Tissue specificity of hedgehog repression by the Polycomb group during Drosophila melanogaster development

Chanas, Grégory; Maschat, Florence

doi:10.1016/j.mod.2005.05.001

Cited by 16 publications

(13 citation statements)

References 56 publications

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“…For example, terminally differentiated cells of the salivary glands from third instar larvae do not express CycA (Edgar and Orr-Weaver 2001), but neither the endogenous gene nor the isolated PRE are able to attract PcG proteins in this tissue. This situation is similar to the hh gene, which is a known target of PcG proteins (Chanas and Maschat 2005). Another chromatin-silencing activity must therefore be responsible for this silencing.…”

Section: Dynamic Repression Versus Stable Silencing Of the Cyca Gene mentioning

confidence: 75%

Polycomb group-dependent Cyclin A repression in Drosophila

Martinez¹,

Colomb²,

Déjardin³

et al. 2006

Genes Dev.

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Polycomb group (PcG) and trithorax group (trxG) proteins are well known for their role in the maintenance of silent and active expression states of homeotic genes. However, PcG proteins may also be required for the control of cellular proliferation in vertebrates. In Drosophila, PcG factors act by associating with specific DNA regions termed PcG response elements (PREs). Here, we have investigated whether Drosophila cell cycle genes are directly regulated by PcG proteins through PREs. We have isolated a PRE that regulates Cyclin A (CycA) expression. This sequence is bound by the Polycomb (PC) and Polyhomeotic (PH) proteins of the PcG, and also by GAGA factor (GAF), a trxG protein that is usually found associated with PREs. This sequence In Drosophila, PcG-mediated repression occurs through cis-regulatory DNA sequences termed PREs (PcG response elements) (Zink et al. 1991;Simon et al. 1993). PREs share several tractable molecular and genetic properties: (1) PcG proteins bind directly to PREs (Zink and Paro 1995; Strutt and Paro 1997); (2) in vivo, PREs induce repression of the adjacent white reporter gene, producing a variegated phenotype (Fauvarque and Dura 1993); (3) this variegated phenotype is dependent on PcG and trxG proteins; and (4) PREs induce pairingsensitive repression (PSR) (for review, see Kassis 2002).Epigenetic regulation of gene expression is emerging as a key mechanism in the control of cellular proliferation. In vertebrates, PRC1 and PRC2/3 components have been implicated in the regulation of proliferation, acting as either potent activators or repressors of the cell cycle. Progression through the cell cycle depends primarily on the activity of the cyclin-dependent kinases (Cdks). Cdks, upon association with their respective cyclin partners, mediate the transitions between the different cell cycle phases. Although with increased complexity, cell Cold Spring Harbor Laboratory Press on May 12, 2018 -Published by genesdev.cshlp.org Downloaded from

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Section: Dynamic Repression Versus Stable Silencing Of the Cyca Gene mentioning

confidence: 75%

Polycomb group-dependent Cyclin A repression in Drosophila

Martinez¹,

Colomb²,

Déjardin³

et al. 2006

Genes Dev.

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“…This underlines the importance of tissue specificity. Indeed, many studies have shown genetically that the PcG and TrxG genes have tissue-specific roles (Breen, 1999;Chanas and Maschat, 2005;Janody et al, 2004;Narbonne et al, 2004). It may well be that each type of adult stem cell in Drosophila uses a different set of PRE/TREs.…”

Section: Switching Upon Differentiation: Insights From Fliesmentioning

confidence: 99%

Polycomb/Trithorax response elements and epigenetic memory of cell identity

2007

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DEVELOPMENT 223Polycomb/Trithorax group response elements (PRE/TREs) are fascinating chromosomal pieces. Just a few hundred base pairs long, these elements can remember and maintain the active or silent transcriptional state of their associated genes for many cell generations, long after the initial determining activators and repressors have disappeared. Recently, substantial progress has been made towards understanding the nuts and bolts of PRE/TRE function at the molecular level and in experimentally mapping PRE/TRE sites across whole genomes. Here we examine the insights, controversies and new questions that have been generated by this recent flood of data. IntroductionDuring the 1990s, studies of the regulation of homeotic genes in the Drosophila Bithorax complex (BX-C) uncovered very different behaviour for two classes of cis-regulatory DNA element: initiator elements and maintenance elements (or Polycomb/Trithorax group response elements, PRE/TREs) (Busturia et al., 1989;Chan et al., 1994;Chiang et al., 1995;Simon et al., 1993;Simon et al., 1990) (reviewed by Maeda and Karch, 2006). One can think of these two types of elements as 'shift workers' that use very different strategies to regulate the expression patterns of the same genes at different stages of embryonic development. In the first three hours of development, the initiator elements are in control: the output of each homeotic gene depends on the local concentrations of segmentation gene products (these are activators and repressors that are present in different concentrations at different positions of the embryo). However, a few hours after these homeotic gene patterns have been established, the segmentation gene products decay, and thus the positional information they provide is lost. The transcriptional history of each gene is subsequently maintained throughout the rest of development, and into adulthood, by the ubiquitously expressed Polycomb group (PcG) and Trithorax group proteins (TrxG), which work antagonistically via the PRE/TRE elements to maintain active (TrxG) or silenced (PcG) transcriptional states (Moehrle and Paro, 1994). Although the effects of mutations in the PcG and TrxG genes are seen only after the segmentation gene products decay, the PcG and TrxG proteins themselves appear to associate with PRE/TREs much earlier, so that PRE/TREs are 'preloaded' with PcG and TrxG proteins, ready to maintain the transcriptional states that are set by the transiently acting segmentation gene products (Orlando et al., 1998).The maintenance of transcriptional memory at PRE/TREs is 'epigenetic'. This term has suffered much overuse and abuse in recent years, but we use here the classical definition given by Ptashne and Gann (Ptashne and Gann, 2002) (p100): "a change in the state of expression of a gene that does not involve a mutation, but that is nevertheless inherited (after cell division) in the absence of the signal (or event) that initiated that change". In the case of PRE/TREs, the information required to turn gene activity off or on after ea...

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“…Moreover, a direct genetic interaction between en and the apoptotic machinery remains to be investigated. As en is known to have multiple interactions with other proteins (Alexandre and Vincent, 2003;Chanas and Maschat, 2005;Joly et al, 2007;Kobayashi et al, 2003), a complex regulatory network involving target proteins of en may be responsible for regulating apoptosis in a lineage-specific manner. Further analysis of interactions with such target proteins is necessary to reveal the full regulatory network in more detail.…”

Section: Research Articlementioning

confidence: 99%

Lineage-specific cell death in postembryonic brain development ofDrosophila

2009

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The Drosophila central brain is composed of thousands of neurons that derive from approximately 100 neuroblasts per hemisphere. Functional circuits in the brain require precise neuronal wiring and tight control of neuronal numbers. How this accurate control of neuronal numbers is achieved during neural development is largely unclear. Specifically, the role of programmed cell death in control of cell numbers has not been studied in the central brain neuroblast lineages. Here, we focus on four postembryonic neuroblast lineages in the central brain identified on the basis that they express the homeobox gene engrailed (en). For each lineage,we determine the total number of adult-specific neurons generated as well as number and pattern of en-expressing cells. We then demonstrate that programmed cell death has a pronounced effect on the number of cells in the four lineages; approximately half of the immature adult-specific neurons in three of the four lineages are eliminated by cell death during postembryonic development. Moreover, we show that programmed cell death selectively affects en-positive versus en-negative cells in a lineage-specific manner and, thus, controls the relative number of en-expressing neurons in each lineage. Furthermore, we provide evidence that Notch signaling is involved in the regulation of en expression. Based on our findings, we conclude that lineage-specific programmed cell death plays a prominent role in the generation of neuronal number and lineage diversity in the Drosophila brain.

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Tissue specificity of hedgehog repression by the Polycomb group during Drosophila melanogaster development

Cited by 16 publications

References 56 publications

Polycomb group-dependent Cyclin A repression in Drosophila

Polycomb group-dependent Cyclin A repression in Drosophila

Polycomb/Trithorax response elements and epigenetic memory of cell identity

Lineage-specific cell death in postembryonic brain development ofDrosophila

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