|
|
|
|||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
Development, Vol 124, Issue 2 261-270, Copyright © 1997 by Company of Biologists
JOURNAL ARTICLES |
M Freeman
MRC Laboratory of Molecular Biology, Cambridge, UK. mf1@mrc-lmb.cam.ac.uk
Cells in the Drosophila eye are determined by inductive signalling. Here I describe a new model of eye development that explains how simple intercellular signals could specify the diverse cell types that constitute the ommatidium. This model arises from the recent observation that the Drosophila homologue of the EGF receptor (DER) is used reiteratively to trigger the differentiation of each of the cell types--successive rounds of DER activation recruit first the photoreceptors, then cone and finally pigment cells. It seems that a cell's identity is not determined by the specific signal that induces it, but is instead a function of the state of the cell when it receives the signal. DER signalling is activated by the ligand, Spitz, and inhibited by the secreted protein, Argos. Spitz is initially produced by the central cells in the ommatidium and diffuses over a small distance. Argos has a longer range, allowing it to block more distal cells from being activated by low levels of Spitz; I have termed this interplay between a short-range activator and a long-range inhibitor 'remote inhibition'. Since inductive signalling is common in many organisms and its components have been conserved, it is possible that the logic of signalling may also be conserved.
This article has been cited by other articles:
![]() |
J. L. Fetting, S. A. Spencer, and T. Wolff The cell adhesion molecules Echinoid and Friend of Echinoid coordinate cell adhesion and cell signaling to regulate the fidelity of ommatidial rotation in the Drosophila eye Development, October 1, 2009; 136(19): 3323 - 3333. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. J. Zartman, J. S. Kanodia, L. S. Cheung, and S. Y. Shvartsman Feedback control of the EGFR signaling gradient: superposition of domain-splitting events in Drosophila oogenesis Development, September 1, 2009; 136(17): 2903 - 2911. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. T. Pickup, L. Ming, and H. D. Lipshitz Hindsight modulates Delta expression during Drosophila cone cell induction Development, March 15, 2009; 136(6): 975 - 982. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Melicharek, A. Shah, G. DiStefano, A. J. Gangemi, A. Orapallo, A. D. Vrailas-Mortimer, and D. R. Marenda Identification of Novel Regulators of atonal Expression in the Developing Drosophila Retina Genetics, December 1, 2008; 180(4): 2095 - 2110. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. W Shingleton, C. K Mirth, and P. W Bates Developmental model of static allometry in holometabolous insects Proc R Soc B, August 22, 2008; 275(1645): 1875 - 1885. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. McNeill, G. M. Craig, and J. M. Bateman Regulation of Neurogenesis and Epidermal Growth Factor Receptor Signaling by the Insulin Receptor/Target of Rapamycin Pathway in Drosophila Genetics, June 1, 2008; 179(2): 843 - 853. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. I. Miura, J.-Y. Roignant, M. Wassef, and J. E. Treisman Myopic acts in the endocytic pathway to enhance signaling by the Drosophila EGF receptor Development, June 1, 2008; 135(11): 1913 - 1922. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Keller and C. R. L. Thompson Cell type specificity of a diffusible inducer is determined by a GATA family transcription factor Development, May 1, 2008; 135(9): 1635 - 1645. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Tran, F. Hamada, T. Schwarz-Romond, and M. Bienz Trabid, a new positive regulator of Wnt-induced transcription with preference for binding and cleaving K63-linked ubiquitin chains Genes & Dev., February 15, 2008; 22(4): 528 - 542. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Silies, Y. Yuva, D. Engelen, A. Aho, T. Stork, and C. Klambt Glial Cell Migration in the Eye Disc J. Neurosci., November 28, 2007; 27(48): 13130 - 13139. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Duan, C. Zhang, J. Chen, H. Sink, E. Frei, and M. Noll A key role of Pox meso in somatic myogenesis of Drosophila Development, November 15, 2007; 134(22): 3985 - 3997. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Gabut, J. Dejardin, J. Tazi, and J. Soret The SR Family Proteins B52 and dASF/SF2 Modulate Development of the Drosophila Visual System by Regulating Specific RNA Targets Mol. Cell. Biol., April 15, 2007; 27(8): 3087 - 3097. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Nagaraj and U. Banerjee Combinatorial signaling in the specification of primary pigment cells in the Drosophila eye Development, March 1, 2007; 134(5): 825 - 831. [Abstract] [Full Text] [PDF] |
||||
![]() |
N.-S. Moon, L. Di Stefano, and N. Dyson A Gradient of Epidermal Growth Factor Receptor Signaling Determines the Sensitivity of rbf1 Mutant Cells to E2F-Dependent Apoptosis Mol. Cell. Biol., October 15, 2006; 26(20): 7601 - 7615. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Alvarado, T. A. Evans, R. Sharma, M. A. Lemmon, and J. B. Duffy Argos Mutants Define an Affinity Threshold for Spitz Inhibition in Vivo J. Biol. Chem., September 29, 2006; 281(39): 28993 - 29001. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Jones, R. Reifegerste, and K. Moses Characterization of Drosophila mini-me, a Gene Required for Cell Proliferation and Survival Genetics, June 1, 2006; 173(2): 793 - 808. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. D. Vrailas, D. R. Marenda, S. E. Cook, M. A. Powers, J. A. Lorenzen, L. A. Perkins, and K. Moses smoothened and thickveins regulate Moleskin/Importin 7-mediated MAP kinase signaling in the developing Drosophila eye Development, April 15, 2006; 133(8): 1485 - 1494. [Abstract] [Full Text] [PDF] |
||||
![]() |
J.-Y. Roignant, S. Hamel, F. Janody, and J. E. Treisman The novel SAM domain protein Aveugle is required for Raf activation in the Drosophila EGF receptor signaling pathway. Genes & Dev., April 1, 2006; 20(7): 795 - 806. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Y. Yampolsky, C. Allen, S. A. Shabalina, and A. S. Kondrashov Persistence Time of Loss-of-Function Mutations at Nonessential Loci Affecting Eye Color in Drosophila melanogaster Genetics, December 1, 2005; 171(4): 2133 - 2138. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. B. Rodrigues, E. Werner, and K. Moses Genetic and biochemical analysis of the role of Egfr in the morphogenetic furrow of the developing Drosophila eye Development, November 1, 2005; 132(21): 4697 - 4707. [Abstract] [Full Text] [PDF] |
||||
![]() |
B.-Z. Shilo Regulating the dynamics of EGF receptor signaling in space and time Development, September 15, 2005; 132(18): 4017 - 4027. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. A. Grzeschik and E. Knust IrreC/rst-mediated cell sorting during Drosophila pupal eye development depends on proper localisation of DE-cadherin Development, May 1, 2005; 132(9): 2035 - 2045. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. S.-M. Zhang, J. Wei, H. Qin, L. Zhang, B. Xie, P. Hui, A. Deisseroth, C. J. Barnstable, and X.-Y. Fu STAT3-Mediated Signaling in the Determination of Rod Photoreceptor Cell Fate in Mouse Retina Invest. Ophthalmol. Vis. Sci., July 1, 2004; 45(7): 2407 - 2412. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Gu, J. Yang, K. A. Mitchell, and J. E. O'Tousa Drosophila NinaB and NinaD Act Outside of Retina to Produce Rhodopsin Chromophore J. Biol. Chem., April 30, 2004; 279(18): 18608 - 18613. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Urban, G. Brown, and M. Freeman EGF receptor signalling protects smooth-cuticle cells from apoptosis during Drosophila ventral epidermis development Development, April 15, 2004; 131(8): 1835 - 1845. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. J. Hwang and P. W. Sternberg A cell-specific enhancer that specifies lin-3 expression in the C. elegans anchor cell for vulval development Development, January 1, 2004; 131(1): 143 - 151. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. G. Voas and I. Rebay The Novel Plant Homeodomain Protein Rhinoceros Antagonizes Ras Signaling in the Drosophila Eye Genetics, December 1, 2003; 165(4): 1993 - 2006. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Gaengel and M. Mlodzik Egfr signaling regulates ommatidial rotation and cell motility in the Drosophila eye via MAPK/Pnt signaling and the Ras effector Canoe/AF6 Development, November 15, 2003; 130(22): 5413 - 5423. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. E. Brown and M. Freeman Egfr signalling defines a protective function for ommatidial orientation in the Drosophila eye Development, November 15, 2003; 130(22): 5401 - 5412. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. Fu and N. E. Baker Deciphering synergistic and redundant roles of Hedgehog, Decapentaplegic and Delta that drive the wave of differentiation in Drosophila eye development Development, November 1, 2003; 130(21): 5229 - 5239. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. P. Kumar, F. Hsiung, M. A. Powers, and K. Moses Nuclear translocation of activated MAP kinase is developmentally regulated in the developing Drosophila eye Development, August 15, 2003; 130(16): 3703 - 3714. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Mankidy, J. Hastings, and J. R. Thackeray Distinct Phospholipase C-{gamma}-Dependent Signaling Pathways in the Drosophila Eye and Wing Are Revealed by a New small wing Allele Genetics, June 1, 2003; 164(2): 553 - 563. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. J. Frankfort and G. Mardon R8 development in the Drosophila eye: a paradigm for neural selection and differentiation Development, March 5, 2003; 129(6): 1295 - 1306. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Roch, G. Jimenez, and J. Casanova EGFR signalling inhibits Capicua-dependent repression during specification of Drosophila wing veins Development, March 4, 2003; 129(4): 993 - 1002. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Gallio, G. Sturgill, P. Rather, and P. Kylsten A conserved mechanism for extracellular signaling in eukaryotes and prokaryotes PNAS, September 17, 2002; 99(19): 12208 - 12213. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. K. Shamloula, M. P. Mbogho, A. C. Pimentel, Z. M. A. Chrzanowska-Lightowlers, V. Hyatt, H. Okano, and T. R. Venkatesh rugose (rg), a Drosophila A kinase Anchor Protein, Is Required for Retinal Pattern Formation and Interacts Genetically With Multiple Signaling Pathways Genetics, June 1, 2002; 161(2): 693 - 710. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. E. Egan, A. B. Hall, B. A. Yatsula, and D. Bar-Sagi The bimodal regulation of epidermal growth factor signaling by human Sprouty proteins PNAS, April 30, 2002; 99(9): 6041 - 6046. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Chanut, K. Woo, S. Pereira, T. J. Donohoe, S.-Y. Chang, T. R. Laverty, A. P. Jarman, and U. Heberlein Rough eye Is a Gain-of-Function Allele of amos That Disrupts Regulation of the Proneural Gene atonal During Drosophila Retinal Differentiation Genetics, February 1, 2002; 160(2): 623 - 635. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Baonza and M. Freeman Notch signalling and the initiation of neural development in the Drosophila eye Development, October 15, 2001; 128(20): 3889 - 3898. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Jiao, M. Daube, H. Duan, Y. Zou, E. Frei, and M. Noll Headless flies generated by developmental pathway interference Development, September 1, 2001; 128(17): 3307 - 3319. [Abstract] [Full Text] [PDF] |
||||
![]() |
H.-S. Yoon and J. W. Golden PatS and Products of Nitrogen Fixation Control Heterocyst Pattern J. Bacteriol., April 15, 2001; 183(8): 2605 - 2613. [Abstract] [Full Text] |
||||
![]() |
L Yang and N. Baker Role of the EGFR/Ras/Raf pathway in specification of photoreceptor cells in the Drosophila retina Development, January 4, 2001; 128(7): 1183 - 1191. [Abstract] [PDF] |
||||
![]() |
F Wittwer, A van der Straten, K Keleman, B. Dickson, and E Hafen Lilliputian: an AF4/FMR2-related protein that controls cell identity and cell growth Development, January 3, 2001; 128(5): 791 - 800. [Abstract] [PDF] |
||||
![]() |
J Bai, W Chiu, J Wang, T Tzeng, N Perrimon, and J Hsu The cell adhesion molecule Echinoid defines a new pathway that antagonizes the Drosophila EGF receptor signaling pathway Development, January 2, 2001; 128(4): 591 - 601. [Abstract] [PDF] |
||||
![]() |
F. Chanut, A. Luk, and U. Heberlein A Screen for Dominant Modifiers of roDom, a Mutation That Disrupts Morphogenetic Furrow Progression in Drosophila, Identifies Groucho and Hairless as Regulators of atonal Expression Genetics, November 1, 2000; 156(3): 1203 - 1217. [Abstract] [Full Text] |
||||
![]() |
Y.-C. Su, C. Maurel-Zaffran, J. E. Treisman, and E. Y. Skolnik The Ste20 Kinase Misshapen Regulates Both Photoreceptor Axon Targeting and Dorsal Closure, Acting Downstream of Distinct Signals Mol. Cell. Biol., July 1, 2000; 20(13): 4736 - 4744. [Abstract] [Full Text] |
||||
![]() |
J. D. Wasserman, S. Urban, and M. Freeman A family of rhomboid-like genes: Drosophila rhomboid-1 and roughoid/rhomboid-3 cooperate to activate EGF receptor signaling Genes & Dev., July 1, 2000; 14(13): 1651 - 1663. [Abstract] [Full Text] |
||||
![]() |
U Weber, N Paricio, and M Mlodzik Jun mediates Frizzled-induced R3/R4 cell fate distinction and planar polarity determination in the Drosophila eye Development, January 8, 2000; 127(16): 3619 - 3629. [Abstract] [PDF] |
||||
![]() |
L Galli-Resta Local, possibly contact-mediated signalling restricted to homotypic neurons controls the regular spacing of cells within the cholinergic arrays in the developing rodent retina Development, January 4, 2000; 127(7): 1509 - 1516. [Abstract] [PDF] |
||||
![]() |
C Pazman, C. Mayes, M Fanto, S. Haynes, and M Mlodzik Rasputin, the Drosophila homologue of the RasGAP SH3 binding protein, functions in ras- and Rho-mediated signaling Development, January 4, 2000; 127(8): 1715 - 1725. [Abstract] [PDF] |
||||
![]() |
T. Newsome, B Asling, and B. Dickson Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics Development, January 2, 2000; 127(4): 851 - 860. [Abstract] [PDF] |
||||
![]() |
Z.-C. Lai and Y. Li Tramtrack69 Is Positively and Autonomously Required for Drosophila Photoreceptor Development Genetics, May 1, 1999; 152(1): 299 - 305. [Abstract] [Full Text] |
||||
![]() |
C.-K. Chen and C.-T. Chien Negative regulation of atonal in proneural cluster formation of Drosophila R8 photoreceptors PNAS, April 27, 1999; 96(9): 5055 - 5060. [Abstract] [Full Text] [PDF] |
||||
![]() |
X. Dong, L. Tsuda, K. H. Zavitz, M. Lin, S. Li, R. W. Carthew, and S. L. Zipursky ebi regulates epidermal growth factor receptor signaling pathways in Drosophila Genes & Dev., April 15, 1999; 13(8): 954 - 965. [Abstract] [Full Text] |
||||
![]() |
S Greenwood and G Struhl Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway Development, January 12, 1999; 126(24): 5795 - 5808. [Abstract] [PDF] |
||||
![]() |
A Daniel, K Dumstrei, J. Lengyel, and V Hartenstein The control of cell fate in the embryonic visual system by atonal, tailless and EGFR signaling Development, January 7, 1999; 126(13): 2945 - 2954. [Abstract] [PDF] |
||||
![]() |
S Kramer, M Okabe, N Hacohen, M. Krasnow, and Y Hiromi Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila Development, January 6, 1999; 126(11): 2515 - 2525. [Abstract] [PDF] |
||||
![]() |
A Amin, Y Li, and R Finkelstein Hedgehog activates the EGF receptor pathway during Drosophila head development Development, January 6, 1999; 126(12): 2623 - 2630. [Abstract] [PDF] |
||||
![]() |
P zur Lage and A. Jarman Antagonism of EGFR and notch signalling in the reiterative recruitment of Drosophila adult chordotonal sense organ precursors Development, January 6, 1999; 126(14): 3149 - 3157. [Abstract] [PDF] |
||||
![]() |
R Sharma-Kishore, J. White, E Southgate, and B Podbilewicz Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis Development, January 2, 1999; 126(4): 691 - 699. [Abstract] [PDF] |
||||
![]() |
R Chen, G Halder, Z Zhang, and G Mardon Signaling by the TGF-beta homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila Development, January 2, 1999; 126(5): 935 - 943. [Abstract] [PDF] |
||||
![]() |
Y. Zhang, L. Cao, C. G. Kiani, B. L. Yang, and B. B. Yang The G3 Domain of Versican Inhibits Mesenchymal Chondrogenesis via the Epidermal Growth Factor-like Motifs J. Biol. Chem., December 4, 1998; 273(49): 33054 - 33063. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Yoon and J. W. Golden Heterocyst Pattern Formation Controlled by a Diffusible Peptide Science, October 30, 1998; 282(5390): 935 - 938. [Abstract] [Full Text] |
||||
![]() |
B. Kerber, S. Fellert, and M. Hoch Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney Genes & Dev., June 15, 1998; 12(12): 1781 - 1786. [Abstract] [Full Text] |
||||
![]() |
S. Spencer, P. Powell, D. Miller, and R. Cagan Regulation of EGF receptor signaling establishes pattern across the developing Drosophila retina Development, January 12, 1998; 125(23): 4777 - 4790. [Abstract] [PDF] |
||||
![]() |
J. Kumar, M Tio, F Hsiung, S Akopyan, L Gabay, R Seger, B. Shilo, and K Moses Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation Development, January 10, 1998; 125(19): 3875 - 3885. [Abstract] [PDF] |
||||
![]() |
K Dumstrei, C Nassif, G Abboud, A Aryai, A Aryai, and V Hartenstein EGFR signaling is required for the differentiation and maintenance of neural progenitors along the dorsal midline of the Drosophila embryonic head Development, January 9, 1998; 125(17): 3417 - 3426. [Abstract] [PDF] |
||||
![]() |
C. Brennan, M Ashburner, and K Moses Ecdysone pathway is required for furrow progression in the developing Drosophila eye Development, January 7, 1998; 125(14): 2653 - 2664. [Abstract] [PDF] |
||||
![]() |
E Buff, A Carmena, S Gisselbrecht, F Jimenez, and A. Michelson Signalling by the Drosophila epidermal growth factor receptor is required for the specification and diversification of embryonic muscle progenitors Development, January 6, 1998; 125(11): 2075 - 2086. [Abstract] [PDF] |
||||
![]() |
G. Thomas, D. Zarnescu, A. Juedes, M. Bales, A Londergan, C. Korte, and D. Kiehart Drosophila betaHeavy-spectrin is essential for development and contributes to specific cell fates in the eye Development, January 6, 1998; 125(11): 2125 - 2134. [Abstract] [PDF] |
||||
![]() |
G Halder, P Callaerts, S Flister, U Walldorf, U Kloter, and W. Gehring Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development Development, January 6, 1998; 125(12): 2181 - 2191. [Abstract] [PDF] |
||||
![]() |
D. Miller and R. Cagan Local induction of patterning and programmed cell death in the developing Drosophila retina Development, January 6, 1998; 125(12): 2327 - 2335. [Abstract] [PDF] |
||||
![]() |
Q. Li, I. K. Hariharan, F. Chen, Y. Huang, and J. A. Fischer Genetic interactions with Rap1 and Ras1 reveal a second function for the Fat facets deubiquitinating enzyme in Drosophila eye development PNAS, November 11, 1997; 94(23): 12515 - 12520. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. Fu and M. Noll The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye Genes & Dev., August 15, 1997; 11(16): 2066 - 2078. [Abstract] [Full Text] [PDF] |
||||
![]() |
G Begemann, N Paricio, R Artero, I Kiss, M Perez-Alonso, and M Mlodzik muscleblind, a gene required for photoreceptor differentiation in Drosophila, encodes novel nuclear Cys3His-type zinc-finger-containing proteins Development, January 11, 1997; 124(21): 4321 - 4331. [Abstract] [PDF] |
||||
![]() |
C Stemerdink and J. Jacobs Argos and Spitz group genes function to regulate midline glial cell number in Drosophila embryos Development, January 10, 1997; 124(19): 3787 - 3796. [Abstract] [PDF] |
||||
![]() |
A. Queenan, A Ghabrial, and T Schupbach Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo Development, January 10, 1997; 124(19): 3871 - 3880. [Abstract] [PDF] |
||||
![]() |
D Szuts, M Freeman, and M Bienz Antagonism between EGFR and Wingless signalling in the larval cuticle of Drosophila Development, January 8, 1997; 124(16): 3209 - 3219. [Abstract] [PDF] |
||||
![]() |
Y. Sun, L. Y. Jan, and Y. N. Jan Ectopic scute induces Drosophila ommatidia development without R8 founder photoreceptors PNAS, June 6, 2000; 97(12): 6815 - 6819. [Abstract] [Full Text] [PDF] |
||||