polyhomeotic controls engrailed expression and the hedgehog signaling pathway in imaginal discs

Randsholt, Neel B.; Maschat, Florence; Santamarı́a, Pedro

doi:10.1016/s0925-4773(00)00342-7

Cited by 33 publications

(44 citation statements)

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“…The trxG and PcG proteins are known to control en expression (Busturia and Morata 1988;Moazed and O'Farrell 1992;Breen et al 1995;Brizuela and Kennison 1997;Strutt 1997;Maschat et al 1998). Previous studies found indications that hh expression itself might also be regulated by the trxG and PcG proteins (Felsenfeld and Kennison 1995;Randsholt et al 2000). In this paper, we present evidence that hh expression is, indeed, directly controlled by the action of trxG and PcG proteins.…”

supporting

confidence: 65%

A cellular memory module conveys epigenetic inheritance of hedgehog expression during Drosophila wing imaginal disc development

Maurange

Paro²

2002

Genes Dev.

102

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In Drosophila, the Trithorax-group (trxG) and Polycomb-group (PcG) proteins interact with chromosomal elements, termed Cellular Memory Modules (CMMs). By modifying chromatin, this ensures a stable heritable maintenance of the transcriptional state of developmental regulators, like the homeotic genes, that is defined embryonically. We asked whether such CMMs could also control expression of genes involved in patterning imaginal discs during larval development. Our results demonstrate that expression of the hedgehog gene, once activated, is maintained by a CMM. In addition, our experiments indicate that the switching of such CMMs to an active state during larval stages, in contrast to embryonic stages, may require specific trans-activators. Our results suggest that the patterning of cells in particular developmental fields in the imaginal discs does not only rely on external cues from morphogens, but also depends on the previous history of the cells, as the control by CMMs ensures a preformatted gene expression pattern.

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supporting

confidence: 65%

A cellular memory module conveys epigenetic inheritance of hedgehog expression during Drosophila wing imaginal disc development

Maurange

Paro²

2002

Genes Dev.

102

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“…The repressive effect of chick Pcl2 on Shh expression suggests that the products of PcG genes not only maintain the silenced status of gene expression involved in long-term developmental decisions, but also function to regulate/silence the expression of active gene during embryonic development. This hypothesis is supported by the finding that in Drosophila the product of Polyhomeotic (ph) exerts negative transcriptional control on active genes (Randsholt et al, 2000). Furthermore, the Xenopus Pcl genes were also shown to repress gene expression in the developing central nervous system (Yoshitake et al, 1999;Kitaguchi et al, 2001).…”

Section: Discussionmentioning

confidence: 94%

ChickPcl2regulates the left-right asymmetry by repressingShhexpression in Hensen's node

Wang

Zhang

et al. 2004

Development

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Asymmetric expression of sonic hedgehog (Shh) in the left side of Hensen's node, a crucial step for specifying the left-right (LR) axis in the chick embryo, is established by the repression of Shhexpression in the right side of the node. The transcriptional regulator that mediates this repression has not been identified. We report the isolation and characterization of a novel chick Polycomblike 2 gene, chick Pcl2, which encodes a transcription repressor and displays an asymmetric expression, downstream from Activin-βB and Bmp4, in the right side of Hensen's node in the developing embryo. In vitro mapping studies define the transcription repression activity to the PHD finger domain of the chick Pcl2 protein. Repression of chick Pcl2expression in the early embryo results in randomized heart looping direction,which is accompanied by the ectopic expression of Shh in the right side of the node and Shh downstream genes in the right lateral plate mesoderm (LPM), while overexpression of chick Pcl2 represses Shh expression in the node. The repression of Shh by chick Pcl2 was also supported by studies in which chick Pcl2 was overexpressed in the developing chick limb bud and feather bud. Similarly,transgenic overexpression of chick Pcl2 in the developing mouse limb inhibits Shh expression in the ZPA. In vitro pull-down assays demonstrated a direct interaction of the chick Pcl2 PHD finger with EZH2, a component of the ESC/E(Z) repressive complex. Taken together with the fact that chick Pcl2 was found to directly repress Shh promoter activity in vitro, our results demonstrate a crucial role for chick Pcl2 in regulating LR axis patterning in the chick by silencing Shh in the right side of the node.

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“…1D and 1E). PcG genes are involved in repression of hh in the A compartment (Randsholt et al, 2000) and, as shown in Fig. 1F, clones of cells located in the A compartment and mutant for the PcG gene Suppressor 2 of zeste [Su(z)2] showed ectopic expression of hh.…”

Section: Abc a 43-kb Region That Recapitulates The Expression Of Hhmentioning

confidence: 99%

Enhancer-PRE communication contributes to the expansion of gene expression domains in proliferating primordia

et al. 2011

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the homeodomain proteins Engrailed (En) and Invected are expressed in the posterior (P) compartment, where they are required to repress Ci expression (Eaton and Kornberg, 1990) and relieve Ci-mediated repression of hh (Bejarano and Milan, 2009). PcG proteins help to maintain the repression of hh expression in A cells whereas TrxG proteins contribute to maintaining the expression of hh in P cells (Bejarano and Milan, 2009;Chanas and Maschat, 2005). Notch activity at the dorsal-ventral (DV) compartment boundary has also been reported to participate in the regulation of hh expression; however, the mechanistic basis behind this is uncertain (Bejarano and Milan, 2009). Although communication between the hh-ME and those cis-enhancers that integrate positional information conferred by the activities of Ci, En and Notch has been proposed as a way to initiate and maintain the transcriptional state of hh in P cells, the identity of these enhancers and the proposed communication remain elusive.Here, we have isolated a 4.3-kb cis-regulatory region that recapitulates hh expression in the P compartment of the wing primordium. This fragment includes the previously defined hh-ME and a nearby enhancer (termed C enhancer) that responds to En, Ci and Notch and drives gene expression to a thin stripe in the P compartment that corresponds to the DV compartment boundary. We present evidence that the ME maintains the initial transcriptional Development 138, 3125-3134 (2011) SUMMARYTrithorax-group and Polycomb-group proteins interact with chromosomal elements, termed PRE/TREs, to ensure stable heritable maintenance of the transcriptional state of nearby genes. Regulatory elements that bind both groups of proteins are termed maintenance elements (MEs). Some of these MEs maintain the initial activated transcriptional state of a nearby reporter gene through several rounds of mitosis during development. Here, we show that expression of hedgehog in the posterior compartment of the Drosophila wing results from the communication between a previously defined ME and a nearby cisregulatory element termed the C enhancer. The C enhancer integrates the activities of the Notch and Hedgehog signalling pathways and, from the early wing primordium stage, drives expression to a thin stripe in the posterior compartment that corresponds to the dorsal-ventral compartment boundary. The ME maintains the initial activated transcriptional state conferred by the C enhancer and contributes to the expansion, by growth, of its expression domain throughout the posterior compartment. Communication between the ME and the C enhancer also contributes to repression of gene expression in anterior cells. Most interestingly, we present evidence that enhancers and MEs of different genes are interchangeable modules whose communication is involved in restricting and expanding the domains of gene expression. Our results emphasize the modular role of MEs in regulation of gene expression within growing tissues.

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polyhomeotic controls engrailed expression and the hedgehog signaling pathway in imaginal discs

Cited by 33 publications

References 50 publications

A cellular memory module conveys epigenetic inheritance of hedgehog expression during Drosophila wing imaginal disc development

A cellular memory module conveys epigenetic inheritance of hedgehog expression during Drosophila wing imaginal disc development

ChickPcl2regulates the left-right asymmetry by repressingShhexpression in Hensen's node

Enhancer-PRE communication contributes to the expansion of gene expression domains in proliferating primordia

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