Genetics tools for corpora allata specific gene expression in Aedes aegypti mosquitoes

. 2022 Nov 28 ; 12 (1) : 20426. [epub] 20221128

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36443489

Grantová podpora
22-21244S Grantová Agentura České Republiky
R21 AI167849 NIAID NIH HHS - United States
R21 AI153689 NIAID NIH HHS - United States

Odkazy

PubMed 36443489
PubMed Central PMC9705396
DOI 10.1038/s41598-022-25009-4
PII: 10.1038/s41598-022-25009-4
Knihovny.cz E-zdroje

Juvenile hormone (JH) is synthesized by the corpora allata (CA) and controls development and reproduction in insects. Therefore, achieving tissue-specific expression of transgenes in the CA would be beneficial for mosquito research and control. Different CA promoters have been used to drive transgene expression in Drosophila, but mosquito CA-specific promoters have not been identified. Using the CRISPR/Cas9 system, we integrated transgenes encoding the reporter green fluorescent protein (GFP) close to the transcription start site of juvenile hormone acid methyl transferase (JHAMT), a locus encoding a JH biosynthetic enzyme, specifically and highly expressed in the CA of Aedes aegypti mosquitoes. Transgenic individuals showed specific GFP expression in the CA but failed to reproduce the full pattern of jhamt spatiotemporal expression. In addition, we created GeneSwitch driver and responder mosquito lines expressing an inducible fluorescent marker, enabling the temporal regulation of the transgene via the presence or absence of an inducer drug. The use of the GeneSwitch system has not previously been reported in mosquitoes and provides a new inducible binary system that can control transgene expression in Aedes aegypti.

Zobrazit více v PubMed

Rivera-Pérez C, Clifton ME, Noriega FG, Jindra M. Juvenile hormone regulation and action. Adv. Invertebr. Endocrinol. 2020;2:1–76.

Noriega FG. Juvenile hormone biosynthesis in insects: What is new, what do we know, what questions remain? ISRN. 2014 doi: 10.1155/2014/967361. PubMed DOI PMC

Zhu J, Noriega FG. The role of juvenile hormone in mosquito development and reproduction. Adv. Insect Physiol. 2016;51:93–113. doi: 10.1016/bs.aiip.2016.04.005. DOI

Dong S, Dong Y, Simões ML, Dimopoulos G. Mosquito transgenesis for malaria control. Trends Parasitol. 2021;38:54–66. doi: 10.1016/j.pt.2021.08.001. PubMed DOI

Wang GH, Gamez S, Raban RR, Marshall JM, Alphey L, Li M, Rasgon JL, Akbari OS. Combating mosquito-borne diseases using genetic control technologies. Nat. Commun. 2021;12:4388. doi: 10.1038/s41467-021-24654-z. PubMed DOI PMC

Venken KJ, Bellen HJ. Emerging technologies for gene manipulation in Drosophila melanogaster. Nat. Rev. Genet. 2005;6:167–178. doi: 10.1038/nrg1553. PubMed DOI

Xu RG, Wang X, Shen D, Sun J, Qiao HH, Wang F, Liu LP, Ni JQ. Perspectives on gene expression regulation techniques in Drosophila. J. Genet. Genomics. 2019;46:213–220. doi: 10.1016/j.jgg.2019.03.006. PubMed DOI

Mirth C, Truman JW, Riddiford LM. The role of the prothoracic gland in determining critical weight for metamorphosis in Drosophila melanogaster. Curr. Biol. 2005;15:1796–1807. doi: 10.1016/j.cub.2005.09.017. PubMed DOI

Adolfi A, Lycett GJ. Opening the toolkit for genetic analysis and control of Anopheles mosquito vectors. Curr. Opin. Insect Sci. 2018;30:8–18. doi: 10.1016/j.cois.2018.07.014. PubMed DOI

Moreira LA, Edwards MJ, Adhami F, Jasinskiene N, James AA, Jacobs-Lorena M. Robust gut-specific gene expression in transgenic Aedes aegypti mosquitoes. Proc. Natl. Acad. Sci. USA. 2000;97:10895–10898. doi: 10.1073/pnas.97.20.10895. PubMed DOI PMC

Kokoza VA, Raikhel AS. Targeted gene expression in the transgenic Aedes aegypti using the binary Gal4-UAS system. Insect Biochem. Mol. Biol. 2011;41:637–644. doi: 10.1016/j.ibmb.2011.04.004. PubMed DOI PMC

Lynd A, Lycett GJ. Development of the bi-partite Gal4-UAS system in the African malaria mosquito, Anopheles gambiae. PLoS ONE. 2012;7:e31552. doi: 10.1371/journal.pone.0031552. PubMed DOI PMC

Riabinina O, Task D, Marr E, Lin CC, Alford R, O'Brochta DA, Potter CJ. Organization of olfactory centres in the malaria mosquito Anopheles gambiae. Nat. Commun. 2016;7:13010. doi: 10.1038/ncomms13010. PubMed DOI PMC

Stebbins MJ, Urlinger S, Byrne G, Bello B, Hillen W, Yin JCP. Tetracycline-inducible systems for Drosophila. Proc. Natl. Acad. Sci. USA. 2001;98:10775–10780. doi: 10.1073/pnas.121186498. PubMed DOI PMC

Lycett GJ, Kafatos FC, Loukeris TG. Conditional expression in the malaria mosquito Anopheles stephensi with Tet-On and Tet-Off systems. Genetics. 2004;167:1781–1790. doi: 10.1534/genetics.104.028175. PubMed DOI PMC

Moullan N, et al. Tetracyclines disturb mitochondrial function across Eukaryotic models: A call for caution in biomedical research. Cell Rep. 2015;10:1681–1691. doi: 10.1016/j.celrep.2015.02.034. PubMed DOI PMC

Osterwalder T, Yoon KS, White BH, Keshishian HA. Conditional tissue-specific transgene expression system using inducible GAL4. Proc. Natl. Acad. Sci. USA. 2001;98:12596–12601. doi: 10.1073/pnas.221303298. PubMed DOI PMC

Scialo F, Sriram A, Stefanatos R, Sanz A. Practical recommendations for the use of the GeneSwitch Gal4 system to knock-down genes in Drosophila melanogaster. PLoS ONE. 2016;11(8):e0161817. doi: 10.1371/journal.pone.0161817. PubMed DOI PMC

Mayoral JG, Nouzova M, Yoshiyama M, Shinoda T, Hernandez-Martinez S, Dolghih E, Turjanski AG, Roitberg AR, Priestap H, Perez M, Mackenzie L, Li Y, Noriega FG. Molecular and functional characterization of a juvenile hormone acid methyltransferase expressed in the corpora allata of mosquitoes. Insect Biochem. Mol. Biol. 2009;39:31–37. doi: 10.1016/j.ibmb.2008.09.010. PubMed DOI PMC

Nouzova M, Edwards MJ, Mayoral JG, Noriega FG. A coordinated expression of biosynthetic enzyme controls the flux of juvenile hormone precursors in the corpora allata of mosquitoes. Insect Biochem. Mol. Biol. 2011;41:660–669. doi: 10.1016/j.ibmb.2011.04.008. PubMed DOI PMC

Nouzova M, Edwards MJ, Michalkova V, Ramirez CE, Ruiz M, Areiza M, DeGennaro M, Fernandez-Lima F, Feyereisen R, Jindra M, Noriega FG. Epoxidation of juvenile hormone was a key innovation improving insect reproductive fitness. Proc. Natl. Acad. Sci. USA. 2021;118(45):e2109381118. doi: 10.1073/pnas.2109381118. PubMed DOI PMC

Li Y, Hernández-Martínez S, Unnithan GC, Feyereisen R, Noriega FG. Activity of the corpora allata of adult female Aedes aegypti: Effects of mating and feeding. Insect Biochem. Mol. Biol. 2003;33:1307–1315. doi: 10.1016/j.ibmb.2003.07.003. PubMed DOI

Ramirez CE, Nouzova M, Michalkova V, Fernandez-Lima F, Noriega FG. Common structural features facilitate the simultaneous identification and quantification of the five most common juvenile hormones by liquid chromatography-tandem mass spectrometry. Insect Biochem. Mol. Biol. 2020;116:103287. doi: 10.1016/j.ibmb.2019.103287. PubMed DOI PMC

Kwon SG, Hadjantonakis AK. Eomes::GFP: A tool for live imaging cells of the trophoblast, primitive streak, and telencephalon in the mouse embryo. Genesis. 2007;45:208–217. doi: 10.1002/dvg.20293. PubMed DOI PMC

Dermauw W, Van Leeuwen T, Feyereisen R. Diversity and evolution of the P450 family in arthropods. Insect Biochem. Mol. Biol. 2020;127:103490. doi: 10.1016/j.ibmb.2020.103490. PubMed DOI

Yoshida S, Watanabe H. Robust salivary gland-specific transgene expression in Anopheles stephensi mosquito. Insect Mol. Biol. 2006;15:403–410. doi: 10.1111/j.1365-2583.2006.00645.x. PubMed DOI

Nirmala X, Marinotti O, Sandoval JM, Phin S, Gakhar S, Jasinskiene N, James AA. Functional characterization of the promoter of the vitellogenin gene, AsVg1, of the malaria vector, Anopheles stephensi. Insect Biochem. Mol. Biol. 2006;36:694–700. doi: 10.1016/j.ibmb.2006.05.011. PubMed DOI

Smith R, Walter M, Hice R, O'Brochta D, Atkinson P. Testis- specific expression of the b2 tubulin promoter of Aedes aegypti and its application as a genetic sex-separation marker. Insect Mol. Biol. 2007;16:61–71. doi: 10.1111/j.1365-2583.2006.00701.x. PubMed DOI

Abdou M, He Q, Wen D, Zyaan O, Wang J, et al. Drosophila Met and Gce are partially redundant in transducing juvenile hormone action. Insect Biochem. Mol. Biol. 2011;41:938–945. doi: 10.1016/j.ibmb.2011.09.003. PubMed DOI

Wen D, Rivera-Perez C, Abdou M, Jia Q, He Q, Zyaan O, Bendena WB, Tobe SS, Noriega FG, Palli SR, Wang J, Li S. Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis. PLoS Genet. 2015;11:e1005038. doi: 10.1371/journal.pgen.1005038. PubMed DOI PMC

Figure TE, et al. 5HTR3A-driven GFP labels immature olfactory sensory neurons. Comp. Neurol. 2017;525:1743–1755. doi: 10.1002/cne.24180. PubMed DOI PMC

Tobe SS. Asymmetry in hormone biosynthesis by insect endocrine glands. Can. J. Zool. 1977;55:1509–1514. doi: 10.1139/z77-195. DOI

Kirkpatrick RB, Parveen Z, Martin PF. Isolation of silencer-containing sequences causing a tissue-specific position effect on alcohol dehydrogenase expression in Drosophila melanogaster. Dev. Genet. 1994;15:188–200. doi: 10.1002/dvg.1020150209. PubMed DOI

Pfeiffer BD, et al. Refinement of tools for targeted gene expression in Drosophila. Genetics. 2010;186:735–755. doi: 10.1534/genetics.110.119917. PubMed DOI PMC

Duncker BP, et al. Introns boost transgene expression in Drosophila melanogaster. Mol. Gen. Genet. 1997;254:291–296. doi: 10.1007/s004380050418. PubMed DOI

Zieler H, Huynh CQ. Intron-dependent stimulation of marker gene expression in cultured insect cells. Insect Mol. Biol. 2002;11:87–95. doi: 10.1046/j.0962-1075.2001.00312.x. PubMed DOI

Baten AKMA, et al. Splice site identification using probabilistic parameters and SVM classification. BMC Bioinform. 2006;7(5):15. doi: 10.1186/1471-2105-7-S5-S15. PubMed DOI PMC

Sibley CR, Blazquez L, Ule J. Lessons from non-canonical splicing. Nat. Rev. Genet. 2016;17:407–421. doi: 10.1038/nrg.2016.46. PubMed DOI PMC

Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993;118:401–415. doi: 10.1242/dev.118.2.401. PubMed DOI

O'Brochta DA, Pilitt KL, Harrell RA, Aluvihare C, Alford RT. Gal4-based enhancer-trapping in the malaria mosquito Anopheles stephensi. G3. 2012;2(11):1305–1315. doi: 10.1534/g3.112.003582. PubMed DOI PMC

Nene V, Wortman JR, Lawson D, et al. Genome sequence of Aedes aegypti, a major arbovirus vector. Science. 2007;316:1718–1723. doi: 10.1126/science.1138878. PubMed DOI PMC

Matthews BJ, Dudchenko O, Kingan SB, et al. Improved reference genome of Aedes aegypti informs arbovirus vector control. Nature. 2018;563:501–507. doi: 10.1038/s41586-018-0692-z. PubMed DOI PMC

Potter CJ, Tasic B, Russler EV, Liang L, Luo L. The Q system: A repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell. 2010;141:536–548. doi: 10.1016/j.cell.2010.02.025. PubMed DOI PMC

del Valle Rodriguez A, Didiano D, Desplan C. Power tools for gene expression and clonal analysis in Drosophila. Nat. Methods. 2012;9:47–55. doi: 10.1038/nmeth.1800. PubMed DOI PMC

Riabinina O, Potter CJ. The Q-system: a versatile expression system for Drosophila. Methods Mol. Biol. 2016;1478:53–78. doi: 10.1007/978-1-4939-6371-3_3. PubMed DOI PMC

Diao F, White BH. A novel approach for directing transgene expression in Drosophila: T2A-Gal4 in-frame fusion. Genetics. 2012;190:1139–1144. doi: 10.1534/genetics.111.136291. PubMed DOI PMC

Matthews BJ, Younger MA, Vosshall LB. The ion channel ppk301 controls freshwater egg-laying in the mosquito Aedes aegypti. Elife. 2019;8:e43963. doi: 10.7554/eLife.43963. PubMed DOI PMC

Rivera-Perez C, Nouzova M, Lamboglia I, Noriega FG. Metabolic analysis reveals changes in the mevalonate and juvenile hormone synthesis pathways linked to the mosquito reproductive physiology. Insect Biochem. Mol. Biol. 2014;51:1–9. doi: 10.1016/j.ibmb.2014.05.001. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...