubMed Web of Science ®Google Scholar
• Ling L, Kokoza VA, Zhang C, et al. MicroRNA-277 targets insulin-like peptides 7 and 8 to control lipid metabolism and reproduction in Aedes aegypti mosquitoes. Proc Natl Acad Sci U S A. 2017;114:E8017–E8024.
   PubMed Web of Science ®Google Scholar
• Lucas KJ, Roy S, Ha J, et al. MicroRNA-8 targets the Wingless signaling pathway in the female mosquito fat body to regulate reproductive processes. Proc Natl Acad Sci U S A. 2015;112:1440–1445.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhao B, Roy S, et al. microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A. 2016;113:E4828–4836.
   PubMed Web of Science ®Google Scholar
• Dennison NJ, BenMarzouk-Hidalgo OJ, Dimopoulos G. MicroRNA-regulation of Anopheles gambiae immunity to Plasmodium falciparum infection and midgut microbiota. Dev Comp Immunol. 2015;49:170–178.
   PubMed Web of Science ®Google Scholar
• Darnell RB. HITS-CLIP: panoramic views of protein-RNA regulation in living cells. Wiley Interdiscip Rev RNA. 2010;1:266–286.
   PubMed Web of Science ®Google Scholar
• Luhur A, Chawla G, Sokol NS. MicroRNAs as components of systemic signaling pathways in drosophila melanogaster. Dev Timing. 2013;105:97–123.
   Google Scholar
• Gulia-Nuss M, Robertson AE, Brown MR, et al. Insulin-like peptides and the target of rapamycin pathway coordinately regulate blood digestion and egg maturation in the mosquito Aedes aegypti. PloS One. 2011;6:e20401.
   PubMed Web of Science ®Google Scholar
• Chen J, Liang Z, Liang Y, et al. Conserved microRNAs miR-8-5p and miR-2a-3p modulate chitin biosynthesis in response to 20-hydroxyecdysone signaling in the brown planthopper, Nilaparvata lugens. Insect Biochem Mol Biol. 2013;43:839–848.
   PubMed Web of Science ®Google Scholar
• Jiang J, Ge X, Li Z, et al. MicroRNA-281 regulates the expression of ecdysone receptor (EcR) isoform B in the silkworm, Bombyx mori. Insect Biochem Mol Biol. 2013;43:692–700.
   PubMed Web of Science ®Google Scholar
• Jin H, Kim VN, Hyun S. Conserved microRNA miR-8 controls body size in response to steroid signaling in Drosophila. Genes Dev. 2012;26:1427–1432.
   PubMed Web of Science ®Google Scholar
• Xiong XP, Kurthkoti K, Chang KY, et al. miR-34 modulates innate immunity and ecdysone signaling in Drosophila. PLoS Pathog. 2016;12:e1006034.
   PubMed Web of Science ®Google Scholar
• Lozano J, Montanez R, Belles X. MiR-2 family regulates insect metamorphosis by controlling the juvenile hormone signaling pathway. Proc Natl Acad Sci U S A. 2015;112:3740–3745.
   PubMed Web of Science ®Google Scholar