Juvenile Hormone-Receptor Complex Acts on and to Promote Polyploidy and Vitellogenesis in the Migratory Locust

English version České info

Vitellogenesis, a hormonally-regulated process for the synthesis of yolk proteins by the fat body or liver and their sequestration in developing oocytes, takes place in all oviparous animals except mammals. Polyploidy has also been implicated in hormone-regulated development and reproduction. Although juvenile hormone (JH) is known to regulate polyploidy in insect models and also plays a pivotal role in stimulating insect vitellogenesis, the molecular mechanisms remain poorly understood. In the migratory locust, Locusta migratoria, vitellogenesis is dependent on JH, and JH stimulates DNA replication and increases ploidy in the fat body. Here, we show that a JH-receptor complex comprised of Methoprene-tolerant (Met) and a steroid receptor co-activator activates the transcription of two mini-chromosome maintenance (Mcm) genes, Mcm4 and Mcm7. Knockdown of Mcm4 or Mcm7 via RNAi can phenocopy JH-deprivation and Met-depletion, resulting in reduced ploidy, blocked vitellogenin (Vg) expression, as well as arrested oocyte maturation and ovarian growth. This study provides evidence that JH acts through its receptor on the Mcm machinery to replicate the genome of fat body cells in preparation for the massive synthesis of Vg and possibly other proteins required for oocyte maturation and egg production.

Vyšlo v časopise: Juvenile Hormone-Receptor Complex Acts on and to Promote Polyploidy and Vitellogenesis in the Migratory Locust. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004702
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004702

Souhrn

Zdroje

1. WyattGR, DaveyKG (1996) Cellular and molecular actions of juvenile Hormone. II. Roles of juvenile hormone in adult insects. Adv Insect Physiol 26: 1–155.

2. RiddifordLM (1994) Cellular and molecular actions of juvenile Hormone I. General considerations and premetamorphic actions. Adv Insect Physiol 24: 213–274.

3. JindraM, PalliSR, RiddifordLM (2013) The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58: 181–204.

4. RiddifordLM (2012) How does juvenile hormone control insect metamorphosis and reproduction? Gen Comp Endocr 179: 477–484.

5. CharlesJ-P, IwemaT, EpaVC, TakakiK, RynesJ, et al. (2011) Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc Natl Acad Sci USA 108: 21128–21133.

6. MiuraK, OdaM, MakitaS, ChinzeiY (2005) Characterization of the Drosophila Methoprene-tolerant gene product - Juvenile hormone binding and ligand-dependent gene regulation. FEBS J 272: 1169–1178.

7. KayukawaT, MinakuchiC, NamikiT, TogawaT, YoshiyamaM, et al. (2012) Transcriptional regulation of juvenile hormone-mediated induction of Krüppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci USA 109: 11729–11734.

8. ZhangZ, XuJ, ShengZ, SuiY, PalliSR (2011) Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, Methoprene tolerant. J Biol Chem 286: 8437–8447.

9. LiM, MeadEA, ZhuJ (2011) Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad Sci USA 108: 638–643.

10. KonopovaB, SmykalV, JindraM (2011) Common and distinct roles of juvenile hormone signaling genes in metamorphosis of holometabolous and hemimetabolous insects. PLoS ONE 6: e28728.

11. Raikhel A, Brown M, Belles X (2005) Hormonal control of reproductive process. In: Gilbert LI, Iatrou K, Gill SS, editors. Comprehensive Molecular Insect Science: Elsevier Ltd., Boston. pp. 433–491.

12. Belles X (2004) Vitellogenesis directed by juvenile hormone. In: Raikhel AS, editor. Reproductive Biology of Invertebrate: Progress in Vitellogenesis: Science Publishers Inc. pp. 157–197.

13. RichardDS, JonesJM, BarbaritoMR, CerulaS, DetweilerJP, et al. (2001) Vitellogenesis in diapausing and mutant Drosophila melanogaster: further evidence for the relative roles of ecdysteroids and juvenile hormones. J Insect Physiol 47: 905–913.

14. BownesM (1989) The roles of juvenile-hormone, ecdysone and the ovary in the control of Drosophila vitellogenesis. J Insect Physiol 35: 409–413.

15. RaikhelAS, KokozaVA, ZhuJS, MartinD, WangSF, et al. (2002) Molecular biology of mosquito vitellogenesis: from basic studies to genetic engineering of antipathogen immunity. Insect Biochem Mol Biol 32: 1275–1286.

16. RaikhelAS, DhadiallaTS (1992) Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol 37: 217–251.

17. ParthasarathyR, PalliSR (2011) Molecular analysis of nutritional and hormonal regulation of female reproduction in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 41: 294–305.

18. ParthasarathyR, SunZ, BaiH, PalliSR (2010) Juvenile hormone regulation of vitellogenin synthesis in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 40: 405–414.

19. ParthasarathyR, ShengZT, SunZY, PalliSR (2010) Ecdysteroid regulation of ovarian growth and oocyte maturation in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 40: 429–439.

20. SmykalV, BajgarA, ProvaznikJ, FexovaS, BuricovaM, et al. (2014) Juvenile hormone signaling during reproduction and development of the linden bug, Pyrrhocoris apterus. Insect Biochem Mol Biol 45: 69–76.

21. OishiM, LockeJ, WyattGR (1985) The ribosomal RNA genes of Locusta migratoria: copy number and evidence for underreplication in a polyploid tissue. Can J Biochem Cell B 63: 1064–1070.

22. NairKK, ChenTT, WyattGR (1981) Juvenile hormone-stimulated polyploidy in adult locust fat body. Dev Biol 81: 356–360.

23. LeeHO, DavidsonJM, DuronioRJ (2009) Endoreplication: polyploidy with purpose. Gene Dev 23: 2461–2477.

24. BochmanML, SchwachaA (2009) The mcm complex: unwinding the mechanism of a replicative helicase. Microbiol Mol Biol R 73: 652–683.

25. YouZ, IshimiY, MasaiH, HanaokaF (2002) Roles of Mcm7 and Mcm4 subunits in the DNA helicase activity of the mouse Mcm4/6/7 complex. J Biol Chem 277: 42471–42479.

26. WatanabeE, OharaR, IshimiY (2012) Effect of an MCM4 mutation that causes tumours in mouse on human MCM4/6/7 complex formation. J Biochem 152: 191–198.

27. BagleyBN, KeaneTM, MaklakovaVI, MarshallJG, LesterRA, et al. (2012) A dominantly acting murine allele of Mcm4 causes chromosomal abnormalities and promotes tumorigenesis. PLoS Genet 8: e1003034.

28. LockeJ, WhiteBN, WyattGR (1987) Cloning and 5′ end nucleotide sequences of two juvenile hormone-inducible vitellogenin genes of the African migratory locust. DNA 6: 331–342.

29. DhadiallaTS, CookKE, WyattGR (1987) Vitellogenin mRNA in locust fat body: Coordinate induction of two genes by a juvenile hormone analog. Dev Biol 123: 108–114.

30. WangX, FangX, YangP, JiangX, JiangF, et al. (2014) The locust genome provides insight into swarm formation and long-distance flight. Nat Commun 5: 2957.

31. ChenS, YangP, JiangF, WeiY, MaZ, et al. (2010) De Novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. PLoS ONE 5: e15633.

32. KaplanDL, DaveyMJ, O'DonnellM (2003) Mcm4,6,7 uses a “pump in ring” mechanism to unwind DNA by steric exclusion and actively translocate along a duplex. J Biol Chem 278: 49171–49182.

33. MassariME, MurreC (2000) Helix-loop-helix proteins: Regulators of transcription in eucaryotic organisms. Mol Cell Biol 20: 429–440.

34. ZouZ, SahaTT, RoyS, ShinSW, BackmanTW, et al. (2013) Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression. Proc Natl Acad Sci USA 110: E2173–2181.

35. ShinSW, ZouZ, SahaTT, RaikhelAS (2012) bHLH-PAS heterodimer of methoprene-tolerant and Cycle mediates circadian expression of juvenile hormone-induced mosquito genes. Proc Natl Acad Sci USA 109: 16576–16581.

36. CuiY, SuiY, XuJ, ZhuF, PalliS (2014) Juvenile hormone regulates Aedes aegypti Krüppel homolog 1 through a conserved E box motif. Insect Biochem Mol Biol doi: 10.1016/j.ibmb.2014.05.009

37. BernardoTJ, DubrovskyEB (2012) The Drosophila juvenile hormone receptor candidates methoprene-tolerant (MET) and germ cell-expressed (GCE) utilize a conserved LIXXL motif to bind the FTZ-F1 nuclear receptor. J Biol Chem 287: 7821–7833.

38. DubrovskyEB, DubrovskayaVA, BernardoT, OtteV, DiFilippoR, et al. (2011) The Drosophila FTZ-F1 nuclear receptor mediates juvenile hormone activation of E75A gene expression through an intracellular pathway. J Biol Chem 286: 33689–33700.

39. GlinkaAV, WyattGR (1996) Juvenile hormone activation of gene transcription in locust fat body. Insect Biochem Mol Biol 26: 13–18.

40. EdwardsGC, BraunRP, WyattGR (1993) Induction of vitellogenin synthesis in Locusta migratoria by the juvenile-hormone analog, pyriproxyfen. J Insect Physiol 39: 609–614.

41. ComasD, PiulachsM-D, BellesX (2001) Induction of vitellogenin gene transcription in vitro by juvenile hormone in Blattella germanica. Mol Cell Endocrinol 183: 93–100.

42. ComasD, PiulachsMD, BellesX (1999) Fast induction of vitellogenin gene expression by juvenile hormone III in the cockroach Blattella germanica (L.) (Dictyoptera, Blattellidae). Insect Biochem Mol Biol 29: 821–827.

43. ShengZ, XuJ, BaiH, ZhuF, PalliSR (2011) Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum. J Biol Chem 286: 41924–41936.

44. HillR, BillasI, BonnetonF, GrahamL, LawrenceM (2013) Ecdysone receptors: from the Ashburner model to structural biology. Annu Rev Entomol 58: 251–271.

45. BonnetonF, BrunetFG, KathirithambyJ, LaudetV (2006) The rapid divergence of the ecdysone receptor is a synapomorphy for Mecopterida that clarifies the Strepsiptera problem. Insect Mol Biol 15: 351–362.

46. BonnetonF, ZelusD, IwemaT, Robinson-RechaviM, LaudetV (2003) Rapid divergence of the ecdysone receptor in Diptera and Lepidoptera suggests coevolution between ECR and USP-RXR. Mol Biol Evol 20: 541–553.

47. TrautweinMD, WiegmannBM, BeutelR, KjerKM, YeatesDK (2012) Advances in Insect phylogeny at the dawn of the postgenomic era. Annu Rev Entomol 57: 449–468.

48. GauntMW, MilesMA (2002) An Insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol 19: 748–761.

49. ZhouS, ZhangJ, HiraiM, ChinzeiY, KayserH, et al. (2002) A locust DNA-binding protein involved in gene regulation by juvenile hormone. Mol Cell Endocrinol 190: 177–185.

50. KethidiDR, PereraSC, ZhengS, FengQL, KrellP, et al. (2004) Identification and characterization of a juvenile hormone (JH) response region in the JH esterase gene from the spruce budworm, Choristoneura fumiferana. J Biol Chem 279: 19634–19642.

51. LiYP, ZhangZL, RobinsonGE, PalliSR (2007) Identification and characterization of a juvenile hormone response element and its binding proteins. J Biol Chem 282: 37605–37617.

52. MasaiH, MatsumotoS, YouZY, Yoshizawa-SugataN, OdaM (2010) Eukaryotic chromosome DNA replication: where, when, and how? Annu Rev Biochem 79: 89–130.

53. ChongJPJ, HayashiMK, SimonMN, XuRM, StillmanB (2000) A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc Natl Acad Sci USA 97: 1530–1535.

54. KanterDM, BruckI, KaplanDL (2008) Mcm subunits can assemble into two different active unwinding complexes. J Biol Chem 283: 31172–31182.

55. ZhangYR, XingYQ, ZhangL, MeiY, YamamotoK, et al. (2012) Regulation of cell cycle progression by forkhead transcription factor FOXO3 through its binding partner DNA replication factor Cdt1. Proc Natl Acad Sci USA 109: 5717–5722.

56. HongA, Narbonne-ReveauK, Riesgo-EscovarJ, FuHQ, AladjemMI, et al. (2007) The cyclin-dependent kinase inhibitor Dacapo promotes replication licensing during Drosophila endocycles. EMBO J 26: 2071–2082.

57. JacobsonAL, JohnstonJS, RotenbergD, WhitfieldAE, BoothW, et al. (2013) Genome size and ploidy of Thysanoptera. Insect Mol Biol 22: 12–17.

58. NordmanJ, Orr-WeaverTL (2012) Regulation of DNA replication during development. Development 139: 455–464.

59. BuntrockL, MarecF, KruegerS, TrautW (2012) Organ growth without cell division: somatic polyploidy in a moth, Ephestia kuehniella. Genome 55: 755–763.

60. LaPointeMC, KoeppeJK, NairKK (1985) Follicle cell polyploidy in Leucophaea maderae: Regulation by juvenile hormone. J Insect Physiol 31: 187–193.

61. NordmanJ, LiS, EngT, MacalpineD, Orr-WeaverTL (2011) Developmental control of the DNA replication and transcription programs. Genome Res 21: 175–181.

62. EdgarBA, Orr-WeaverTL (2001) Endoreplication Cell Cycles: More for Less. Cell 105: 297–306.

63. SunJJ, SmithL, ArmentoA, DengWM (2008) Regulation of the endocycle/gene amplification switch by Notch and ecdysone signaling. J Cell Biol 182: 885–896.

64. KoyamaT, IwamiM, SakuraiS (2004) Ecdysteroid control of cell cycle and cellular commitment in insect wing imaginal discs. Mol Cell Endocrinol 213: 155–166.

65. DeanRL, BollenbacherWE, LockeM, SmithSL, GilbertLI (1980) Haemolymph ecdysteroid levels and cellular events in the intermoult/moult sequence of Calpodes ethlius. J Insect Physiol 26: 267–280.

66. WielgusJJ, BollenbacherWE, GilbertLI (1979) Correlations between epidermal DNA synthesis and haemolymph ecdysteroid titre during the last larval instar of the tobacco hornworm, Manduca sexta. J Insect Physiol 25: 9–16.

67. LiTR, WhiteKP (2003) Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev cell 5: 59–72.

68. LiRQ, YuC, LiYR, LamTW, YiuSM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966–1967.

69. MortazaviA, WilliamsBA, MccueK, SchaefferL, WoldB (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628.

70. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.