Academic journal article Genetics

Drosophila Nemo Promotes Eye Specification Directed by the Retinal Determination Gene Network

Academic journal article Genetics

Drosophila Nemo Promotes Eye Specification Directed by the Retinal Determination Gene Network

Article excerpt

ABSTRACT

Drosophila nemo (nmo) is the founding member of the Nemo-like kinase (Nlk) family of serine-threonine kinases. Previous work has characterized nmo's role in planar cell polarity during ommatidial patterning. Here we examine an earlier role for nmo in eye formation through interactions with the retinal determination gene network (RDGN). nmo is dynamically expressed in second and third instar eye imaginal discs, suggesting additional roles in patterning of the eyes, ocelli, and antennae. We utilized genetic approaches to investigate Nmo's role in determining eye fate. nmo genetically interacts with the retinal determination factors Eyeless (Ey), Eyes Absent (Eya), and Dachshund (Dac). Loss of nmo rescues ey and eya mutant phenotypes, and heterozygosity for eya modifies the nmo eye phenotype. Reducing nmo also rescues small-eye defects induced by misexpression of ey and eya in early eye development. nmo can potentiate RDGN-mediated eye formation in ectopic eye induction assays. Moreover, elevated Nmo alone can respecify presumptive head cells to an eye fate by inducing ectopic expression of dac and eya. Together, our genetic analyses reveal that nmo promotes normal and ectopic eye development directed by the RDGN.

THE adult structures of Drosophila melanogaster are patterned during the larval stages in discrete epithelial compartments called imaginal discs. Larval imaginal discs are inherited from the embryo as small groups of progenitor cells (Garcia-Bellido and Merriam 1969). As these cells proliferate, each imaginal disc becomes compartmentalized into fields of cells expressing unique protein sets. Each protein set confers a specific cellular identity. As development progresses, highly complex and integrated signaling networks further refine the fields of cells to achieve the final organ pattern. These signaling networks not only orchestrate cell determination, but also tightly regulate proliferation and cell survival to ensure the proportionality of the resulting adult.

In Drosophila, the adult eyes, antennae, and the majority of head structures are derived from the eyeantennal imaginal discs (Haynie and Bryant 1986). The smaller, anterior region of the disc is fated to become the antenna, and the larger posterior compartment contains the eye and head primordia. In this article, we refer to the anterior and posterior compartments as the antennal and eye discs, respectively (Figure 1B). These discs are composed of two epithelial layers: the main epithelium (ME) and the squamous peripodial epithelium (PE) (Haynie and Bryant 1986). The ME comprises primordia of the compound eye, its surrounding cuticle, and the antennae, while the PE gives rise to the remainder of the head. Studies have revealed a novel role for PE cells in directing cellular events in theME through cell-cell signaling mediated by lumenal processes (Gibson and Schubiger 2001).

Eye specification is directed in the posterior region of the eye disc by the concerted efforts of the retinal determination gene network (RDGN), a cassette of evolutionarily conserved nuclear factors (Figure 1A; reviewed in Pappu andMardon 2004; Silver and Rebay 2005; Jemc and Rebay 2006). RDGN mutants are generally characterized by loss of eye tissue (Bonini et al. 1993; Cheyette et al. 1994; Mardon et al. 1994; Quiring et al. 1994). twin-of-eyeless (toy) (Czerny et al. 1999) and eyeless (ey) (Quiring et al. 1994) are Pax-6 genes positioned at the top of the network hierarchy. toy is expressed in the embryonic eye field and activates ey in all cells of the first instar larval imaginal disc (Figure 1A) (Czerny et al. 1999). The primary eye/antennal division of the disc is achieved by downregulation of ey in the anterior-most region of the disc in early second instar, allowing expression of the antennal selector cut (Kenyon et al. 2003). Ey deploys the RDGN by activating sine oculis (so) and eyes absent (eya) expression at the posterior margin (Halder et al. …

Search by... Author
Show... All Results Primary Sources Peer-reviewed

Oops!

An unknown error has occurred. Please click the button below to reload the page. If the problem persists, please try again in a little while.