Dorsal eye selector pannier (pnr) suppresses the eye fate to define dorsal margin of the Drosophila eye

University of Dayton, Dayton, OH 45469, USA.
Developmental Biology (Impact Factor: 3.55). 10/2010; 346(2):258-71. DOI: 10.1016/j.ydbio.2010.07.030
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Axial patterning is crucial for organogenesis. During Drosophila eye development, dorso-ventral (DV) axis determination is the first lineage restriction event. The eye primordium begins with a default ventral fate, on which the dorsal eye fate is established by expression of the GATA-1 transcription factor pannier (pnr). Earlier, it was suggested that loss of pnr function induces enlargement in the dorsal eye due to ectopic equator formation. Interestingly, we found that in addition to regulating DV patterning, pnr suppresses the eye fate by downregulating the core retinal determination genes eyes absent (eya), sine oculis (so) and dacshund (dac) to define the dorsal eye margin. We found that pnr acts downstream of Ey and affects the retinal determination pathway by suppressing eya. Further analysis of the "eye suppression" function of pnr revealed that this function is likely mediated through suppression of the homeotic gene teashirt (tsh) and is independent of homothorax (hth), a negative regulator of eye. Pnr expression is restricted to the peripodial membrane on the dorsal eye margin, which gives rise to head structures around the eye, and pnr is not expressed in the eye disc proper that forms the retina. Thus, pnr has dual function, during early developmental stages pnr is involved in axial patterning whereas later it promotes the head specific fate. These studies will help in understanding the developmental regulation of boundary formation of the eye field on the dorsal eye margin.

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    • "Prior to the imposition of dorsal identity, the entire eye disc expresses the ventral selector gene fringe ( fng). During the late first/early second instar, expression of pannier ( pnr), which encodes a GATA transcription factor, is activated via an unknown mechanism in a small group of cells within the peripodial membrane along the dorsal margin (Heitzler et al., 1996; Maurel-Zaffran and Treisman, 2000; Oros et al., 2010). Pnr is then responsible for inducing the expression of wingless (wg) (Maurel-Zaffran and Treisman, 2000), which in turn activates expression of the Iroquois complex (Iro-C) genes within the dorsal half of the eye (McNeill et al., 1997; Heberlein et al., 1998). "
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    ABSTRACT: One of the seminal events in the history of a tissue is the establishment of the anterior-posterior, dorsal-ventral (D/V) and proximal-distal axes. Axis formation is important for the regional specification of a tissue and allows cells along the different axes to obtain directional and positional information. Within the Drosophila retina, D/V axis formation is essential to ensure that each unit eye first adopts the proper chiral form and then rotates precisely 90° in the correct direction. These two steps are important because the photoreceptor array must be correctly aligned with the neurons of the optic lobe. Defects in chirality and/or ommatidial rotation will lead to disorganization of the photoreceptor array, misalignment of retinal and optic lobe neurons, and loss of visual acuity. Loss of the helix-loop-helix protein Extramacrochaetae (Emc) leads to defects in both ommatidial chirality and rotation. Here, we describe a new role for emc in eye development in patterning the D/V axis. We show that the juxtaposition of dorsal and ventral fated tissue in the eye leads to an enrichment of emc expression at the D/V midline. emc expression at the midline can be eliminated when D/V patterning is disrupted and can be induced in situations in which ectopic boundaries are artificially generated. We also show that emc functions downstream of Notch signaling to maintain the expression of four-jointed along the midline. © 2015. Published by The Company of Biologists Ltd.
    Development 03/2015; 142(5):1006-15. DOI:10.1242/dev.120618 · 6.46 Impact Factor
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    • "Loss-of-function clones of pnrexhibit ectopic dorsal eyes, which are restricted within the clones, and suggests that absence of pnrfunction promotes ectopic eye formation in the dorsal eye margin. Thus, Pnr defines the boundary between the head cuticle and the dorsal margin of the developing eye field (Fig. 7; Oros et al., 2010). Since pnris not expressed in the ventral eye, there is a different mechanism to define the boundary of the eye field on the ventral margin. "
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    ABSTRACT: During organogenesis in all multi-cellular organisms, axial patterning is required to transform a single layer organ primordium into a three-dimensional organ. The Drosophila eye model serves as an excellent model to study axial patterning. Dorso-ventral (DV) axis determination is the first lineage restriction event during axial patterning of the Drosophila eye. The early Drosophila eye primordium has a default ventral fate, and the dorsal eye fate is established by onset of dorsal selector gene pannier (pnr) expression in a group of cells on the dorsal eye margin. The boundary between dorsal and ventral compartments called the equator is the site for Notch (N) activation, which triggers cell proliferation and differentiation. This review will focus on (1) chronology of events during DV axis determination; (2) how early division of eye into dorsal and ventral compartments contributes towards the growth and patterning of the fly retina, and (3) functions of DV patterning genes.
    Developmental Dynamics 01/2012; 241(1):69-84. DOI:10.1002/dvdy.22764 · 2.38 Impact Factor
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    ABSTRACT: Organ formation requires a delicate balance of positive and negative regulators. In Drosophila eye development, wingless (wg) is expressed at the lateral margins of the eye disc and serves to block retinal development. The T-box gene optomotor-blind (omb) is expressed in a similar pattern and is regulated by Wg. Omb mediates part of Wg activity in blocking eye development. Omb exerts its function primarily by blocking cell proliferation. These effects occur predominantly in the ventral margin. Our results suggest that the primary effect of Omb is the blocking of Jak/STAT signaling by repressing transcription of upd which encodes the Jak receptor ligand Unpaired.
    PLoS ONE 03/2015; 10(3):e0120236. DOI:10.1371/journal.pone.0120236 · 3.23 Impact Factor
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