Regulation of Gene Expression Patterns in Mosquito Reproduction

English version České info

In addition to being vectors of devastating human diseases, mosquitoes represent outstanding model organisms for studying regulatory mechanisms of differential gene expression due to their rapid reproductive cycles. About 7500 transcripts are differentially expressed in four sequential waves during the 72-h reproductive period in the fat body, a critical reproductive organ. The major regulators for these waves of gene expression are the two very important insect hormones, 20-hydroxyecdysone (20E) and Juvenile hormone (JH), their respective receptors Ecdysone Receptor (EcR) and Methoprene-Tolerant (Met), amino acids and the orphan nuclear receptor HR3. These key regulators are responsible for activation and repression of co-regulated gene sets, at different time points, within the 72-h reproductive period. Importantly, this study, apart from providing an insight into the regulatory complexity involved in the temporal coordination of gene expression, also reveals the previously unidentified roles of 20E/EcR, JH/Met and HR3 during the 72-h period post blood meal.

Vyšlo v časopise: Regulation of Gene Expression Patterns in Mosquito Reproduction. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005450
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005450

Souhrn

Zdroje

1. White KP, Hurban P, Watanabe T, Hogness DS (1997) Coordination of Drosophila metamorphosis by two ecdysone-induced nuclear receptors. Science. 276(5309):114–117

2. Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS, et al. (2002) Gene expression during the life cycle of Drosophila melanogaster. Science. 297(5590):2270–2275

3. Li TR, White KP (2003) Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev Cell. 5(1):59–72

4. Stolc V, Gauhar Z, Mason C, Halasz G, van Batenburg MF, Rifkin SA, et al. (2004) A gene expression map for the euchromatic genome of Drosophila melanogaster. Science. 306(5696):655–660

5. Hooper SD, Boué S, Krause R, Jensen LJ, Mason CE, Ghanim M, et al. (2007) Identification of tightly regulated groups of genes during Drosophila melanogaster embryogenesis. Mol Syst Biol 3:72

6. Papatsenko I, Levine M, Papatsenko D (2010) Temporal waves of coherent gene expression during Drosophila embryogenesis. Bioinformatics. 26(21):2731–2736

7. Short SM and Lazzaro BP (2013) Reproductive status alters transcriptomic response to infection in female Drosophila melanogaster. G3 (Bethesda). 3(5):827–840

8. Chanut-Delalande H, Hashimoto Y, Pelissier-Monier A, Spokony R, Dib A, Kondo T, et al. (2014) Pri peptides are mediators of ecdysone for the temporal control of development. Nat Cell Biol. 16(11):1035–1044

9. Potier D, Davie K, Hulselmans G, Naval Sanchez M, Haagen L, Huynh-Thu VA, et al. (2014) Mapping gene regulatory networks in Drosophila eye development by large-scale transcriptome perturbations and motif inference. Cell Rep. 9(6):2290–2303

10. Dana AN, Hong YS, Kern MK, Hillenmeyer ME, Harker BW, Lobo NF, et al. (2005) Gene expression patterns associated with blood-feeding in the malaria mosquito Anopheles gambiae. BMC Genomics. 6:5

11. Marinotti O, Calvo E, Nguyen QK, Dissanayake S, Ribeiro JM, James AA (2006) Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect Mol Biol. 1:1–12

12. Bonizzoni M, Dunn WA, Campbell CL, Olson KE, Dimon MT, Marinotti O, et al. (2011) RNA-seq analyses of blood-induced changes in gene expression in the mosquito vector species, Aedes aegypti. BMC Genomics. 12:82

13. Hagedorn HH (2005) Mosquito Endocrinology. In: Marquardt WC, editor. Biology of Disease Vectors. Elsevier Academic Press. p317–327

14. Zou Z, Saha TT, Roy S, Shin SW, Backman TW, Girke T, et al.(2013) Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression. Proc Natl Acad Sci U S A. 110(24):E2173–E2181

15. Hansen IA, Attardo GM, Park JH, Peng Q, Raikhel AS (2004) Target of rapamycin-mediated amino acid signaling in mosquito anautogeny. Proc Natl Acad Sci U S A. 101(29):10626–10631

16. Roy SG, Hansen IA, Raikhel AS (2007) Effect of insulin and 20-hydroxyecdysone in the fat body of the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol. 37(12):1317–1326

17. Brown MR, Clark KD, Gulia M, Zhao Z, Garczynski SF, Crim JW, et al. (2008) An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A. 105(15):5716–5721

18. Brandon MC, Pennington JE, Isoe J, Zamora J, Schillinger AS, Miesfeld RL (2008) TOR signaling is required for amino acid stimulation of early trypsin protein synthesis in the midgut of Aedes aegypti mosquitoes. Insect Biochem Mol Biol. 38(10):916–922

19. Gulia-Nuss M, Robertson AE, Brown MR, Strand MR (2011) Insulin-like peptides and the target of rapamycin pathway coordinately regulate blood digestion and egg maturation in the mosquito Aedes aegypti. PLoS One. 6(5):e20401

20. Raikhel AS (2005) Vitellogenesis of Disease Vectors, From Physiology to Genes. In: Marquardt WC, editor. Biology of Disease Vectors. Elsevier Academic Press. p329–345

21. Bryant B, Raikhel AS (2011) Programmed autophagy in the fat body of Aedes aegypti is required to maintain egg maturation cycles. PLoS One. 6(11):e25502

22. Zou Z, Souza-Neto J, Xi Z, Kokoza V, Shin SW, Dimopoulos G, et al. (2011) Transcriptome analysis of Aedes aegypti transgenic mosquitoes with altered immunity. PLoS Pathog. 7(11):e1002394

23. Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, et al. (2011) eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res. 40(database issue):D284–289

24. Attardo GM, Hansen IA, Shiao SH, Raikhel AS (2006) Identification of two cationic amino acid transporters required for nutritional signaling during mosquito reproduction. J Exp Biol. 209(Pt 16):3071–3078

25. Shapiro AB, Wheelock GD, Hagedorn HH, Baker FC, Tsai LW, Schooley DA (1986) Juvenile hormone and juvenile esterase in adult females in Aedes aegypti. J Insect Physiol. 32:867–877

26. Hernández-Martínez S, Rivera-Perez C, Nouzova M, Noriega FG (2014) Coordinated changes in JH biosynthesis and JH hemolymph titers in Aedes aegypti mosquitoes. J Insect Physiol. 72:22–27

27. Roy SG, Raikhel AS (2011) The small GTPase Rheb is a key component linking amino acid signaling and TOR in the nutritional pathway that controls mosquito egg development. Insect Biochem Mol Biol. 41(1):62–69

28. Mane-Padros D, Cruz J, Cheng A, Raikhel AS (2012) A critical role of the nuclear receptor HR3 in regulation of gonadotrophic cycles of the mosquito Aedes aegypti. PLoS One. 2012;7(9):e45019

29. Price DP, Nagarajan V, Churbanov A, Houde P, Milligan B, Drake LL, et al. (2011) The fat body transcriptomes of the yellow fever mosquito Aedes aegypti, pre- and post- blood meal. PLoS One. 6(7):e22573

30. Feitosa FM, Calvo E, Merino EF, Durham AM, James AA, de Bianchi AG, et al. (2006) A transcriptome analysis of the Aedes aegypti vitellogenic fat body. J Insect Sci. 6:1–26

31. Attardo GM, Hansen IA, Raikhel AS (2005) Nutritional regulation of vitellogenesis in mosquitoes: implications for anautogeny. Insect Biochem Mol Biol. 35(7):661–675

32. Raikhel AS, Dhadialla TS (1992) Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol. 37:217–251

33. Hagedorn HH, Turner S, Hagedorn EA, Pontecorvo D, Greenbaum P, Pfeiffer D, et al. (1977) Postemergence growth of the ovarian follicles of Aedes aegypti. J Insect Physiol. 23(2):203–206

34. Raikhel AS, Lea AO (1990) Juvenile hormone controls previtellogenic proliferation of ribosomal RNA in the mosquito fat body. Gen Comp Endocrinol. 77(3):423–434

35. Zhu J, Chen L, Raikhel AS (2003) Posttranscriptional control of the competence factor betaFTZ-F1 by juvenile hormone in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A. 100(23):13338–13343

36. Raikhel AS, Lea AO (1983) Previtellogenic development and vitellogenin synthesis in the fat body of a mosquito: an ultrastructural and immunocytochemical study. Tissue Cell. 15(2):281–299

37. Shiao SH, Hansen IA, Zhu J, Sieglaff DH, Raikhel AS (2007) Juvenile hormone connects larval nutrition with target of rapamycin signaling in the mosquito Aedes aegypti. Journal of Insect Physiology. 54(1):231–239

38. Price DP, Schilkey FD, Ulanov A, Hansen IA (2015) Small mosquitoes, large implications: crowding and starvation affects gene expression and nutrient accumulation in Aedes aegypti. Parasites & Vectors 8:252

39. Zahurak M, Parmigiani G, Yu W, Scharpf RB, Berman D, Schaeffer E, et al. (2007) Pre-processing Agilent microarray data. BMC Bioinformatics. 8:142

40. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit Set al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5(10):R80