Temporal Patterning of Neural Progenitors in Drosophila

Overview

Journal Curr Top Dev Biol

Publisher Elsevier

Specialties Biology
Reproductive Medicine

Date 2013 Aug 22

PMID 23962839

Citations 44

Authors

Xin Li

Zhenqing Chen

Claude Desplan

Affiliations

Soon will be listed here.

Abstract

Drosophila has recently become a powerful model system to understand the mechanisms of temporal patterning of neural progenitors called neuroblasts (NBs). Two different temporal sequences of transcription factors (TFs) have been found to be sequentially expressed in NBs of two different systems: the Hunchback, Krüppel, Pdm1/Pdm2, Castor, and Grainyhead sequence in the Drosophila ventral nerve cord; and the Homothorax, Klumpfuss, Eyeless, Sloppy-paired, Dichaete, and Tailless sequence that patterns medulla NBs. In addition, the intermediate neural progenitors of type II NB lineages are patterned by a different sequence: Dichaete, Grainyhead, and Eyeless. These three examples suggest that temporal patterning of neural precursors by sequences of TFs is a common theme to generate neural diversity. Cross-regulations, including negative feedback regulation and positive feedforward regulation among the temporal factors, can facilitate the progression of the sequence. However, there are many remaining questions to understand the mechanism of temporal transitions. The temporal sequence progression is intimately linked to the progressive restriction of NB competence, and eventually determines the end of neurogenesis. Temporal identity has to be integrated with spatial identity information, as well as with the Notch-dependent binary fate choices, in order to generate specific neuron fates.

Citing Articles

Fate specification is spatially intermingled across planarian stem cells.

Park C, Owusu-Boaitey K, Valdes G, Reddien P Nat Commun. 2023; 14(1):7422.

PMID: 37973979 PMC: 10654723. DOI: 10.1038/s41467-023-43267-2.

A circular RNA Edis-Relish-castor axis regulates neuronal development in Drosophila.

Liu W, Liang W, Xiong X, Li J, Zhou R PLoS Genet. 2022; 18(10):e1010433.

PMID: 36301831 PMC: 9612563. DOI: 10.1371/journal.pgen.1010433.

Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in .

Bostock M, Prasad A, Donoghue A, Fernandes V Elife. 2022; 11.

PMID: 36004721 PMC: 9507128. DOI: 10.7554/eLife.78093.

Post-transcriptional regulation of transcription factor codes in immature neurons drives neuronal diversity.

Guan W, Bellemin S, Bouchet M, Venkatasubramanian L, Guillermin C, Laurencon A Cell Rep. 2022; 39(13):110992.

PMID: 35767953 PMC: 9479746. DOI: 10.1016/j.celrep.2022.110992.

Hunchback prevents notch-induced apoptosis in the serotonergic lineage of Drosophila Melanogaster.

Perez E, Venkatanarayan A, Lundell M Dev Biol. 2022; 486:109-120.

PMID: 35381219 PMC: 9260952. DOI: 10.1016/j.ydbio.2022.03.012.

References

Naka H, Nakamura S, Shimazaki T, Okano H . Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development. Nat Neurosci. 2009; 11(9):1014-23. DOI: 10.1038/nn.2168. View

Tran K, Miller M, Doe C . Recombineering Hunchback identifies two conserved domains required to maintain neuroblast competence and specify early-born neuronal identity. Development. 2010; 137(9):1421-30. PMC: 2853844. DOI: 10.1242/dev.048678. View

Mellerick D, Kassis J, Zhang S, Odenwald W . castor encodes a novel zinc finger protein required for the development of a subset of CNS neurons in Drosophila. Neuron. 1992; 9(5):789-803. DOI: 10.1016/0896-6273(92)90234-5. View

Cenci C, Gould A . Drosophila Grainyhead specifies late programmes of neural proliferation by regulating the mitotic activity and Hox-dependent apoptosis of neuroblasts. Development. 2005; 132(17):3835-45. DOI: 10.1242/dev.01932. View

Schmid A, Chiba A, Doe C . Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development. 1999; 126(21):4653-89. DOI: 10.1242/dev.126.21.4653. View

Schuldt A, Brand A . Mastermind acts downstream of notch to specify neuronal cell fates in the Drosophila central nervous system. Dev Biol. 1999; 205(2):287-95. DOI: 10.1006/dbio.1998.9014. View

Das A, Reichert H, Rodrigues V . Notch regulates the generation of diverse cell types from the lateral lineage of Drosophila antennal lobe. J Neurogenet. 2010; 24(1):42-53. DOI: 10.3109/01677060903582202. View

Yu H, Chen C, Shi L, Huang Y, Lee T . Twin-spot MARCM to reveal the developmental origin and identity of neurons. Nat Neurosci. 2009; 12(7):947-53. PMC: 2701974. DOI: 10.1038/nn.2345. View

Kambadur R, Koizumi K, Stivers C, Nagle J, Poole S, Odenwald W . Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev. 1998; 12(2):246-60. PMC: 316437. DOI: 10.1101/gad.12.2.246. View

10.

Yu H, Kao C, He Y, Ding P, Kao J, Lee T . A complete developmental sequence of a Drosophila neuronal lineage as revealed by twin-spot MARCM. PLoS Biol. 2010; 8(8). PMC: 2927434. DOI: 10.1371/journal.pbio.1000461. View

11.

Li X, Erclik T, Bertet C, Chen Z, Voutev R, Venkatesh S . Temporal patterning of Drosophila medulla neuroblasts controls neural fates. Nature. 2013; 498(7455):456-62. PMC: 3701960. DOI: 10.1038/nature12319. View

12.

Bayraktar O, Boone J, Drummond M, Doe C . Drosophila type II neuroblast lineages keep Prospero levels low to generate large clones that contribute to the adult brain central complex. Neural Dev. 2010; 5:26. PMC: 2958855. DOI: 10.1186/1749-8104-5-26. View

13.

White K, Kankel D . Patterns of cell division and cell movement in the formation of the imaginal nervous system in Drosophila melanogaster. Dev Biol. 1978; 65(2):296-321. DOI: 10.1016/0012-1606(78)90029-5. View

14.

Lundell M, Hirsh J . eagle is required for the specification of serotonin neurons and other neuroblast 7-3 progeny in the Drosophila CNS. Development. 1998; 125(3):463-72. DOI: 10.1242/dev.125.3.463. View

15.

Wu Y, Chen C, Mercer A, Sokol N . Let-7-complex microRNAs regulate the temporal identity of Drosophila mushroom body neurons via chinmo. Dev Cell. 2012; 23(1):202-9. PMC: 3401410. DOI: 10.1016/j.devcel.2012.05.013. View

16.

Truman J, Moats W, Altman J, Marin E, Williams D . Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster. Development. 2009; 137(1):53-61. PMC: 2796924. DOI: 10.1242/dev.041749. View

17.

Buescher M, Yeo S, Udolph G, Zavortink M, Yang X, Tear G . Binary sibling neuronal cell fate decisions in the Drosophila embryonic central nervous system are nonstochastic and require inscuteable-mediated asymmetry of ganglion mother cells. Genes Dev. 1998; 12(12):1858-70. PMC: 316905. DOI: 10.1101/gad.12.12.1858. View

18.

Kao C, Yu H, He Y, Kao J, Lee T . Hierarchical deployment of factors regulating temporal fate in a diverse neuronal lineage of the Drosophila central brain. Neuron. 2012; 73(4):677-84. PMC: 3566789. DOI: 10.1016/j.neuron.2011.12.018. View

19.

Baumgardt M, Miguel-Aliaga I, Karlsson D, Ekman H, Thor S . Specification of neuronal identities by feedforward combinatorial coding. PLoS Biol. 2007; 5(2):e37. PMC: 1790951. DOI: 10.1371/journal.pbio.0050037. View

20.

Spana E, Doe C . Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron. 1996; 17(1):21-6. DOI: 10.1016/s0896-6273(00)80277-9. View