Modulators of hormonal response regulate temporal fate specification in the Drosophila brain

English version

Autoři: Giovanni Marchetti ^aff001; Gaia Tavosanis ^aff001
Působiště autorů: Dynamics of neuronal circuits, German Center for Neurodegenerative Diseases (DZNE), Germany ^aff001; LIMES-Institute, University of Bonn, Germany ^aff002
Vyšlo v časopise: Modulators of hormonal response regulate temporal fate specification in the Drosophila brain. PLoS Genet 15(12): e32767. doi:10.1371/journal.pgen.1008491
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008491

Souhrn

Neuronal diversity is at the core of the complex processing operated by the nervous system supporting fundamental functions such as sensory perception, motor control or memory formation. A small number of progenitors guarantee the production of this neuronal diversity, with each progenitor giving origin to different neuronal types over time. How a progenitor sequentially produces neurons of different fates and the impact of extrinsic signals conveying information about developmental progress or environmental conditions, on this process represent a key, but elusive questions. Each of the four progenitors of the Drosophila mushroom body (MB) sequentially gives rise to the MB neuron subtypes. The temporal fate determination pattern of MB neurons can be influenced by extrinsic cues, conveyed by the steroid hormone ecdysone. Here, we show that the activation of Transforming Growth Factor-β (TGF-β) signalling via glial-derived Myoglianin regulates the fate transition between the early-born α’β’ and the pioneer αβ MB neurons by promoting the expression of the ecdysone receptor B1 isoform (EcR-B1). While TGF-β signalling is required in MB neuronal progenitors to promote the expression of EcR-B1, ecdysone signalling acts postmitotically to consolidate theα’β’ MB fate. Indeed, we propose that if these signalling cascades are impaired α’β’ neurons lose their fate and convert to pioneer αβ. Conversely, an intrinsic signal conducted by the zinc finger transcription factor Krüppel-homolog 1 (Kr-h1) antagonises TGF-β signalling and acts as negative regulator of the response mediated by ecdysone in promoting α’β’ MB neuron fate consolidation. Taken together, the consolidation of α’β’ MB neuron fate requires the response of progenitors to local signalling to enable postmitotic neurons to sense a systemic signal.

Klíčová slova:

Cell staining – Metamorphosis – Neurons – RNA interference – Vision – Neuroblasts – Hormone receptor signaling

Zdroje

1. Kohwi M, Doe CQ. Temporal fate specification and neural progenitor competence during development. Nat Rev Neurosci. 2013;14(12):823–38. doi: 10.1038/nrn3618 24400340

2. Doe CQ. Temporal Patterning in the Drosophila CNS. Annu Rev Cell Dev Biol. 2017;33:219–40. doi: 10.1146/annurev-cellbio-111315-125210 28992439

3. Okano H, Temple S. Cell types to order: temporal specification of CNS stem cells. Curr Opin Neurobiol. 2009;19(2):112–9. doi: 10.1016/j.conb.2009.04.003 19427192

4. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, et al. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci. 2006;9(6):743–51. doi: 10.1038/nn1694 16680166

5. Marchetti G, Tavosanis G. Steroid Hormone Ecdysone Signaling Specifies Mushroom Body Neuron Sequential Fate via Chinmo. Curr Biol. 2017;27(19):3017–24 e4. doi: 10.1016/j.cub.2017.08.037 28966087

6. Syed MH, Mark B, Doe CQ. Steroid hormone induction of temporal gene expression in Drosophila brain neuroblasts generates neuronal and glial diversity. Elife. 2017;6.

7. Heisenberg M. Mushroom body memoir: from maps to models. Nat Rev Neurosci. 2003;4(4):266–75. doi: 10.1038/nrn1074 12671643

8. Lee T, Lee A, Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development. 1999;126(18):4065–76. 10457015

9. Danielsen ET, Moeller ME, Rewitz KF. Nutrient signaling and developmental timing of maturation. Curr Top Dev Biol. 2013;105:37–67. doi: 10.1016/B978-0-12-396968-2.00002-6 23962838

10. Zheng X, Wang J, Haerry TE, Wu AY, Martin J, O'Connor MB, et al. TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell.

11. Pfeiffer BD, Ngo TT, Hibbard KL, Murphy C, Jenett A, Truman JW, et al. Refinement of tools for targeted gene expression in Drosophila. Genetics. 2010;186(2):735–55. doi: 10.1534/genetics.110.119917 20697123

12. Kraft KF, Massey EM, Kolb D, Walldorf U, Urbach R. Retinal homeobox promotes cell growth, proliferation and survival of mushroom body neuroblasts in the Drosophila brain. Mech Dev. 2016;142:50–61. doi: 10.1016/j.mod.2016.07.003 27455861

13. Wu JS, Luo L. A protocol for mosaic analysis with a repressible cell marker (MARCM) in Drosophila. Nat Protoc. 2006;1(6):2583–9. doi: 10.1038/nprot.2006.320 17406512

14. McGuire SE, Mao Z, Davis RL. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE. 2004;2004(220):pl6. doi: 10.1126/stke.2202004pl6 14970377

15. Zhu S, Lin S, Kao CF, Awasaki T, Chiang AS, Lee T. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell. 2006;127(2):409–22. doi: 10.1016/j.cell.2006.08.045 17055440

16. Kucherenko MM, Barth J, Fiala A, Shcherbata HR. Steroid-induced microRNA let-7 acts as a spatio-temporal code for neuronal cell fate in the developing Drosophila brain. EMBO J. 2012;31(24):4511–23. doi: 10.1038/emboj.2012.298 23160410

17. Yang L, Titlow J, Ennis D, Smith C, Mitchell J, Young FL, et al. Single molecule fluorescence in situ hybridisation for quantitating post-transcriptional regulation in Drosophila brains. Methods.

18. Neumuller RA, Richter C, Fischer A, Novatchkova M, Neumuller KG, Knoblich JA. Genome-wide analysis of self-renewal in Drosophila neural stem cells by transgenic RNAi. Cell Stem Cell.

19. Truman JW, Talbot WS, Fahrbach SE, Hogness DS. Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development. 1994;120(1):219–34. 8119129

20. Awasaki T, Huang Y, O'Connor MB, Lee T. Glia instruct developmental neuronal remodeling through TGF-beta signaling. Nat Neurosci. 2011;14(7):821–3. doi: 10.1038/nn.2833 21685919

21. Beck Y, Pecasse F, Richards G. Kruppel-homolog is essential for the coordination of regulatory gene hierarchies in early Drosophila development. Dev Biol. 2004;268(1):64–75. doi: 10.1016/j.ydbio.2003.12.017 15031105

22. Pecasse F, Beck Y, Ruiz C, Richards G. Kruppel-homolog, a stage-specific modulator of the prepupal ecdysone response, is essential for Drosophila metamorphosis. Dev Biol. 2000;221(1):53–67. doi: 10.1006/dbio.2000.9687 10772791

23. Shi L, Lin S, Grinberg Y, Beck Y, Grozinger CM, Robinson GE, et al. Roles of Drosophila Kruppel-homolog 1 in neuronal morphogenesis. Dev Neurobiol. 2007;67(12):1614–26. 17562531

24. Alyagor I, Berkun V, Keren-Shaul H, Marmor-Kollet N, David E, Mayseless O, et al. Combining Developmental and Perturbation-Seq Uncovers Transcriptional Modules Orchestrating Neuronal Remodeling. Dev Cell. 2018;47(1):38–52 e6. doi: 10.1016/j.devcel.2018.09.013 30300589

25. Minakuchi C, Zhou X, Riddiford LM. Kruppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev. 2008;125(1–2):91–105. doi: 10.1016/j.mod.2007.10.002 18036785

26. Dias JM, Alekseenko Z, Applequist JM, Ericson J. Tgfbeta signaling regulates temporal neurogenesis and potency of neural stem cells in the CNS. Neuron. 2014;84(5):927–39. doi: 10.1016/j.neuron.2014.10.033 25467979

27. Zheng X, Zugates CT, Lu Z, Shi L, Bai JM, Lee T. Baboon/dSmad2 TGF-beta signaling is required during late larval stage for development of adult-specific neurons. EMBO J. 2006;25(3):615–27. doi: 10.1038/sj.emboj.7600962 16437159

28. Pauls D, Selcho M, Gendre N, Stocker RF, Thum AS. Drosophila larvae establish appetitive olfactory memories via mushroom body neurons of embryonic origin. J Neurosci. 2010;30(32):10655–66. doi: 10.1523/JNEUROSCI.1281-10.2010 20702697

29. Arber S, Han B, Mendelsohn M, Smith M, Jessell TM, Sockanathan S. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron. 1999;23(4):659–74. doi: 10.1016/s0896-6273(01)80026-x 10482234

30. Thaler J, Harrison K, Sharma K, Lettieri K, Kehrl J, Pfaff SL. Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron. 1999;23(4):675–87. doi: 10.1016/s0896-6273(01)80027-1 10482235

31. Choi J, Park S, Sockanathan S. Activated retinoid receptors are required for the migration and fate maintenance of subsets of cortical neurons. Development. 2014;141(5):1151–60. doi: 10.1242/dev.104505 24504337

32. Yaron A, Sprinzak D. The cis side of juxtacrine signaling: a new role in the development of the nervous system. Trends Neurosci. 2012;35(4):230–9. doi: 10.1016/j.tins.2011.12.003 22222351

33. Bray SJ. Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol. 2006;7(9):678–89. doi: 10.1038/nrm2009 16921404

34. Liu S, Li K, Gao Y, Liu X, Chen W, Ge W, et al. Antagonistic actions of juvenile hormone and 20-hydroxyecdysone within the ring gland determine developmental transitions in Drosophila. Proc Natl Acad Sci U S A. 2018;115(1):139–44. doi: 10.1073/pnas.1716897115 29255055

35. Santos CG, Fernandez-Nicolas A, Belles X. Smads and insect hemimetabolan metamorphosis. Dev Biol. 2016;417(1):104–13. doi: 10.1016/j.ydbio.2016.07.006 27452629

36. Gesualdi SC, Haerry TE. Distinct signaling of Drosophila Activin/TGF-beta family members. Fly (Austin). 2007;1(4):212–21.

37. Beckwith EJ, Gorostiza EA, Berni J, Rezaval C, Perez-Santangelo A, Nadra AD, Ceriani MF. Circadian period integrates network information through activation of the BMP signaling pathway. PLoS Biol, 2013. 11(12): p. e1001733. doi: 10.1371/journal.pbio.1001733 24339749

38. Langerak S, Kim MJ, Lamberg H, Godinez M, Main M, Winslow L, O’Connor MB, Zhu CC. The Drosophila TGF-beta/Activin-like ligands Dawdle and Myoglianin appear to modulate adult lifespan through regulation of 26S proteasome function in adult muscle. Biol Open, 2018. 7(4).

39. Wells BS, Pistillo D, Barnhart E, Desplan C. Parallel Activin and BMP signaling coordinates R7/R8 photoreceptor subtype pairing in the stochastic Drosophila retina. Elife, 2017. 6.

40. Wu YC, Chen CH, Mercer A, Sokol NS. Let-7-complex microRNAs regulate the temporal identity of Drosophila mushroom body neurons via chinmo. Dev Cell. 2012;23(1):202–9. doi: 10.1016/j.devcel.2012.05.013 22814608

41. Sugimura K, Satoh D, Estes P, Crews S, Uemura T. Development of morphological diversity of dendrites in Drosophila by the BTB-zinc finger protein abrupt. Neuron. 2004;43(6):809–22. doi: 10.1016/j.neuron.2004.08.016 15363392

42. Gavet O, Pines J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev Cell. 2010;18(4):533–43. doi: 10.1016/j.devcel.2010.02.013 20412769

43. Sommer C, Strähle C, Köthe U, Hamprecht A. in: Eighth IEEE International Symposium on Biomedical Imaging (ISBI). Proceedings. 2011;533–43.