Advertisement
JOURNAL ARTICLES
Decoding vectorial information from a gradient: sequential roles of the receptors Frizzled and Notch in establishing planar polarity in the Drosophila eye
A. Tomlinson, G. Struhl
Development 1999 126: 5725-5738;

Summary

The Drosophila eye is composed of several hundred ommatidia that can exist in either of two chiral forms, depending on position: ommatidia in the dorsal half of the eye adopt one chiral form, whereas ommatidia in the ventral half adopt the other. Chirality appears to be specified by a polarizing signal with a high activity at the interface between the two halves (the ‘equator’), which declines in opposite directions towards the dorsal and ventral poles. Here, using genetic mosaics, we show that this polarizing signal is decoded by the sequential use of two receptor systems. The first depends on the seven-transmembrane receptor Frizzled (Fz) and distinguishes between the two members of the R3/R4 pair of presumptive photoreceptor cells, predisposing the cell that is located closer to the equator and having higher Fz activity towards the R3 photoreceptor fate and the cell further away towards the R4 fate. This bias is then amplified by subsequent interactions between the two cells mediated by the receptor Notch (N) and its ligand Delta (Dl), ensuring that the equatorial cell becomes the R3 photoreceptor while the polar cell becomes the R4 photoreceptor. As a consequence of this reciprocal cell fate decision, the R4 cell moves asymmetrically relative to the R3 cell, initiating the appropriate chiral pattern of the remaining cells of the ommatidium.

Reference

    1. Adler P. N.
    (1992) The genetic control of tissue polarity in Drosophila. BioEssays 14, 735–741
    OpenUrlCrossRefPubMedWeb of Science
    1. Adler P.N.,
    2. Krasnow R. E.,
    3. Liu J.
    (1997) Tissue polarity points from cells that have higher Frizzled levels towards cells that have lower Frizzled levels. Curr. Biol 7, 940–949
    OpenUrlCrossRefPubMedWeb of Science
    1. Bailey A. M.,
    2. Posakony J. W.
    (1995) Suppressor of Hairless directly activates transcription of Enhancer of split complex genes in response to Notch receptor activity. Genes Dev 9, 2609–.
    OpenUrlAbstract/FREE Full Text
    1. Basler K.,
    2. Siegrist P.,
    3. Hafen E.
    (1989) The spatial and temporal expression pattern of sevenless is exclusively controlled by gene-internal elements. EMBO J 8, 2381–2386
    OpenUrlPubMedWeb of Science
    1. Bhanot P.,
    2. Brink M.,
    3. Harryman Samos C.,
    4. Hsieh J.-C.,
    5. Wang Y.,
    6. Macke J. P.,
    7. Andrew D.,
    8. Nathans J.,
    9. Nusse R.
    (1996) A new member of the frizzled family from Drosophila functions as a wingless receptor. Nature 382, 225–230
    OpenUrlCrossRefPubMedWeb of Science
    1. Bowtell D. D.,
    2. Kimmel B. E.,
    3. Simon M. A.,
    4. Rubin G. M.
    (1989) Regulation of the complex pattern of sevenless expression in the developing Drosophila eye. Proc. Natl. Acad. Sci. USA 86, 6245–6249
    OpenUrlAbstract/FREE Full Text
    1. Cagan R. L.,
    2. Ready D. F.
    (1989) Notch is required for successive celldecisions in the developing Drosophila retina. Genes Dev 3, 1099–1112
    OpenUrlAbstract/FREE Full Text
    1. Cho K.-O.,
    2. Choi K.-W.
    (1998) Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature 396, 272–276
    OpenUrlCrossRefPubMed
    1. Chou T.-B.,
    2. Perrimon N.
    (1992) Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643–653
    OpenUrlAbstract/FREE Full Text
    1. Cooper M. T. D.,
    2. Bray S. J.
    (1999) Frizzled regulation of Notch signaling polarizes cell fate in the Drosophila eye. Nature 397, 526–530
    OpenUrlCrossRefPubMed
    1. Doe C. Q.,
    2. Goodman C. S.
    (1985) Early events in insect neurogenesis. II. Role of cell interactions and cell lineage in the determination of neuronal precursor cells. Dev. Biol 111, 206–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Dominguez M.,
    2. de Celis J. F.
    (1998) A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature 396, 276–278
    OpenUrlCrossRefPubMed
    1. Fanto M.,
    2. Mlodzik M.
    (1999) Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397, 523–526
    OpenUrlCrossRefPubMedWeb of Science
    1. Fortini M. E.,
    2. Rebay I.,
    3. Caron L. A.,
    4. Artavanis-Tsakonas S.
    (1993) An activated Notch receptor blocks cell-fate commitment in the developing Drosophila eye. Nature 365, 555–557
    OpenUrlCrossRefPubMedWeb of Science
    1. Foster G. G.,
    2. Suzuki D. T.
    (1970) Temperature-sensitive mutations in Drosophilamelanogaster. IV. A mutation affecting eye facet arrangement in a polarized manner. Proc. Natl. Acad. Sci. USA 67, 738–745
    OpenUrlAbstract/FREE Full Text
    1. Golic K.
    (1991) Site-specific recombination between homologous chromosomes in Drosophila. Science 252, 958–961
    OpenUrlAbstract/FREE Full Text
    1. Greenwald I.
    (1998) Lin-12/Notch signaling; lessons from worms and flies. Genes Dev 12, 1751–1762
    OpenUrlFREE Full Text
    1. Gubb D.,
    2. Garcia-Bellido A.
    (1982) A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. J. Embryol. Exp. Morph 68, 37–57
    OpenUrlPubMedWeb of Science
    1. Heitzler P.,
    2. Simpson P.
    (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64, 1083–1092
    OpenUrlCrossRefPubMedWeb of Science
    1. Klemenz R.,
    2. Weber U.,
    3. Gehring W. J.
    (1987) The white gene as a marker in a new P-element vector for gene transfer in Drosophila. Nucleic Acids Res 15, 3947–3959
    OpenUrlAbstract/FREE Full Text
    1. Lawrence P. A.
    (1966) Gradients in the insect segment: The orientation of hairs in the milkweed bug Oncopeltus fasciatus. J. Exp. Biol 44, 607–620
    OpenUrlAbstract/FREE Full Text
    1. Lecourtois M.,
    2. Schweisguth F.
    (1995) The neurogenic Suppressor of Hairless DNA-binding protein mediates the transcriptional activation of the Enhancer of split Complex genes triggered by Notch signaling. Genes Dev 9, 2598–2608
    OpenUrlAbstract/FREE Full Text
    1. Papayannopoulos V. P.,
    2. Tomlinson A.,
    3. Panin V. M.,
    4. Rauskolb C. R.,
    5. Irvine K. D.
    (1998) Dorsal-ventral signaling in the Drosophila eye. Science 281, 2031–2034
    OpenUrlAbstract/FREE Full Text
    1. Schweisguth F.,
    2. Posakony J. W.
    (1992) Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein gene, controls sensory organ cell fates. Cell 69, 1199–1212
    OpenUrlCrossRefPubMedWeb of Science
    1. Seydoux G.,
    2. Greenwald I.
    (1989) Cell autonomy of lin-12 function in a cell fate decision in C. elegans. Cell 57, 1237–1245
    OpenUrlCrossRefPubMedWeb of Science
    1. Struhl G.,
    2. Adachi A.
    (1998) Nuclear Access and Action of Notch in vivo. Cell 93, 649–660
    OpenUrlCrossRefPubMedWeb of Science
    1. Struhl G.,
    2. Barbash A.,
    3. Lawrence P. A.
    (1997) Hedgehog acts by distinct gradient and signal relay mechanisms to organise cell type and polarity in the Drosophilla abdomen. Development 124, 2155–2165
    OpenUrlAbstract
    1. Struhl G.,
    2. Basler K.
    (1993) Organizing activity of Wingless protein in Drosophila. Cell 72, 527–540
    OpenUrlCrossRefPubMedWeb of Science
    1. Struhl G.,
    2. Fitzgerald K.,
    3. Greenwald I.
    (1993) Intrinsic activity of the lin-12 and Notch intracellular domains in vivo. Cell 74, 331–345
    OpenUrlCrossRefPubMedWeb of Science
    1. Stumpf H.
    (1966) Mechanism by which cells estimate their location in the body. Nature 212, 430–431
    OpenUrlCrossRefPubMed
    1. Tomlinson A.
    (1985) The cellular dynamics of pattern formation in the eye of Drosophila. J. Embryol. Exp. Morph 89, 313–331
    OpenUrlPubMedWeb of Science
    1. Tomlinson A.,
    2. Strapps W. R.,
    3. Heemskerk J.
    (1997) Linking Frizzled and Wnt signaling in Drosophila development. Development 124, 4515–4521
    OpenUrlAbstract
    1. Tomlinson A.,
    2. Ready D. F.
    (1987) Cell fate in the Drosophila ommatidium. Dev. Biol 123, 264–275
    OpenUrlCrossRefPubMedWeb of Science
    1. Vinson C.,
    2. Adler P. N.
    (1987) Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 329, 549–551
    OpenUrlCrossRefPubMed
    1. Vinson C. R.,
    2. Conover S.,
    3. Adler P. N.
    (1989) A Drosophila tissue polarity locus Frizzled encodes a protein containing seven potential transmembrane domain. Nature 338, 263–264
    OpenUrlCrossRefPubMed
    1. Wehrli M.,
    2. Tomlinson A.
    (1998) Independent regulation of anterior/posterior and equatorial /polar polarity in the Drosophila eye; evidence for the involvement of Wnt signaling in the equatorial/polar axis. Development 125, 1421–1432
    OpenUrlAbstract
    1. Wilkinson H. A.,
    2. Fitzgerald K.,
    3. Greenwald I.
    (1994) Reciprocal changes in expression of the receptor lin-12 and its ligand lag-2 prior ro commitment in a C. elegans cell fate decision. Cell 79, 1187–1198
    OpenUrlCrossRefPubMedWeb of Science
    1. Wolff T.,
    2. Rubin G. M.
    (1998) Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125, 1149–1159
    OpenUrlAbstract
    1. Xu T.,
    2. Rubin G. M.
    (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237
    OpenUrlAbstract
    1. Zheng L.,
    2. Zhang J.,
    3. Carthew R. W.
    (1995) frizzled regulates mirror-symmetric pattern formation in the Drosophila eye. Development 121, 3045–3055
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Decoding vectorial information from a gradient: sequential roles of the receptors Frizzled and Notch in establishing planar polarity in the Drosophila eye
A. Tomlinson, G. Struhl
Development 1999 126: 5725-5738;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

A new society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.

Upcoming special issue: call for papers

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.