Juvenile Hormone and Its Receptor Methoprene-tolerant Promote Ribosomal Biogenesis and Vitellogenesis in the Mosquito

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2017 Apr 28

PMID 28446607

Citations 20

Authors

Jia-Lin Wang

Tusar T Saha

Yang Zhang

Changyu Zhang

Alexander S Raikhel

Affiliations

Soon will be listed here.

Abstract

Juvenile hormone (JH) controls many biological activities in insects, including development, metamorphosis, and reproduction. In the mosquito, a vector of dengue, yellow fever, chikungunya, and zika viruses, the metabolic tissue (the fat body, which is an analogue of the vertebrate liver) produces yolk proteins for developing oocytes. JH is important for the fat body to acquire competence for yolk protein production. However, the molecular mechanisms of how JH promotes mosquito reproduction are not completely understood. In this study we show that stimulation of the JH receptor methoprene-tolerant (Met) activates expression of genes encoding the regulator of ribosome synthesis 1 (RRS1) and six ribosomal proteins (two ribosomal large subunit proteins, two ribosomal small subunit proteins, and two mitochondrial ribosomal proteins). Moreover, RNAi-mediated depletion of decreased biosynthesis of the ribosomal protein L32 (RpL32). Depletion of , , or led to retardation of ovarian growth and reduced mosquito fecundity, which may at least in part have resulted from decreased vitellogenin protein production in the fat body. In summary, our results indicate that JH is critical for inducing the expression of ribosomal protein genes and demonstrate that RRS1 mediates the JH signal to enhance both ribosomal biogenesis and vitellogenesis.

Citing Articles

Dual roles of methoprene-tolerant gene in male molting and female reproduction of the tomato leafminer, (meyrick).

Zhang T, Xu K, Liu D, Ma H, Liu W, Yang W Front Physiol. 2024; 15:1500391.

PMID: 39611077 PMC: 11603827. DOI: 10.3389/fphys.2024.1500391.

Mosquito gene targeted RNAi studies for vector control.

Yadav M, Dahiya N, Sehrawat N Funct Integr Genomics. 2023; 23(2):180.

PMID: 37227504 PMC: 10211311. DOI: 10.1007/s10142-023-01072-6.

The LIM Domain Protein BmFHL2 Inhibits Egg Production in Female Silkworm, .

Yuan Q, Sun X, Lu R, Qu Z, Ding X, Dai T Cells. 2023; 12(3).

PMID: 36766794 PMC: 9913792. DOI: 10.3390/cells12030452.

Aspirin Inhibition of Prostaglandin Synthesis Impairs Mosquito Egg Development.

Choi D, Al Baki M, Ahmed S, Kim Y Cells. 2022; 11(24).

PMID: 36552860 PMC: 9776805. DOI: 10.3390/cells11244092.

Genome-Wide Identification and Stage-Specific Expression Profile Analysis Reveal the Function of Ribosomal Proteins for Oogenesis of .

Sun R, Liu J, Xu Y, Jiang L, Li Y, Zhong G Front Physiol. 2022; 13:943205.

PMID: 35812325 PMC: 9259932. DOI: 10.3389/fphys.2022.943205.

References

Estep A, Sanscrainte N, Becnel J . DsRNA-mediated targeting of ribosomal transcripts RPS6 and RPL26 induces long-lasting and significant reductions in fecundity of the vector Aedes aegypti. J Insect Physiol. 2016; 90:17-26. DOI: 10.1016/j.jinsphys.2016.05.001. View

Tsuno A, Miyoshi K, Tsujii R, Miyakawa T, Mizuta K . RRS1, a conserved essential gene, encodes a novel regulatory protein required for ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol. 2000; 20(6):2066-74. PMC: 110823. DOI: 10.1128/MCB.20.6.2066-2074.2000. View

Zhang J, Harnpicharnchai P, Jakovljevic J, Tang L, Guo Y, Oeffinger M . Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes Dev. 2007; 21(20):2580-92. PMC: 2000323. DOI: 10.1101/gad.1569307. View

Miyoshi K, Shirai C, Horigome C, Takenami K, Kawasaki J, Mizuta K . Rrs1p, a ribosomal protein L11-binding protein, is required for nuclear export of the 60S pre-ribosomal subunit in Saccharomyces cerevisiae. FEBS Lett. 2004; 565(1-3):106-10. DOI: 10.1016/j.febslet.2004.03.087. View

He F, James A, Raje H, Ghaffari H, DiMario P . Deletion of Drosophila Nopp140 induces subcellular ribosomopathies. Chromosoma. 2014; 124(2):191-208. DOI: 10.1007/s00412-014-0490-9. View

Tsetsarkin K, Chen R, Weaver S . Interspecies transmission and chikungunya virus emergence. Curr Opin Virol. 2016; 16:143-150. PMC: 4824623. DOI: 10.1016/j.coviro.2016.02.007. View

Bian G, Raikhel A, Zhu J . Characterization of a juvenile hormone-regulated chymotrypsin-like serine protease gene in Aedes aegypti mosquito. Insect Biochem Mol Biol. 2008; 38(2):190-200. PMC: 2253661. DOI: 10.1016/j.ibmb.2007.10.008. View

Zhang Z, Xu J, Sheng Z, Sui Y, Palli S . Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, methoprene tolerant. J Biol Chem. 2010; 286(10):8437-8447. PMC: 3048728. DOI: 10.1074/jbc.M110.191684. View

Li M, Mead E, Zhu J . Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad Sci U S A. 2010; 108(2):638-43. PMC: 3021087. DOI: 10.1073/pnas.1013914108. View

10.

Attardo G, Hansen I, Raikhel A . Nutritional regulation of vitellogenesis in mosquitoes: implications for anautogeny. Insect Biochem Mol Biol. 2005; 35(7):661-75. DOI: 10.1016/j.ibmb.2005.02.013. View

11.

Raikhel A, Lea A . Control of follicular epithelium development and vitelline envelope formation in the mosquito; role of juvenile hormone and 20-hydroxyecdysone. Tissue Cell. 1991; 23(4):577-91. DOI: 10.1016/0040-8166(91)90015-l. View

12.

Miura K, Oda M, Makita S, Chinzei Y . Characterization of the Drosophila Methoprene -tolerant gene product. Juvenile hormone binding and ligand-dependent gene regulation. FEBS J. 2005; 272(5):1169-78. DOI: 10.1111/j.1742-4658.2005.04552.x. View

13.

Zhao B, Hou Y, Wang J, Kokoza V, Saha T, Wang X . Determination of juvenile hormone titers by means of LC-MS/MS/MS and a juvenile hormone-responsive Gal4/UAS system in Aedes aegypti mosquitoes. Insect Biochem Mol Biol. 2016; 77:69-77. PMC: 5028310. DOI: 10.1016/j.ibmb.2016.08.003. View

14.

Ernst K, Walker K, Reyes-Castro P, Joy T, Castro-Luque A, Diaz-Caravantes R . Aedes aegypti (Diptera: Culicidae) Longevity and Differential Emergence of Dengue Fever in Two Cities in Sonora, Mexico. J Med Entomol. 2017; 54(1):204-211. PMC: 5853638. DOI: 10.1093/jme/tjw141. View

15.

Roy S, Hansen I, Raikhel A . Effect of insulin and 20-hydroxyecdysone in the fat body of the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol. 2007; 37(12):1317-26. PMC: 2104489. DOI: 10.1016/j.ibmb.2007.08.004. View

16.

Raikhel A, Dhadialla T . Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol. 1992; 37:217-51. DOI: 10.1146/annurev.en.37.010192.001245. View

17.

Guo W, Wu Z, Song J, Jiang F, Wang Z, Deng S . Juvenile hormone-receptor complex acts on mcm4 and mcm7 to promote polyploidy and vitellogenesis in the migratory locust. PLoS Genet. 2014; 10(10):e1004702. PMC: 4207617. DOI: 10.1371/journal.pgen.1004702. View

18.

Zhu J, Chen L, Raikhel A . Posttranscriptional control of the competence factor betaFTZ-F1 by juvenile hormone in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A. 2003; 100(23):13338-43. PMC: 263810. DOI: 10.1073/pnas.2234416100. View

19.

Zou Z, Saha T, Roy S, Shin S, Backman T, Girke T . Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression. Proc Natl Acad Sci U S A. 2013; 110(24):E2173-81. PMC: 3683779. DOI: 10.1073/pnas.1305293110. View

20.

Massari M, Murre C . Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol. 1999; 20(2):429-40. PMC: 85097. DOI: 10.1128/MCB.20.2.429-440.2000. View