The TGFβ homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina

Heberlein, Ulrike; Wolff, Tanya; Rubin, Gerald M.

doi:10.1016/0092-8674(93)90535-x

Cited by 407 publications

(271 citation statements)

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“…This is unaffected by the size, width or location of the clone. We confirmed that the furrow was in fact accelerating through emc mutant tissue by analyzing the dpplacZ transcriptional reporter, which, during the late third instar, is expressed solely within the advancing furrow (Blackman et al, 1991;Heberlein et al, 1993;Chanut and Heberlein, 1997a;Chanut and Heberlein, 1997b). As the furrow passes through emc-null clones dpp appears to be expressed in a broader swathe of cells and at higher levels ( Fig.…”

Section: Research Articlementioning

confidence: 61%

“…As the furrow progresses across the eye field, Hh is secreted by differentiating photoreceptors and received by cells within the furrow (Heberlein et al, 1993;Ma et al, 1993). As a result, the active version of the transcription factor Ci (Ci ACT ) is stabilized, which in turn leads to the transcriptional activation of dpp, a longrange morphogen (Heberlein et al, 1993;Borod and Heberlein, 1998;Fu and Baker, 2003;Pappu et al, 2003). Dpp is then used to prepare more anteriorly positioned cells for entry into the furrow (Greenwald and Struhl, 1999).…”

Section: Discussionmentioning

confidence: 99%

“…The impetus for asking the first question lies in the fact that Hh signaling is also required for furrow initiation (Ma et al, 1993;Heberlein et al, 1993;Chanut and Heberlein, 1995;Heberlein et al, 1995;Ma and Moses, 1995;Pan and Rubin, 1995;Strutt et al, 1995;Wehrli and Tomlinson, 1995). However, expression of emc under the control of either dpp or ey enhancers, both of which drive expression at the posterior margin of the disc (Blackman et al, 1991;Hauck et al, 1999), failed to have any observable effect on furrow initiation (supplementary material Fig.…”

Section: Emc Both Regulates and Cooperates With Wg Signaling To Prevementioning

confidence: 99%

“…Progression of the furrow and dpp activation are both dependent upon Hh signaling (Heberlein et al, 1993;Ma et al, 1993;Heberlein et al, 1995;Domínguez and Hafen, 1997;Borod and Heberlein, 1998). We attempted to ascertain whether furrow acceleration and increased dpp transcription within emc-null clones are due to elevated Hh signaling.…”

Section: Emc Controls the Pace Of Furrow Movement Through Regulation mentioning

confidence: 99%

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Extramacrochaetae imposes order on the Drosophila eye by refining the activity of the Hedgehog signaling gradient

Spratford

Kumar

2013

Development

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The compound eye of Drosophila melanogaster is configured by a differentiating wave, the morphogenetic furrow, that sweeps across the eye imaginal disc and transforms thousands of undifferentiated cells into a precisely ordered repetitive array of 800 ommatidia. The initiation of the furrow at the posterior margin of the epithelium and its subsequent movement across the eye field is controlled by the activity of the Hedgehog (Hh) signaling pathway. Differentiating photoreceptors that lie behind the furrow produce and secrete the Hh morphogen, which is captured by cells within the furrow itself. This leads to the stabilization of the full-length form of the zinc-finger transcription factor Cubitus interruptus (Ci155), the main effector of Hh signaling. Ci155 functions as a transcriptional activator of a number of downstream targets, including decapentaplegic (dpp), a TGFβ homolog. In this report, we describe a mechanism that is in place within the fly retina to limit Hh pathway activity within and ahead of the furrow. We demonstrate that the helix-loop-helix (HLH) protein Extramacrochaetae (Emc) regulates Ci155 levels. Loss of emc leads to an increase in Ci155 levels, nuclear migration, apical cell constriction and an acceleration of the furrow. We find that these roles are distinct from the bHLH protein Hairy (H), which we show restricts atonal (ato) expression ahead of the furrow. Secondary furrow initiation along the dorsal and ventral margins is blocked by the activity of the Wingless (Wg) pathway. We also show that Emc regulates and cooperates with Wg signaling to inhibit lateral furrow initiation.

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Section: Research Articlementioning

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Section: Emc Both Regulates and Cooperates With Wg Signaling To Prevementioning

confidence: 99%

Section: Emc Controls the Pace Of Furrow Movement Through Regulation mentioning

confidence: 99%

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Extramacrochaetae imposes order on the Drosophila eye by refining the activity of the Hedgehog signaling gradient

Spratford

Kumar

2013

Development

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“…Furthermore, no defects in the positioning of mitochondria or nuclei, were observed. Overall, although the organization of photoreceptor cell cytoplasm was mildly affected by a loss of KHC, ultrastructural changes known to correlate with serious disruptions of the recycling and secretory pathways were not seen.During eye development, cell specification is controlled through cell-cell signaling, which requires membrane proteins and secreted morphogens (Heberlein et al, 1993(Heberlein et al, , 1995Ma et al, 1995) (reviewed by Dickson and Hafen, 1993;Wolff and Ready, 1993). If photoreceptors in Khc null test clones were aberrant or missing as a consequence of poor signaling, the effect should have been nonautonomous: mutant cells could cause defects in neighboring wild-type cells, or wildtype cells could rescue the defects in neighboring mutant cells.…”

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confidence: 99%

Clonal Tests of Conventional Kinesin Function during Cell Proliferation and Differentiation

Brendza

Sheehan

Turner

et al. 2000

MBoC

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Null mutations in the Drosophila Kinesin heavy chain gene (Khc), which are lethal during the second larval instar, have shown that conventional kinesin is critical for fast axonal transport in neurons, but its functions elsewhere are uncertain. To test other tissues, single imaginal cells in young larvae were rendered null for Khc by mitotic recombination. Surprisingly, the null cells produced large clones of adult tissue. The rates of cell proliferation were not reduced, indicating that conventional kinesin is not essential for cell growth or division. This suggests that in undifferentiated cells vesicle transport from the Golgi to either the endoplasmic reticulum or the plasma membrane can proceed at normal rates without conventional kinesin. In adult eye clones produced by null founder cells, there were some defects in differentiation that caused mild ultrastructural changes, but they were not consistent with serious problems in the positioning or transport of endoplasmic reticulum, mitochondria, or vesicles. In contrast, defective cuticle deposition by highly elongated Khc null bristle shafts suggests that conventional kinesin is critical for proper secretory vesicle transport in some cell types, particularly ones that must build and maintain long cytoplasmic extensions. The ubiquity and evolutionary conservation of kinesin heavy chain argue for functions in all cells. We suggest interphase organelle movements away from the cell center are driven by multilayered transport mechanisms; that is, individual organelles can use kinesin-related proteins and myosins, as well as conventional kinesin, to move toward the cell periphery. In this case, other motors can compensate for the loss of conventional kinesin except in cells that have extremely long transport tracks. INTRODUCTIONVesicle transport is important in eukaryotic cells for the addition of material to the plasma membrane, for secretion, and for cell polarity. Active vesicle transport is thought to be driven by mechanochemical enzymes (motor proteins). Motors attach to vesicle membranes and then use ATP hydrolysis to drive unidirectional movement along polar cytoskeletal filaments. Characterized members of the myosin family of motors move toward the barbed or fast-growing ends of actin filaments with the exception of myosin VI, which moves toward the pointed or slow-growing ends (Wells et al., 1999) (reviewed by Sellers and Goodson, 1995). Actin filaments in undifferentiated and in some differentiated cell types are highly concentrated in the cortex (WatermanStorer et al., 1998; reviewed by Cramer, 1999). Cytoplasmic myosins may therefore be important for anchoring or moving vesicles when they are near the plasma membrane (Fath et al., 1994). Motors in the kinesin and dynein families move along microtubules. Characterized dyneins and members of the C-terminal kinesin subfamily move toward microtubule minus ends, whereas other kinesins that act as motors move toward microtubule plus ends (reviewed by Vale and Fletterick, 1997;Hirokawa, 1998;Goldstein and Ya...

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Divergentdecapentaplegic expression patterns in compound eye development and the evolution of insect metamorphosis

Friedrich

Benzer

2000

J. Exp. Zool.

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The TGFβ homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina

Cited by 407 publications

References 50 publications

Extramacrochaetae imposes order on the Drosophila eye by refining the activity of the Hedgehog signaling gradient

Extramacrochaetae imposes order on the Drosophila eye by refining the activity of the Hedgehog signaling gradient

Clonal Tests of Conventional Kinesin Function during Cell Proliferation and Differentiation

Divergentdecapentaplegic expression patterns in compound eye development and the evolution of insect metamorphosis

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