The POU Factor Ventral Veins Lacking/Drifter Directs the Timing of Metamorphosis through Ecdysteroid and Juvenile Hormone Signaling
Hormones play major roles in initiating major developmental transitions, such as puberty and metamorphosis. However, how organisms coordinate changes across multiple hormones remains unclear. In this study, we show that silencing the POU domain transcription factor Ventral veins lacking (Vvl)/Drifter in the red flour beetle Tribolium castaneum leads to precocious metamorphosis and an inability to molt. We show that Vvl regulates the biosynthesis and signaling of two key insect developmental hormones, juvenile hormone (JH) and ecdysteroids. Vvl therefore appears to act as a potential central regulator of developmental timing by influencing two major hormones. Because POU factors are known as a major regulator of the onset of puberty, POU factors play a major role during sexual maturation in both vertebrates and insects.
Vyšlo v časopise:
The POU Factor Ventral Veins Lacking/Drifter Directs the Timing of Metamorphosis through Ecdysteroid and Juvenile Hormone Signaling. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004425
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004425
Souhrn
Hormones play major roles in initiating major developmental transitions, such as puberty and metamorphosis. However, how organisms coordinate changes across multiple hormones remains unclear. In this study, we show that silencing the POU domain transcription factor Ventral veins lacking (Vvl)/Drifter in the red flour beetle Tribolium castaneum leads to precocious metamorphosis and an inability to molt. We show that Vvl regulates the biosynthesis and signaling of two key insect developmental hormones, juvenile hormone (JH) and ecdysteroids. Vvl therefore appears to act as a potential central regulator of developmental timing by influencing two major hormones. Because POU factors are known as a major regulator of the onset of puberty, POU factors play a major role during sexual maturation in both vertebrates and insects.
Zdroje
1. TrumanJW, RiddifordLM (1974) Physiology of insect rhythms. 3. The temporal organization of the endocrine events underlying pupation of the tobacco hornworm. J Exp Biol 60: 371–382.
2. TrumanJW (1972) Physiology of insect rhythms. 1. Circadian organization of endocrine events underlying molting cycle of larval tobacco hornworms. J Exp Biol 57: 805–820.
3. Nijhout HF (1998) Insect Hormones. Princeton, NJ: Princeton University Press.
4. RoaJ, Garcia-GalianoD, CastellanoJM, GaytanF, PinillaL, et al. (2010) Metabolic control of puberty onset: new players, new mechanisms. Mol Cell Endocrinol 324: 87–94.
5. ClarksonJ, HanSK, LiuX, LeeK, HerbisonAE (2010) Neurobiological mechanisms underlying kisspeptin activation of gonadotropin-releasing hormone (GnRH) neurons at puberty. Mol Cell Endocrinol 324: 45–50.
6. McBrayerZ, OnoH, ShimellM, ParvyJP, BecksteadRB, et al. (2007) Prothoracicotropic hormone regulates developmental timing and body size in Drosophila. Dev Cell 13: 857–871.
7. AndersenB, RosenfeldMG (2001) POU domain factors in the neuroendocrine system: Lessons from developmental biology provide insights into human disease. Endocr Rev 22: 2–35.
8. RosenfeldMG (1991) Pou-domain transcription factors - pou-er-ful developmental regulators. Genes Dev 5: 897–907.
9. RamkumarT, AdlerS (1999) A requirement for the POU transcription factor, Brn-2, in corticotropin-releasing hormone expression in a neuronal cell line. Mol Endocrinol 13: 1237–1248.
10. WiermanME, XiongXY, KepaJK, SpauldingAJ, JacobsenBM, et al. (1997) Repression of gonadotropin-releasing hormone promoter activity by the POU homeodomain transcription factor SCIP/Oct-6/Tst-1: A regulatory mechanism of phenotype expression? Mol Cell Biol 17: 1652–1665.
11. EralySA, NelsonSB, HuangKM, MellonPL (1998) Oct-1 binds promoter elements required for transcription of the GnRH gene. Mol Endocrinol 12: 469–481.
12. ClarkME, MellonPL (1995) The POU homeodomain transcription factor Oct-1 is essential for activity of the gonadotropin-releasing hormone neuron-specific enhancer. Mol Cell Biol 15: 6169–6177.
13. OjedaSR, HillJ, HillDF, CostaME, TapiaV, et al. (1999) The Oct-2 POU domain gene in the neuroendocrine brain: A transcriptional regulator of mammalian puberty. Endocrinology 140: 3774–3789.
14. HerrW, ClearyMA (1995) The POU domain: versatility in transcriptional regulation by a flexible two-in-one DNA-binding domain. Genes Dev 9: 1679–1693.
15. OjedaSR, DubayC, LomnicziA, KaidarG, MatagneV, et al. (2010) Gene networks and the neuroendocrine regulation of puberty. Mol Cell Endocrinol 324: 3–11.
16. AndersonMG, PerkinsGL, ChittickP, ShrigleyRJ, JohnsonWA (1995) Drifter, a Drosophila Pou-domain transcription factor, is required for correct differentiation and migration of tracheal cells and midline glia. Genes Dev 9: 123–137.
17. MaY, CertelK, GaoYP, NiemitzE, MosherJ, et al. (2000) Functional interactions between Drosophila bHLH/PAS, Sox, and POU transcription factors regulate CNS midline expression of the slit gene. J Neurosci 20: 4596–4605.
18. CertelK, AndersonMG, ShrigleyRJ, WayneAJ (1996) Distinct variant DNA-Binding sites determine cell-specific autoregulated expression of the Drosophila POU domain transcription factor drifter in midline glia or trachea. Mol Cell Biol 16: 1813–1823.
19. InbalA, LevanonD, SalzbergA (2003) Multiple roles for u-turn/ventral veinless in the development of Drosophila PNS. Development 130: 2467–2478.
20. MeierS, SprecherSG, ReichertH, HirthF (2006) ventral veins lacking is required for specification of the tritocerebrum in embryonic brain development of Drosophila. Mech Dev 123: 76–83.
21. CertelSJ, ThorS (2004) Specification of Drosophila motoneuron identity by the combinatorial action of POU and LIM-HD factors. Development 131: 5429–5439.
22. AndersonMG, CertelSJ, CertelK, LeeT, MontellDJ, et al. (1996) Function of the Drosophila POU domain transcription factor Drifter as an upstream regulator of Breathless receptor tyrosine kinase expression in developing trachea. Development 122: 4169–4178.
23. ZhangTY, KangL, ZhangZF, XuWH (2004) Identification of a POU factor involved in regulating the neuron-specific expression of the gene encoding diapause hormone and pheromone biosynthesis-activating neuropeptide in Bombyx mori. Biochem J 380: 255–263.
24. ZhangTY, XuWH (2009) Identification and characterization of a POU transcription factor in the cotton bollworm, Helicoverpa armigera. BMC Mol Biol 10: 25 doi: 10.1186/1471-2199-10-25
25. Sanchez-HiguerasC, SotillosS, Castelli-Gair HombriaJ (2014) Common origin of insect trachea and endocrine organs from a segmentally repeated precursor. Curr Biol 24: 76–81.
26. GilbertLI, RybczynskiR, WarrenJT (2002) Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 47: 883–916.
27. WarrenJT, PetrykA, MarquesG, JarchoM, ParvyJP, et al. (2002) Molecular and biochemical characterization of two P450 enzymes in the ecdysteroidogenic pathway of Drosophila melanogaster. Proc Natl Acad Sci U S A 99: 11043–11048.
28. WarrenJT, SakuraiS, RountreeDB, GilbertLI, LeeSS, et al. (1988) Regulation of the ecdysteroid titer of Manduca-sexta - reappraisal of the role of the prothoracic glands. Proc Natl Acad Sci U S A 85: 958–962.
29. AribiN, PitoizetN, QuennedeyA, DelbecqueJP (1997) 2-deoxyecdysone is a circulating ecdysteroid in the beetle Zophobas atratus. Biochem Biophys Acta 1335: 246–252.
30. NijhoutHF, WilliamsCM (1974) Control of molting and metamorphosis in tobacco hornworm, Manduca sexta (L): Growth of last-instar larva and decision to pupate. J Exp Biol 61: 481–491.
31. MirthC, TrumanJW, RiddifordLM (2005) The role of the prothoracic gland in determining critical weight to metamorphosis in Drosophila melanogaster. Curr Biol 15: 1796–1807.
32. Smith WA, Rybczynski R (2011) Prothoracicotropic hormone. In: Gilbert LI, editor. Insect Endocrinology. New York: Academic Press. pp. 1–62.
33. RewitzKF, O'ConnorMB, GilbertLI (2007) Molecular evolution of the insect Halloween family of cytochrome P450s: Phylogeny, gene organization and functional conservation. Insect Biochem Mol Biol 37: 741–753.
34. WalkiewiczMA, SternM (2009) Increased insulin/insulin growth factor signaling advances the onset of metamorphosis in Drosophila. PLoS ONE 4(4): e5072 doi:10.1371/journal.pone.0005072
35. HentzeJL, MoellerME, JorgensenAF, BengtssonMS, BordoyAM, et al. (2013) Accessory gland as a site for prothoracicotropic hormone controlled ecdysone synthesis in adult male insects. PLoS ONE 8(2): e55131 doi:10.1371/journal.pone.0055131
36. PetrykA, WarrenJT, MarquesG, JarchoMP, GilbertLI, et al. (2003) Shade is the Drosophila P450 enzyme that mediates the hydroxylation of ecdysone to the steroid insect molting hormone 20-hydroxyecdysone. Proc Natl Acad Sci U S A 100: 13773–13778.
37. HallBL, ThummelCS (1998) The RXR homolog Ultraspiracle is an essential component of the Drosophila ecdysone receptor. Development 125: 4709–4717.
38. LiTR, BenderM (2000) A conditional rescue system reveals essential functions for the ecdysone receptor (EcR) gene during molting and metamorphosis in Drosophila. Development 127: 2897–2905.
39. MartinD, MaestroO, CruzJ, Mane-PadrosD, BellesX (2006) RNAi studies reveal a conserved role for RXR in molting in the cockroach Blattella germanica. J Insect Physiol 52: 410–416.
40. TanA, PalliSR (2008) Edysone receptor isoforms play distinct roles in controlling molting and metamorphosis in the red flour beetle, Tribolium castaneum. Mol Cell Endocrinol 291: 42–49.
41. SegravesWA, HognessDS (1990) The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev 4: 204–219.
42. BurtisKC, ThummelCS, JonesCW, KarimFD, HognessDS (1990) The Drosophila 74EF early puff contains E74, a complex ecdysone-inducible gene that encodes two ets-related proteins. Cell 61: 85–99.
43. King-JonesK, ThummelCS (2005) Nuclear receptors - a perspective from Drosophila. Nat Rev Genet 6: 311–323.
44. ThummelCS (1995) From embryogenesis to metamorphosis: the regulation and function of Drosophila nuclear receptor superfamily members. Cell 83: 871–877.
45. LamGT, JiangC, ThummelCS (1997) Coordination of larval and prepupal gene expression by the DHR3 orphan receptor during Drosophila metamorphosis. Development 124: 1757–1769.
46. HuetF, RuizC, RichardsG (1995) Sequential gene activation by ecdysone in Drosophila melanogaster: the hierarchical equivalence of early and early late genes. Development 121: 1195–1204.
47. LamG, HallBL, BenderM, ThummelCS (1999) DHR3 is required for the prepupal-pupal transition and differentiation of adult structures during Drosophila metamorphosis. Dev Biol 212: 204–216.
48. TanA, PalliSR (2008) Identification and characterization of nuclear receptors from the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 38: 430–439.
49. FletcherJC, BurtisKC, HognessDS, ThummelCS (1995) The Drosophila E74 gene is required for metamorphosis and plays a role in the polytene chromosome puffing response to ecdysone. Development 121: 1455–1465.
50. NijhoutHF, WilliamsCM (1974) Control of molting and metamorphosis in tobacco hornworm, Manduca sexta (L): Cessation of juvenile hormone secretion as a trigger for pupation. J Exp Biol 61: 493–501.
51. RiddifordLM (1996) Juvenile hormone: The status of its “status quo” action. Arch Insect Biochem Physiol 32: 271–286.
52. Goodman WG, Granger NA, Editors-in-Chief: Lawrence IG, Kostas I, Sarjeet SG(2005) The Juvenile Hormones. Comprehensive Molecular Insect Science. Amsterdam: Elsevier. pp. 319–408.
53. FutahashiR, FujiwaraH (2008) Juvenile hormone regulates butterfly larval pattern switches. Science 319: 1061–1061.
54. SuzukiY, TrumanJW, RiddifordLM (2008) The role of broad in the development of Tribolium castaneum: implications for the evolution of the holometabolous insect pupa. Development 135: 569–577.
55. WilliamsCM (1961) The juvenile hormone. II. Its role in the endocrine control of molting, pupation, and adult development in the Cecropia silkworm. Biol Bull 121: 572–585.
56. KamimuraM, KiuchiM (2002) Applying fenoxycarb at the penultimate instar triggers an additional ecdysteroid surge and induces perfect extra larval molting in the silkworm. Gen Comp Endocrinol 128: 231–237.
57. FukudaS (1944) The hormonal mechanism of larval molting and metamorphosis in the silkworm. J Fac Sci Tokyo Imp Univ 4: 477–532.
58. 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 U S A 109: 11729–11734.
59. KonopovaB, JindraM (2007) Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. Proc Natl Acad Sci U S A 104: 10488–10493.
60. CharlesJP, IwemaT, EpaVC, TakakiK, RynesJ, et al. (2011) Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc Natl Acad Sci U S A 108: 21128–21133.
61. ParthasarathyR, TanAJ, PalliSR (2008) bHLH-PAS family transcription factor methoprene-tolerant plays a key role in JH action in preventing the premature development of adult structures during larval-pupal metamorphosis. Mech Dev 125: 601–616.
62. KonopovaB, JindraM (2008) Broad-complex acts downstream of Met in juvenile hormone signaling to coordinate primitive Holometabolan metamorphosis. Development 135: 559–568.
63. MinakuchiC, NamikiT, YoshiyamaM, ShinodaT (2008) RNAi-mediated knockdown of juvenile hormone acid O-methyltransferase gene causes precocious metamorphosis in the red flour beetle Tribolium castaneum. FEBS J 275: 2919–2931.
64. KinjohT, KanekoY, ItoyamaK, MitaK, HirumaK, et al. (2007) Control of juvenile hormone biosynthesis in Bombyx mori: Cloning of the enzymes in the mevalonate pathway and assessment of their developmental expression in the corpora allata. Insect Biochem Mol Biol 37: 808–818.
65. RiddifordLM, AshburnerM (1991) Effects of juvenile hormone mimics on larval development and metamorphosis of Drosophila melanogaster. Gen Comp Endocrinol 82: 172–183.
66. BurnsKA, GutzwillerLM, TomoyasuY, GebeleinB (2012) Oenocyte development in the red flour beetle Tribolium castaneum. Dev Genes Evol 222: 77–88.
67. RomerF, EmmerichH, NowockJ (1974) Biosynthesis of ecdysones in isolated prothoracic glands and oenocytes of Tenebrio molitor in vitro. J Insect Physiol 20: 1975–1987.
68. DelbecqueJP, WeidnerK, HoffmannKH (1990) Alternative sites for ecdysteroid production in insects. Inv Rep Dev 18: 29–42.
69. SrivastavaUS (1958) Prothoracic glands in Tenebrio molitor L. (Coleoptera: Tenebrionidae). Nature 181: 1668–1668.
70. ParthasarathyR, TanA, SunZ, ChenZ, RankinM, et al. (2009) Juvenile hormone regulation of male accessory gland activity in the red flour beetle, Tribolium castaneum. Mech Dev 126: 563–579.
71. MinakuchiC, NamikiT, ShinodaT (2009) Krüppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Dev Biol 325: 341–350.
72. DengHM, ZhangJL, LiY, ZhengSC, LiuL, et al. (2012) Homeodomain POU and Abd-A proteins regulate the transcription of pupal genes during metamorphosis of the silkworm, Bombyx mori. Proc Natl Acad Sci U S A 109: 12598–12603.
73. DelbecqueJP, MeisterMF, QuennedeyA (1986) Conversion of radiolabelled 2,22,25-tri-deoxyecdysone in Tenebrio pupae. Insect Biochem 16: 57–63.
74. EwerJ, GammieSC, TrumanJW (1997) Control of insect ecdysis by a positive-feedback endocrine system: Roles of eclosion hormone and ecdysis triggering hormone. J Exp Biol 200: 869–881.
75. ParkY, FilippovV, GillSS, AdamsME (2002) Deletion of the ecdysis-triggering hormone gene leads to lethal ecdysis deficiency. Development 129: 493–503.
76. ParkY, ZitnanD, GillSJ, AdamsME (1999) Molecular cloning and biological activity of ecdysis-triggering hormones in Drosophila melanogaster. FEBS Lett 463: 133–138.
77. ZitnanD, ZitnanovaI, SpalovskaI, TakacP, ParkY, et al. (2003) Conservation of ecdysis-triggering hormone signalling in insects. J Exp Biol 206: 1275–1289.
78. ZitnanD, KinganTG, HermesmanJL, AdamsME (1996) Identification of ecdysis-triggering hormone from an epitracheal endocrine system. Science 271: 88–91.
79. GauthierSA, HewesRS (2006) Transcriptional regulation of neuropeptide and peptide hormone expression by the Drosophila dimmed and cryptocephal genes. J Exp Biol 209: 1803–1815.
80. GauthierSA, VanHaaftenE, CherbasL, CherbasP, HewesRS (2012) Cryptocephal, the Drosophila melanogaster ATF4, is a specific coactivator for ecdysone receptor isoform B2. PLoS Genetics 8(8): e1002883 doi:10.1371/journal.pgen.1002883
81. GrilloM, CasanovaJ, AverofM (2014) Development: a deep breath for endocrine organ evolution. Curr Biol 24: R38–40.
82. TraunerJ, SchinkoJ, LorenzenMD, ShippyTD, WimmerEA, et al. (2009) Large-scale insertional mutagenesis of a coleopteran stored grain pest, the red flour beetle Tribolium castaneum, identifies embryonic lethal mutations and enhancer traps. BMC Biol 7: 73.
83. HughesCL, KaufmanTC (2000) RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the Hemipteran head. Development 127: 3683–3694.
84. WarrenJT, SmithW, GilbertLI (1984) Simplification of the ecdysteroid radioimmunoassay by the use of protein A from Staphylococcus aureus. Experientia 40: 393–394.
85. SuzukiY, SquiresDC, RiddifordLM (2009) Larval leg integrity is maintained by Distal-less and is required for proper timing of metamorphosis in the flour beetle, Tribolium castaneum. Dev Biol 326: 60–67.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2014 Číslo 6
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Early Back-to-Africa Migration into the Horn of Africa
- PINK1-Mediated Phosphorylation of Parkin Boosts Parkin Activity in
- OsHUS1 Facilitates Accurate Meiotic Recombination in Rice
- An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICE in B13