Charlatan , a Zn - finger transcription factor , establishes a novel level of regulation of the proneural achaete / scute genes of Drosophila Luis

Abstract

A classical example of two-dimensional pattern is that formed by the bristles and other types of sensory organs (SOs) in the epidermis of the adult Drosophila fly (Lindsley and Zimm, 1992). On the head and the dorsal mesothorax (notum), conspicuous large bristles (macrochaetae) arise in stereotyped positions, while smaller bristles (microchaetae) appear in density patterns. During the third instar larval and early pupal stages, the location of each macrochaeta is specified by the emergence of a precursor cell (SO precursor cell, SOP) at a stereotyped position of the imaginal disks, the larval epithelia that give rise to a large part of the adult epidermis (Cubas et al., 1991; Huang et al., 1991). This accurate positioning of SOPs in the imaginal disks is thought to be the culmination of a multistep process in which positional information is gradually refined (reviewed by Gómez-Skarmeta et al., 2003; Modolell and Campuzano, 1998). A key step of this process is the expression of the proneural genes achaete (ac) and scute (sc) in groups of cells, the proneural clusters, that prefigure the sites of the future macrochaetae (Cubas et al., 1991; Romani et al., 1989; Skeath and Carroll, 1991). These genes, members of the achaete-scute complex (ASC) (reviewed by Campuzano and Modolell, 1992; Ghysen and Dambly-Chaudière, 1988; Ghysen and DamblyChaudière, 1989), encode transcriptional factors of the basic helix-loop-helix (bHLH) family. These factors confer to cells the potential to become SOPs, presumably by implementing neural differentiation programs. From each proneural cluster, a fixed number of SOPs are born, usually one or two. The proneural clusters of the wing imaginal disks (the precursors of each heminotum, wing and mesothoracic pleura) not only appear in constant positions, but each of them has a characteristic size, shape and time of appearance and disappearance (Cubas et al., 1991; Skeath and Carroll, 1991). Moreover, a typical cluster that gives rise to one bristle may consist of 20 to 30 cells, but the SOP is selected from a smaller subgroup of cells that accumulate higher levels of Ac-Sc proteins than their neighbors, which constitute the proneural field (Cubas et al., 1991; Cubas and Modolell, 1992; Skeath and Carroll, 1991). This subgroup and the SOP, which accumulates the highest levels of Ac-Sc, always occupy the same position within the cluster. Hence, the expression of ac/sc in proneural clusters is exquisitely regulated. The regulation of ac/sc is effected by means of two classes of cis-regulatory sequences, namely, cluster-specific and SOP-specific enhancers. The first type normally directs expression of both ac and sc in one specific proneural cluster and defines many of its characteristics, such as position, size and shape. These cluster-specific enhancers appear to be controlled by local combinations of transcription factors that together form a prepattern (reviewed by Ghysen and DamblyChaudière, 1988; Gómez-Skarmeta et al., 2003). Expression occurs only at sites with the appropriate combinations of factors. Although in a few cases some of the prepattern The proneural genes achaete (ac) and scute (sc) are necessary for the formation of the external sensory organs (SOs) of Drosophila. ac and sc are expressed in proneural clusters and impart their cells with neural potential. For this potential to be realized, and the SO precursor cell (SOP) to arise within a cluster, sufficient proneural protein must accumulate in the cluster. Here we describe a novel gene, charlatan (chn), which encodes a zinc finger transcription factor that facilitates this accumulation by forming a stimulatory loop with ac/sc. We find that loss of function of chn decreases the accumulation of Sc in proneural clusters and partially removes notum macrochaetae, while overexpression of chn enhances ac/sc expression and the formation of extra SOs. Moreover, chn is activated by ac/sc in proneural clusters. Chn apparently stimulates ac/sc by physically interacting with the proneural cluster-specific enhancers and increasing enhancer efficiency, thus acting as a stimulator of ac/sc expression in proneural clusters. chn is also required for the proper development of the embryonic peripheral nervous system, as its absence leads to loss of neurons and causes aberrant development of chordotonal organs.

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Cite this paper

@inproceedings{Escudero2005CharlatanA, title={Charlatan , a Zn - finger transcription factor , establishes a novel level of regulation of the proneural achaete / scute genes of Drosophila Luis}, author={Margarita Escudero and Eva Caminero and Karen L . Schulze and Hugo J. Bellen and Juan Modolell}, year={2005} }