optix functions as a link between the retinal determination network and the dpp pathway to control morphogenetic furrow progression in Drosophila

ABSTRACT In Drosophila melanogaster, the loss of activator de2f1 leads to a severe reduction in cell proliferation and repression of E2F targets. To date, the only known way to rescue the proliferation block in de2f1 mutants was through the inactivation of dE2F2. This suggests that dE2F2 provides a major contribution to the de2f1 mutant phenotype. Here, we report that in mosaic animals, in addition to de2f2, the loss of a DEAD box protein Belle (Bel) also rescues proliferation of de2f1 mutant cells. Surprisingly, the rescue occurs in a dE2F2-independent manner since the loss of Bel does not relieve dE2F2-mediated repression. In the eye disc, bel mutant cells fail to undergo a G1 arrest in the morphogenetic furrow, delay photoreceptor recruitment and differentiation, and show a reduction of the transcription factor Ci155. The down-regulation of Ci155 is important since it is sufficient to partially rescue proliferation of de2f1 mutant cells. Thus, mutation of bel relieves the dE2F2-mediated cell cycle arrest in de2f1 mutant cells through a novel Ci155-dependent mechanism without functional inactivation of the dE2F2 repressor.

Download Full-text

Catching the Next Wave: Patterning of the Drosophila Eye by the Morphogenetic Furrow

Molecular Genetics of Axial Patterning, Growth and Disease in the Drosophila Eye ◽

10.1007/978-1-4614-8232-1_3 ◽

2013 ◽

pp. 75-97 ◽

Cited By ~ 8

Author(s):

Justin P. Kumar

Keyword(s):

Morphogenetic Furrow ◽

Drosophila Eye

Download Full-text

Wingless blocks bristle formation and morphogenetic furrow progression in the eye through repression of Daughterless

Development ◽

10.1242/dev.129.14.3393 ◽

2002 ◽

Vol 129 (14) ◽

pp. 3393-3402 ◽

Cited By ~ 1

Author(s):

Kenneth M. Cadigan ◽

Austin D. Jou ◽

Roel Nusse

Keyword(s):

Gene Expression ◽

Ectopic Expression ◽

Dominant Negative ◽

Proneural Gene ◽

Morphogenetic Furrow ◽

Heterologous Promoter ◽

Basic Helix Loop Helix ◽

Helix Loop Helix ◽

Dominant Negative Form ◽

Negative Form

In the developing eye, wingless activity represses proneural gene expression (and thus interommatidial bristle formation) and positions the morphogenetic furrow by blocking its initiation in the dorsal and ventral regions of the presumptive eye. We provide evidence that wingless mediates both effects, at least in part, through repression of the basic helix-loop-helix protein Daughterless. daughterless is required for high proneural gene expression and furrow progression. Ectopic expression of wingless blocks Daughterless expression in the proneural clusters. This repression, and that of furrow progression, can be mimicked by an activated form of armadillo and blocked by a dominant negative form of pangolin/TCF. Placing daughterless under the control of a heterologous promoter blocks the ability of ectopic wingless to inhibit bristle formation and furrow progression. hedgehog and decapentapleigic could not rescue the wingless furrow progression block, indicating that wingless acts downstream of these genes. In contrast, Atonal and Scute, which are thought to heterodimerize with Daughterless to promote furrow progression and bristle formation, respectively, can block ectopic wingless action. These results are summarized in a model where daughterless is a major, but probably not the only, target of wingless action in the eye.

Download Full-text

Characterization of Star and its interactions with sevenless and EGF receptor during photoreceptor cell development in Drosophila

Development ◽

10.1242/dev.120.7.1731 ◽

1994 ◽

Vol 120 (7) ◽

pp. 1731-1745 ◽

Cited By ~ 17

Author(s):

A.L. Kolodkin ◽

A.T. Pickup ◽

D.M. Lin ◽

C.S. Goodman ◽

U. Banerjee

Keyword(s):

Genetic Background ◽

Egf Receptor ◽

Transmembrane Domain ◽

Loss Of Function ◽

Morphogenetic Furrow ◽

Eye Disc ◽

Son Of Sevenless ◽

Photoreceptor Development ◽

Star Gene

Loss-of-function mutations in Star impart a dominant rough eye phenotype and, when homozygous, are embryonic lethal with ventrolateral cuticular defects. We have cloned the Star gene and show that it encodes a novel protein with a putative transmembrane domain. Star transcript is expressed in a dynamic pattern in the embryo including in cells of the ventral midline. In the larval eye disc, Star is expressed first at the morphogenetic furrow, then in the developing R2, R5, and R8 cells as well as in the posterior clusters of the disc in additional R cells. Star interacts with Drosophila EGF receptor in the eye and mosaic analysis of Star in the larval eye disc reveals that homozygous Star patches contain no developing R cells. Taken together with the expression pattern at the morphogenetic furrow, these results demonstrate an early role for Star in photoreceptor development. Additionally, loss-of-function mutations in Star act as suppressors of R7 development in a sensitized genetic background involving the Son of sevenless (Sos) locus, and overexpression of Star enhances R7 development in this genetic background. Based on the genetic interactions with Sos, we suggest that Star also has a later role in photoreceptor development including the recruitment of the R7 cell through the sevenless pathway.

Download Full-text

Regulators of the Morphogenetic Furrow

Results and Problems in Cell Differentiation - Drosophila Eye Development ◽

10.1007/978-3-540-45398-7_3 ◽

2002 ◽

pp. 21-33 ◽

Cited By ~ 9

Author(s):

Jeffrey D. Lee ◽

Jessica E. Treisman

Keyword(s):

Morphogenetic Furrow

Download Full-text

frizzled regulates mirror-symmetric pattern formation in the Drosophila eye

Development ◽

10.1242/dev.121.9.3045 ◽

1995 ◽

Vol 121 (9) ◽

pp. 3045-3055 ◽

Cited By ~ 38

Author(s):

L. Zheng ◽

J. Zhang ◽

R.W. Carthew

Keyword(s):

Pattern Formation ◽

Cell Surface ◽

Transmembrane Protein ◽

Photoreceptor Cells ◽

Mirror Image ◽

Morphogenetic Furrow ◽

Symmetric Pattern ◽

Mosaic Analysis ◽

Drosophila Eye ◽

A Cell

Coordinated morphogenesis of ommatidia during Drosophila eye development establishes a mirror-image symmetric pattern across the entire eye bisected by an anteroposterior equator. We have investigated the mechanisms by which this pattern formation occurs and our results suggest that morphogenesis is coordinated by a graded signal transmitted bidirectionally from the presumptive equator to the dorsal and ventral poles. This signal is mediated by frizzled, which encodes a cell surface transmembrane protein. Mosaic analysis indicates that frizzled acts non-autonomously in an equatorial to polar direction. It also indicates that relative levels of frizzled in photoreceptor cells R3 and R4 of each ommatidium affect their positional fate choices such that the cell with greater frizzled activity becomes an R3 cell and the cell with less frizzled activity becomes an R4 cell. Moreover, this bias affects the choice an ommatidium makes as to which direction to rotate. Equator-outwards progression of elav expression and expression of the nemo gene in the morphogenetic furrow are regulated by frizzled, which itself is dynamically expressed about the morphogenetic furrow. We propose that frizzled mediates a bidirectional signal emanating from the equator.

Download Full-text

Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway

Development ◽

10.1242/dev.126.24.5795 ◽

1999 ◽

Vol 126 (24) ◽

pp. 5795-5808 ◽

Cited By ~ 9

Author(s):

S. Greenwood ◽

G. Struhl

Keyword(s):

Transcription Factor ◽

Short Range ◽

Morphogenetic Furrow ◽

Serine Threonine Kinase ◽

Present Evidence ◽

Threonine Kinase ◽

Drosophila Eye ◽

Undifferentiated Cells ◽

Hh Signaling ◽

Necessary And Sufficient

During Drosophila eye development, Hedgehog (Hh) protein secreted by maturing photoreceptors directs a wave of differentiation that sweeps anteriorly across the retinal primordium. The crest of this wave is marked by the morphogenetic furrow, a visible indentation that demarcates the boundary between developing photoreceptors located posteriorly and undifferentiated cells located anteriorly. Here, we present evidence that Hh controls progression of the furrow by inducing the expression of two downstream signals. The first signal, Decapentaplegic (Dpp), acts at long range on undifferentiated cells anterior to the furrow, causing them to enter a ‘pre-proneural’ state marked by upregulated expression of the transcription factor Hairy. Acquisition of the pre-proneural state appears essential for all prospective retinal cells to enter the proneural pathway and differentiate as photoreceptors. The second signal, presently unknown, acts at short range and is transduced via activation of the Serine-Threonine kinase Raf. Activation of Raf is both necessary and sufficient to cause pre-proneural cells to become proneural, a transition marked by downregulation of Hairy and upregulation of the proneural activator, Atonal (Ato), which initiates differentiation of the R8 photoreceptor. The R8 photoreceptor then organizes the recruitment of the remaining photoreceptors (R1-R7) through additional rounds of Raf activation in neighboring pre-proneural cells. Finally, we show that Dpp signaling is not essential for establishing either the pre-proneural or proneural states, or for progression of the furrow. Instead, Dpp signaling appears to increase the rate of furrow progression by accelerating the transition to the pre-proneural state. In the abnormal situation in which Dpp signaling is blocked, Hh signaling can induce undifferentiated cells to become pre-proneural but does so less efficiently than Dpp, resulting in a retarded rate of furrow progression and the formation of a rudimentary eye.

Download Full-text