Role of Methoprene-tolerant in the regulation of oogenesis in Dipetalogaster maxima

. 2022 Aug 20 ; 12 (1) : 14195. [epub] 20220820

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

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

Perzistentní odkaz   https://www.medvik.cz/link/pmid35988007

Grantová podpora
R21 AI153689 NIAID NIH HHS - United States
R21 AI167849 NIAID NIH HHS - United States

Odkazy

PubMed 35988007
PubMed Central PMC9392760
DOI 10.1038/s41598-022-18384-5
PII: 10.1038/s41598-022-18384-5
Knihovny.cz E-zdroje

Juvenile hormone (JH) signalling, via its receptor Methoprene-tolerant (Met), controls metamorphosis and reproduction in insects. Met belongs to a superfamily of transcription factors containing the basic Helix Loop Helix (bHLH) and Per Arnt Sim (PAS) domains. Since its discovery in 1986, Met has been characterized in several insect species. However, in spite of the importance as vectors of Chagas disease, our knowledge on the role of Met in JH signalling in Triatominae is limited. In this study, we cloned and sequenced the Dipetalogaster maxima Met transcript (DmaxMet). Molecular modelling was used to build the structure of Met and identify the JH binding site. To further understand the role of the JH receptor during oogenesis, transcript levels were evaluated in two main target organs of JH, fat body and ovary. Functional studies using Met RNAi revealed significant decreases of transcripts for vitellogenin (Vg) and lipophorin (Lp), as well as their receptors. Lp and Vg protein amounts in fat body, as well as Vg in hemolymph were also decreased, and ovarian development was impaired. Overall, these studies provide additional molecular insights on the roles of JH signalling in oogenesis in Triatominae; and therefore are relevant for the epidemiology of Chagas´ disease.

Zobrazit více v PubMed

Rivera-Perez, C., Clifton, M. E., Noriega, F. G. & Jindra, M. Juvenile hormone regulation and action, in Advances in Invertebrate (Neuro) Endocrinology (eds. Saleuddin, S, Lange, A.B, Orchard, I) Vol. 2, 1–76 (Apple Academic Press 2020).

Wigglesworth VB. The physiology of ecdysis in Rhodnius prolixus (Hemiptera). II. Factors controlling moulting and ‘metamorphosis’. Q. J. Microsc. Sci. 1934;77:191–222.

Wigglesworth VB. The function of corpus allatum in the growth and reproduction of R. prolixus (Hemiptera) Q. J. Microsc. Sci. 1936;79:91–121.

Wigglesworth VB. The determination of characters at metamorphosis in Rhodnius prolixus (Hemiptera) J. Experim. Biol. 1940;17:201–223. doi: 10.1242/jeb.17.2.201. DOI

Tobe SS, Bendena WG. The regulation of juvenile hormone production in arthropods. Functional and evolutionary perspectives. Ann. N. Y. Acad. Sci. 1999;897:300–310. doi: 10.1111/j.1749-6632.1999.tb07901.x. PubMed DOI

Ashok M, Turner C, Wilson TG. Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proc. Natl. Acad. Sci. USA. 1998;95:2761–2766. doi: 10.1073/pnas.95.6.2761. PubMed DOI PMC

Charles JP, et al. Ligand-binding properties of a juvenile hormone receptor methoprene-tolerant. Proc. Natl. Acad. Sci. USA. 2011;108:21128–21133. doi: 10.1073/pnas.1116123109. PubMed DOI PMC

Jindra M, et al. Purification of an insect juvenile hormone receptor complex enables insights into its post-translational phosphorylation. J. Biol. Chem. 2021;297(6):101387. doi: 10.1016/j.jbc.2021.101387. PubMed DOI PMC

Bittova L, et al. Exquisite ligand stereoselectivity of a Drosophila juvenile hormone receptor contrasts with its broad agonist repertoire. J. Biol. Chem. 2019;294:410–423. doi: 10.1074/jbc.RA118.005992. PubMed DOI PMC

Li M, Mead EA, Zhu J. Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl. Acad. Sci. USA. 2011;108:638–643. doi: 10.1073/pnas.1013914108. PubMed DOI PMC

Kayukawa T, et al. Transcriptional regulation of juvenile hormone-mediated induction of Krüppel homolog 1, a repressor of insect metamorphosis. Proc. Natl. Acad. Sci. USA. 2012;109:11729–11734. doi: 10.1073/pnas.1204951109. PubMed DOI PMC

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

Villalobos-Sambucaro MJ, et al. The juvenile hormone described in Rhodnius prolixus by Wigglesworth is juvenile hormone III skipped bisepoxide. Sci. Rep. 2020 doi: 10.1038/s41598-020-59495-1. PubMed DOI PMC

Aguirre SA, Frede S, Rubiolo ER, Canavoso LE. Vitellogenesis in the hematophagous Dipetalogaster maxima (Hemiptera: Reduviidae), a vector of Chagas’ disease. J. Insect Physiol. 2008;54:393–402. doi: 10.1016/j.jinsphys.2007.10.012. PubMed DOI

Aguirre SA, et al. Biochemical changes in the transition from vitellogenesis to follicular atresia in the hematophagous dipetalogaster maxima (Hemiptera: Reduviidae) Insect Biochem. Mol. Biol. 2011;41:832–841. doi: 10.1016/j.ibmb.2011.06.005. PubMed DOI

Leyria J, Fruttero LL, Aguirre SA, Canavoso LE. Ovarian nutritional resources during the reproductive cycle of the hematophagous Dipetalogaster maxima (Hemiptera: Reduviidae): Focus on lipid metabolism. Arch. Insect Biochem. Physiol. 2014;87:148–163. doi: 10.1002/arch.21186. PubMed DOI

Leyria J, Fruttero LL, Nazar M, Canavoso LE. The role of DmCatD, a cathepsin D-like peptidase, and acid phosphatase in the process of follicular atresia in Dipetalogaster maxima (Hemiptera: Reduviidae), a vector of chagas’ disease. PLoS ONE. 2015;10(6):e0130144. doi: 10.1371/journal.pone.0130144. PubMed DOI PMC

Leyria J, et al. DmCatD, a cathepsin D-like peptidase of the hematophagous insect Dipetalogaster maxima (Hemiptera: Reduviidae): Purification, bioinformatic analyses and the significance of its interaction with lipophorin in the internalization by developing oocytes. J. Insect Physiol. 2018;105:28–39. doi: 10.1016/j.jinsphys.2018.01.002. PubMed DOI PMC

Ramos FO, et al. Juvenile hormone mediates lipid storage in the oocytes of Dipetalogaster maxima. Insect Biochem. Mol. Biol. 2021;133:103499. doi: 10.1016/j.ibmb.2020.103499. PubMed DOI

Jindra M, Tumova S, Milacek M, Bittova L. A decade with the juvenile hormone receptor. Adv. Insect Physiol. 2021;60:37–8521. doi: 10.1016/bs.aiip.2021.03.001. DOI

Villalobos-Sambucaro MJ, et al. Genomic and functional characterization of a methoprene-tolerant gene in the kissing-bug Rhodnius prolixus. Gen. Comp. Endocrinol. 2015;216:1–8. doi: 10.1016/j.ygcen.2015.04.018. PubMed DOI

Yang J, Zhang Y. Protein structure and function prediction using I-TASSER. Curr. Protoc. Bioinform. 2015;52:5–8. doi: 10.1002/0471250953.bi0508s52. PubMed DOI PMC

Scheuermann TH, et al. Artificial ligand binding within the HIF2α PAS-B domain of the HIF2 transcription factor. Proc. Natl. Acad. Sci. USA. 2009;106:450–455. doi: 10.1073/pnas.0808092106. PubMed DOI PMC

Davey K. The interaction of feeding and mating in the hormonal control of egg production in Rhodnius prolixus. J. Insect. Physiol. 2007;53:208–215. doi: 10.1016/j.jinsphys.2006.10.002. PubMed DOI

Wang Z, Davey KG. The role of juvenile hormone in vitellogenin production in Rhodnius prolixus. J. Insect Physiol. 1993;39:471–476. doi: 10.1016/0022-1910(93)90078-6. DOI

Scheff DS, Campbell JF, Arthur FH, Zhu KY. Effects of aerosol insecticide application location on the patterns of residual efficacy against Tribolium confusum (Coleoptera: Tenebrionidae) larvae. J. Econ. Entomol. 2020;113:2007–2015. doi: 10.1093/jee/toaa103. PubMed DOI

Wilson TG, Fabian J. A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev. Biol. 1986;118:190–201. doi: 10.1016/0012-1606(86)90087-4. PubMed DOI

Konopova B, Smykal V, Jindra M. Common and distinct roles of juvenile hormone signaling genes in metamorphosis of holometabolous and hemimetabolous insects. PLoS ONE. 2011;6(12):e28728. doi: 10.1371/journal.pone.0028728. PubMed DOI PMC

Li M, et al. A steroid receptor coactivator acts as the DNA-binding partner of the methoprene-tolerant protein in regulating juvenile hormone response genes. Mol. Cell. Endocrinol. 2014;394:47–58. doi: 10.1016/j.mce.2014.06.021. PubMed DOI PMC

Jindra M, Uhlirova M, Charles JP, Smykal V, Hill RJ. Genetic evidence for function of the bHLH-PAS protein Gce/Met as a juvenile hormone receptor. PLoS Genet. 2015;11(7):e1005394. doi: 10.1371/journal.pgen.1005394. PubMed DOI PMC

Kotaki T, Shinada T, Kaihara K, Ohfune Y, Numata H. Structure determination of a new juvenile hormone from a Heteropteran insect. Org. Lett. 2009;11:5234–5237. doi: 10.1021/ol902161x. PubMed DOI PMC

Wu Z, Yang L, He Q, Zhou S. Regulatory mechanisms of vitellogenesis in insects. Front. Cell Dev. Biol. 2021;8:593613. doi: 10.3389/fcell.2020.593613. PubMed DOI PMC

Roy S, Saha TT, Zou Z, Raikhel AS. Regulatory pathways controlling female insect reproduction. Annu. Rev. Entomol. 2018;63:489–511. doi: 10.1146/annurev-ento-020117-043258. PubMed DOI

Downer RGH, Chino H. Turnover of protein and diacylglycerol components of lipophorin in insect haemolymph. Insect. Biochem. 1985;15:627–630. doi: 10.1016/0020-1790(85)90124-6. DOI

Chen ME, Lewis DK, Keeley LL, Pietrantonio PV. cDNA cloning and transcriptional regulation of the vitellogenin receptor from the imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae) Insect Mol. Biol. 2004;13:195–204. doi: 10.1111/j.0962-1075.2004.00477.x. PubMed DOI

Clifton ME, Noriega FG. The fate of follicles after a blood meal is dependent on previtellogenic nutrition and juvenile hormone in Aedes aegypti. J. Insect. Physiol. 2012;58:1007–1019. doi: 10.1016/j.jinsphys.2012.05.005. PubMed DOI PMC

Ciudad L, Bellés X, Piulachs MD. Structural and RNAi characterization of the German cockroach lipophorin receptor, and the evolutionary relationships of lipoprotein receptors. BMC Mol. Biol. 2007;8:53. doi: 10.1186/1471-2199-8-53. PubMed DOI PMC

Marchal E, et al. Methoprene-tolerant (met) knockdown in the adult female cockroach, Diploptera punctata completely inhibits ovarian development. PLoS ONE. 2014;9(9):e106737. doi: 10.1371/journal.pone.0106737. PubMed DOI PMC

Tufail M, Takeda M. Insect vitellogenin/lipophorin receptors: Molecular structures, role in oogenesis, and regulatory mechanisms. J. Insect. Physiol. 2009;55:88–104. doi: 10.1016/j.jinsphys.2008.11.007. PubMed DOI

Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Pettersen EF, et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004;25:1605–1612. doi: 10.1002/jcc.20084. PubMed DOI

de Magalhães CS, Barbosa HJC, Dardenne LE. Selection-insertion schemes in genetic algorithms for the flexible ligand docking problem. Comput. Sci. 2004;3102:368–379. doi: 10.1007/978-3-540-24854-5_38. DOI

de Magalhães CS, Almeida DM, Barbosa HJC, Dardenne LE. A dynamic niching genetic algorithm strategy for docking highly flexible ligands. Inf. Sci. 2014;289:206–224. doi: 10.1016/j.ins.2014.08.002. DOI

Katoh K, Rozewicki J, Yamada KD. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 2019;20:1160–1166. doi: 10.1093/bib/bbx108. PubMed DOI PMC

Sela I, Ashkenazy H, Katoh K, Pupko T. GUIDANCE2: Accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res. 2015;43:W7–W14. doi: 10.1093/nar/gkv318. PubMed DOI PMC

Guindon S, et al. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI

Müller T, Vingron MJ. Modeling amino acid replacement. J. Comput. Biol. 2000;7:761–776. doi: 10.1089/10665270050514918. PubMed DOI

Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol. Biol. Evol. 2008;25:1307–1320. doi: 10.1093/molbev/msn067. PubMed DOI

Lefort V, Longueville JE, Gascuel O. SMS: Smart model selection in PhyML. Mol. Biol. Evol. 2017;34:2422–2424. doi: 10.1093/molbev/msx149. PubMed DOI PMC

Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 2006;55:539–552. doi: 10.1080/10635150600755453. PubMed DOI

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

Majerowicz D, et al. Looking for reference genes for real-time quantitative PCR experiments in Rhodnius prolixus (Hemiptera: Reduviidae) Insect Mol. Biol. 2011;20:713–722. doi: 10.1111/j.1365-2583.2011.01101.x. PubMed DOI

Leyria J, Orchard I, Lange AB. Transcriptomic analysis of regulatory pathways involved in female reproductive physiology of Rhodnius prolixus under different nutritional states. Sci. Rep. 2020 doi: 10.1038/s41598-020-67932-4. PubMed DOI PMC

Fruttero LL, Rubiolo ER, Canavoso LE. Biochemical and cellular characterization of lipophorin-midgut interaction in the hematophagous Panstrongylus megistus (Hemiptera: Reduviidae) Insect Biochem. Mol. Biol. 2009;39:322–331. doi: 10.1016/j.ibmb.2009.01.009. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...