Steroid hormone-dependent transformation of<i>polyhomeotic</i>mutant neurons in the<i>Drosophila</i>brain

Wang, Jian; Lee, Ching-Hsien J.; Lin, Suewei; Lee, Tzumin

doi:10.1242/dev.02299

Cited by 24 publications

(24 citation statements)

References 68 publications

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“…Thus, the effects of PcG gene loss on neurogenesis are context-dependent and differ during embryonic development as compared with postembryonic development. This is underscored in recent work which indicates that the PcG gene ph is essential for maintaining neuronal identity and diversity during metamorphosis (Wang et al, 2006).…”

Section: Research Articlementioning

confidence: 97%

“…Although many aspects of PcG gene Polycomb group genes are required for neural stem cell survival in postembryonic neurogenesis of Drosophila structure and function are conserved from flies to mammals, little is known about the roles of PcG genes in neuronal developmental processes in Drosophila. In ph mutants, global misrouting of CNS axons and ecdysone-dependent loss of neuronal subtype identity during metamorphosis have been reported (Smouse and Perrimon, 1990;Wang et al, 2006). However, there is currently little evidence for a role of PcG genes in neural stem cell fate or neuronal proliferation in Drosophila.…”

Section: Introductionmentioning

confidence: 99%

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Polycomb group genes are required for neural stem cell survival in postembryonic neurogenesis ofDrosophila

2007

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Genes of the Polycomb group (PcG) are part of a cellular memory system that maintains appropriate inactive states of Hox gene expression in Drosophila. Here, we investigate the role of PcG genes in postembryonic development of the Drosophila CNS. We use mosaic-based MARCM techniques to analyze the role of these genes in the persistent larval neuroblasts and progeny of the central brain and thoracic ganglia. We find that proliferation in postembryonic neuroblast clones is dramatically reduced in the absence of Polycomb, Sex combs extra, Sex combs on midleg, Enhancer of zeste or Suppressor of zeste 12. The proliferation defects in these PcG mutants are due to the loss of neuroblasts by apoptosis in the mutant clones. Mutation of PcG genes in postembryonic lineages results in the ectopic expression of posterior Hox genes, and experimentally induced misexpression of posterior Hox genes, which in the wild type causes neuroblast death, mimics the PcG loss-of-function phenotype. Significantly, full restoration of wild-type-like properties in the PcG mutant lineages is achieved by blocking apoptosis in the neuroblast clones. These findings indicate that loss of PcG genes leads to aberrant derepression of posterior Hox gene expression in postembryonic neuroblasts, which causes neuroblast death and termination of proliferation in the mutant clones. Our findings demonstrate that PcG genes are essential for normal neuroblast survival in the postembryonic CNS of Drosophila. Moreover, together with data on mammalian PcG genes, they imply that repression of aberrant reactivation of Hox genes may be a general and evolutionarily conserved role for PcG genes in CNS development.

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Section: Research Articlementioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Polycomb group genes are required for neural stem cell survival in postembryonic neurogenesis ofDrosophila

2007

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“…Studies of the expression patterns of PcG genes and the consequences of overexpression of PcG genes suggest that PcG genes may affect the patterning of the vertebrate CNS along the anterior-posterior (AP) axis, analogous to their functions in specifying the body plan (Barnett et al 2001;Kitaguchi et al 2001;Kwon and Chung 2003). A recent study demonstrates that the PcG gene Polyhomeotic regulates aspects of neuronal diversity in the Drosophila CNS (Wang et al 2006). Our study now links the function of PcG genes to maintenance of dendritic coverage of class IV sensory neurons.…”

Section: A Role For Polycomb Group Genes In Neuronal Developmentmentioning

confidence: 99%

Polycomb genes interact with the tumor suppressor genes hippo and warts in the maintenance of Drosophila sensory neuron dendrites

Parrish¹,

Emoto²,

Jan³

2007

Genes Dev.

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Dendritic fields are important determinants of neuronal function. However, how neurons establish and then maintain their dendritic fields is not well understood. Here we show that Polycomb group (PcG) genes are required for maintenance of complete and nonoverlapping dendritic coverage of the larval body wall by Drosophila class IV dendrite arborization (da) neurons. In esc, Su(z)12, or Pc mutants, dendritic fields are established normally, but class IV neurons display a gradual loss of dendritic coverage, while axons remain normal in appearance, demonstrating that PcG genes are specifically required for dendrite maintenance. Both multiprotein Polycomb repressor complexes (PRCs) involved in transcriptional silencing are implicated in regulation of dendrite arborization in class IV da neurons, likely through regulation of homeobox (Hox) transcription factors. We further show genetic interactions and association between PcG proteins and the tumor suppressor kinase Warts (Wts), providing evidence for their cooperation in multiple developmental processes including dendrite maintenance.[Keywords: Drosophila; neuron; dendrite; Polycomb; homeobox; tumor suppressor] Supplemental material is available at http://www.genesdev.org. Received November 20, 2006; revised version accepted February 26, 2007. Dendrite arborization patterns are important for neuronal function and proper wiring of neuronal circuitry. Moreover, sensory perception in some cases depends on complete and nonredundant coverage of the receptive field by dendrites of functionally related neurons, a phenomenon known as tiling. For example, many types of neurons tile the mammalian retina, most likely to ensure efficient and unambiguous representation of the visual field. At least 11 distinct physiological classes of rabbit retinal ganglion cells (RGCs) cover their receptive field nonredundantly by avoiding overlap between dendrites of a single neuron as well as between dendrites of the same type of neurons, whereas dendrites of different types of neurons freely cross one another (Wassle et al. 1978(Wassle et al. , 1983Rockhill et al. 2002). Similarly, >20 classes of amacrine cells in the rabbit retina can be distinguished on the basis of dendrite morphology, and many of these classes of amacrine cells appear to tile the retina. Sensory neurons in Manduca, Drosophila, and the leech Hirudu medicinalis also exhibit tiling, suggesting that tiling may be a general mechanism to organize dendritic fields Grueber and Jan 2004).Once neurons tile their receptive field and achieve complete coverage during development, the tiling is maintained even as the territory changes; for example, as the animal grows in size. Whereas like-repels-like homotypic repulsion is one mechanism important for the establishment of receptive fields (Grueber et al. 2003b), how tiling is maintained after the establishment of the dendritic field is not well understood. Underscoring the potential physiological significance of the maintenance of dendritic fields, dendrites of layer III cortical ...

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“…For example, levels of H3K27me3 at the Neurog1 locus increase with each neural progenitor division, providing a potential mechanism for timing the loss of competence to make neurons (Hirabayashi et al, 2009). In Drosophila, PRCs were first identified as regulators of Hox gene expression but have since been shown to control multiple processes, including cell cycle regulation (O'Dor et al, 2006;Martinez et al, 2006), differentiation of germline progenitors (Chen et al, 2005;Narbonne et al, 2004), dendrite remodeling (Parrish et al, 2007) and the diversity of neuronal projection patterns (Wang et al, 2006). Genome-wide mapping of PRC targets in Drosophila suggests that PRCs regulate a wide range of developmental programs (Schwartz et al, 2006;Oktaba et al, 2008;Schuettengruber et al, 2009), including potentially regulating cell fate specification during neurogenesis.…”

Section: Introductionmentioning

confidence: 99%

Drosophila Polycomb complexes restrict neuroblast competence to generate motoneurons

2012

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SUMMARYSimilar to mammalian neural progenitors, Drosophila neuroblasts progressively lose competence to make early-born neurons. In neuroblast 7-1 (NB7-1), Kruppel (Kr) specifies the third-born U3 motoneuron and Kr misexpression induces ectopic U3 cells. However, competence to generate U3 cells is limited to early divisions, when the Eve + U motoneurons are produced, and competence is lost when NB7-1 transitions to making interneurons. We have found that Polycomb repressor complexes (PRCs) are necessary and sufficient to restrict competence in NB7-1. PRC loss of function extends the ability of Kr to induce U3 fates and PRC gain of function causes precocious loss of competence to make motoneurons. PRCs also restrict competence to make HB9 + Islet + motoneurons in another neuroblast that undergoes a motoneuron-to-interneuron transition, NB3-1. In contrast to the regulation of motoneuron competence, PRC activity does not affect the production of Eve + interneurons by NB3-3, HB9 + Islet + interneurons by NB7-3, or Dbx + interneurons by multiple neuroblasts. These findings support a model in which PRCs establish motoneuronspecific competence windows in neuroblasts that transition from motoneuron to interneuron production.

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Steroid hormone-dependent transformation ofpolyhomeoticmutant neurons in theDrosophilabrain

Cited by 24 publications

References 68 publications

Polycomb group genes are required for neural stem cell survival in postembryonic neurogenesis ofDrosophila

Polycomb group genes are required for neural stem cell survival in postembryonic neurogenesis ofDrosophila

Polycomb genes interact with the tumor suppressor genes hippo and warts in the maintenance of Drosophila sensory neuron dendrites

Drosophila Polycomb complexes restrict neuroblast competence to generate motoneurons

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