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JOURNAL ARTICLES
Lineage-tracing cells born in different domains along the PD axis of the developing Drosophila leg
K. Weigmann, S.M. Cohen
Development 1999 126: 3823-3830;

Summary

Patterning of the developing limbs by the secreted signaling proteins Wingless, Hedgehog and Dpp takes place while the imaginal discs are growing rapidly. Cells born in regions of high ligand concentration may be displaced through growth to regions of lower ligand concentration. We have used a novel lineage-tagging method to address the reversibility of cell fate specification by morphogen gradients. We find that responses to Hedgehog and Dpp in the wing disc are readily reversible. In the leg, we find that cells readily adopt more distal fates, but do not normally shift from distal to proximal fate. However, they can do so if given a growth advantage. These results indicate that cell fate specification by morphogen gradients remains largely reversible while the imaginal discs grow. In other systems, where growth and patterning are uncoupled, nonreversible specification events or ‘ratchet’ effects may be of functional significance.

Reference

    1. Abu-Shaar M.,
    2. Mann R.
    (1998) Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 125, 3821–3830
    OpenUrlAbstract
    1. Basler K.,
    2. Struhl G.
    (1994) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208–214
    OpenUrlCrossRefPubMedWeb of Science
    1. Brand A.,
    2. Perrimon N.
    (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
    OpenUrlAbstract
    1. Britton J. S.,
    2. Edgar B. A.
    (1998) Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125, 2149–2158
    OpenUrlAbstract
    1. Bryant S. V.,
    2. French V.,
    3. Bryant P. J.
    (1981) Distal regeneration and symmetry. Science 212, 993–1002
    OpenUrlAbstract/FREE Full Text
    1. Calleja M.,
    2. Moreno E.,
    3. Pelaz S.,
    4. Morata G.
    (1996) Visualization of gene expression in living adult Drosophila. Science 274, 252–255
    OpenUrlAbstract/FREE Full Text
    1. Campbell G.,
    2. Tomlinson A.
    (1998) The roles of homeobox genes aristaless and Distal-less in patterning legs and wings of Drosophila. Development 125, 4483–4493
    OpenUrlAbstract
    1. Cohen B.,
    2. Simcox A. A.,
    3. Cohen S. M.
    (1993) Allocation of the thoracic imaginal disc primordia in the Drosophila embryo. Development 117, 597–608
    OpenUrlAbstract
    1. Cohen S. M.,
    2. Jurgens G.
    (1989) Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development. EMBO J 8, 2045–2055
    OpenUrlPubMedWeb of Science
    1. de Celis J. F.,
    2. Barrio R.,
    3. Kafatos F. C.
    (1996) A gene complex acting downstream of dpp in Drosophila wing morphogenesis. Nature 381, 421–424
    OpenUrlCrossRefPubMed
    1. Diaz-Benjumea F. J.,
    2. Cohen B.,
    3. Cohen S. M.
    (1994) Cell interactions between compartments establishes the proximal-distal axis of Drosophila limbs. Nature 372, 175–179
    OpenUrlCrossRefPubMed
    1. Duncan D. M.,
    2. Burgess E. A.,
    3. Duncan I.
    (1998) Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor. Genes Dev 12, 1290–1303
    OpenUrlAbstract/FREE Full Text
    1. Dyson S.,
    2. Gurdon J. B.
    (1998) The interpretation of position in amorphogen gradient as revealed by occupancy of Activin receptors. Cell 93, 557–568
    OpenUrlCrossRefPubMedWeb of Science
    1. Fasano L.,
    2. Röder L.,
    3. Core N.,
    4. Alexandre E. C. V.,
    5. Jacq B.,
    6. Kerridge S.
    (1991) The gene teashirt is required for development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs. Cell 64, 63–79
    OpenUrlCrossRefPubMedWeb of Science
    1. French V.,
    2. Bryant P. J.,
    3. Bryant S. V.
    (1976) Pattern regulation in epimorphic fields. Science 193, 969–981
    OpenUrlAbstract/FREE Full Text
    1. Gorfinkiel N.,
    2. Morata G.,
    3. Guerrero I.
    (1997) The homeobox gene Distal-less induces ventral appendage development in Drosophila. Genes Dev 11, 2259–2271
    OpenUrlAbstract/FREE Full Text
    1. Gurdon J. B.,
    2. Harger P.,
    3. Mitchell A.,
    4. Lemaire P.
    (1994) Activin signalling and response to a morphogen gradient. Nature 371, 487–492
    OpenUrlCrossRefPubMed
    1. Gurdon J. B.,
    2. Mitchell A.,
    3. Mahoney D.
    (1995) Direct and continuous assessment by cells of their position in a morphogen gradient. Nature 376, 520–521
    OpenUrlCrossRefPubMed
    1. Kuhnlein R. P.,
    2. Frommer G.,
    3. Friedrich M.,
    4. GonzalezGaitan M.,
    5. Weber A.,
    6. Wagner-Bernholz J. F.,
    7. Gehring W. J.,
    8. Jäckle H.,
    9. Schuh R.
    (1994) spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo. EMBO J 13, 168–179
    OpenUrlPubMedWeb of Science
    1. Lawrence P. A.,
    2. Struhl G.
    (1996) Morphogens, compartments and pattern: lessons from Drosophila?. Cell 85, 951–961
    OpenUrlCrossRefPubMedWeb of Science
    1. Lecuit T.,
    2. Brook W. J.,
    3. Ng M.,
    4. Calleja M.,
    5. Sun H.,
    6. Cohen S. M.
    (1996) Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381, 387–393
    OpenUrlCrossRefPubMedWeb of Science
    1. Lecuit T.,
    2. Cohen S. M.
    (1997) Proximal-distal axis formation in the Drosophila leg. Nature 388, 139–145
    OpenUrlCrossRefPubMed
    1. Lecuit T.,
    2. Cohen S. M.
    (1998) Dpp receptor levels contribute to shaping the Dpp morphogen gradient in the Drosophila wing imaginal disc. Development 125, 4901–4907
    OpenUrlAbstract
    1. Mardon G.,
    2. Solomon N. M.,
    3. Rubin G. M.
    (1994) dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120, 3473–3486
    OpenUrlAbstract
    1. Morimura S.,
    2. Maves L.,
    3. Chen Y.,
    4. Hoffmann F. M.
    (1996) decapentaplegic overexpression affects Drosophila wing and leg imaginal disc development and wingless expression. Dev. Biol 177, 136–151
    OpenUrlCrossRefPubMedWeb of Science
    1. Nellen D.,
    2. Burke R.,
    3. Struhl G.,
    4. Basler K.
    (1996) Direct and long-range action of a Dpp morphogen gradient. Cell 85, 357–368
    OpenUrlCrossRefPubMedWeb of Science
    1. Neumann C. J.,
    2. Cohen S. M.
    (1996) A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing. Development 122, 3477–3485
    OpenUrlAbstract
    1. Neumann C. J.,
    2. Cohen S. M.
    (1997) Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 124, 871–880
    OpenUrlAbstract
    1. Neumann C. J.,
    2. Cohen S. M.
    (1997) Morphogens and pattern formation. BioEssays 19, 721–729
    OpenUrlCrossRefPubMedWeb of Science
    1. Ng M.,
    2. Diaz-Benjumea F. J.,
    3. Vincent J.-P.,
    4. Wu J.,
    5. Cohen S. M.
    (1996) Specification of the wing primordium in Drosophila. Nature 381, 316–319
    OpenUrlCrossRefPubMed
    1. Nichols M.,
    2. Rientjes J. M. R.,
    3. Logie C.,
    4. Stewart A. F.
    (1997) FLP recombinase/Estrogen receptor fusion proteins require the receptor D domain for response to antagonists but not agonists. Mol. Endo 11, 950–961
    OpenUrlCrossRefPubMedWeb of Science
    1. Schubiger G.,
    2. Schubiger M.
    (1978) Distal transformation in Drosophila leg imaginal disc fragments. Dev. Biol 67, 286–295
    OpenUrlCrossRefPubMedWeb of Science
    1. Singer M. A.,
    2. Penton A.,
    3. Twombly V.,
    4. Hoffmann F. M.,
    5. Gelbart W. M.
    (1997) Signaling through both type I Dpp receptors is required for anterior-posterior patterning of the entire Drosophila wing. Development 124, 79–89
    OpenUrlAbstract
    1. Strigini M.,
    2. Cohen S. M.
    (1997) A Hedgehog activity gradient contributes to AP axial patterning of the Drosophila wing. Development 124, 4697–4705
    OpenUrlAbstract
    1. Struhl G.,
    2. Basler K.
    (1993) Organizing activity of wingless protein in Drosophila. Cell 72, 527–540
    OpenUrlCrossRefPubMedWeb of Science
    1. Tabata T.,
    2. Kornberg T.
    (1994) Hedgehog is a signalling protein with a key role in patterning Drosophila imaginal discs. Cell 76, 89–102
    OpenUrlCrossRefPubMedWeb of Science
    1. Thomas U.,
    2. Jönsson F.,
    3. Speicher S. A.,
    4. Knust E.
    (1995) Phenotypic and molecular characterization of SerD, a dominant allele of the Drosophila gene Serrate. Genetics 139, 203–213
    OpenUrlAbstract/FREE Full Text
    1. Wu J.,
    2. Cohen S. M.
    (1999) Proximal distal axis formation in the Drosophila leg: Primary subdivision into proximal and distal domains by Homothorax, Teashirt and Distal-less expression. Development 126, 109–117
    OpenUrlAbstract
    1. Zecca M.,
    2. Basler K.,
    3. Struhl G.
    (1996) Direct and long-range action of a Wingless morphogen gradient. Cell 87, 833–844
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Lineage-tracing cells born in different domains along the PD axis of the developing Drosophila leg
K. Weigmann, S.M. Cohen
Development 1999 126: 3823-3830;
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