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JOURNAL ARTICLES
four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila
J.L. Villano, F.N. Katz
Development 1995 121: 2767-2777;

Summary

Genes capable of translating positional information into regulated growth lie at the heart of morphogenesis, yet few genes with this function have been identified. Mutants in the Drosophila four-jointed (fj) gene show reduced growth and altered differentiation only within restricted sectors of the proximal-distal (PD) axis in the leg and wing, thus fj is a candidate for a gene with this coordination function. Consistent with a position-sensitive role, we show that fj is expressed in a regional pattern in the developing leg, wing, eye and optic lobe. The fj gene encodes a novel type II membrane glycoprotein. When the cDNA is translated in an in vitro translation system in the presence of exogenous microsomal membranes, the intralumenal portion of some of the molecules is cleaved, yielding a secreted C-terminal fragment. We propose that fj encodes a secreted signal that functions as a positive regulator of regional growth and differentiation along the PD axis of the imaginal discs.

Reference

    1. Ashley J. A.,
    2. Katz F. N.
    (1994) Competition and position-dependent targeting in the development of the Drosophila R7 visual projections. Development 120, 1537–1547
    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. Bellen H. J.,
    2. O'Kane C.J.,
    3. Wilson C.,
    4. Grossniklaus U.,
    5. Pearson R.K.,
    6. Gehring W. J.
    (1989) P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev 3, 1288–1300
    OpenUrlAbstract/FREE Full Text
    1. Bier E.,
    2. Vaessin H.,
    3. Shepherd S.,
    4. Lee K.,
    5. McCall K.,
    6. Barbel S.,
    7. Ackerman L.,
    8. Carretto R.,
    9. Uemura T.,
    10. Grell E.,
    11. Jan L. Y.,
    12. Jan Y.N.
    (1989) Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev 3, 1273–1287
    OpenUrlAbstract/FREE Full Text
    1. Boedigheimer M.,
    2. Laughon A.
    (1993) expanded: a gene involved in the control of cell proliferation in imaginal discs. Development 118, 1291–1301
    OpenUrlAbstract/FREE Full Text
    1. Bryant P. J.
    (1993) The polar coordinate model goes molecular. Science 259, 471–472
    OpenUrlFREE Full Text
    1. Bryant P. J.,
    2. Huettner B.,
    3. Held L. I.,
    4. Ryerse J.,
    5. Szidonya J.
    (1988) Mutations at the fat locus interfere with cell proliferation control and epithelial morphogenesis in Drosophila. Dev. Biol 129, 541–554
    OpenUrlCrossRefPubMedWeb of Science
    1. Buckles G. R.,
    2. Smith Z. D. M.,
    3. Katz F. N.
    (1992) mip causes hyperinnervation of a retinotopic map in Drosophila by excessive recruitment of R7 photoreceptor cells. Neuron 8, 1015–1029
    OpenUrlCrossRefPubMed
    1. Campbell G.,
    2. Weaver T.,
    3. Tomlinson A.
    (1993) Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74, 113–1123
    OpenUrl
    1. Cavener D. R.,
    2. Ray S. C.
    (1991) Eukaryotic start and stop translation sites. Nucleic Acids Res 19, 3185–3192
    OpenUrlAbstract/FREE Full Text
    1. Cohen S. M.,
    2. Bronner G.,
    3. Kuttner F.,
    4. Jurgens G.,
    5. Jackle H.
    (1989) Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 338, 432–434
    OpenUrlCrossRefPubMedWeb of Science
    1. Couso J. P.,
    2. Bate M.,
    3. Martinez-Arias A.
    (1993) A wingless -dependent polar coordinate system in Drosophila imaginal discs. Science 259, 484–489
    OpenUrlAbstract/FREE Full Text
    1. Deng Y.,
    2. Rizki T. M.
    (1988) Genetic and developmental analysis of the A1 phenoloxidase of Drosophila. Genome 30, 192–.
    OpenUrl
    1. Diaz-Benjumea F. J.,
    2. Cohen B.,
    3. Cohen S. M.
    (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372, 175–179
    OpenUrlCrossRefPubMed
    1. Eipper B. A.,
    2. Stoffers D. A.,
    3. Mains R. E.
    (1992) The biosynthesis of neuropeptides: peptide-amidation. Annu. Rev. Neurosci 15, 57–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Godt D.,
    2. Couderc J. L.,
    3. Cramton S. E.,
    4. Laski F. A.
    (1993) Pattern formation in the limbs of Drosophila: bric a brac is expressed in both a gradient and a wave-like pattern and is required for specification and proper segmentation of the tarsus. Development 119, 799–812
    OpenUrlAbstract/FREE Full Text
    1. Hartmann E.,
    2. Rapoport T. A.,
    3. Lodish H. F.
    (1989) Predicting the orientation of eukaryotic membrane-spanning proteins. Proc. Natl. Acad. Sci. USA 86, 5786–5790
    OpenUrlAbstract/FREE Full Text
    1. Hortsch M.,
    2. Goodman C. S.
    (1991) Cell and substrate adhesion molecules in Drosophila. Ann. Rev. Cell Biol 7, 505–557
    OpenUrlCrossRefWeb of Science
    1. Kunes S.,
    2. Wilson C.,
    3. Steller H.
    (1993) Independent guidance of retinal axons in the visual system of Drosophila. J. Neurosci 13, 752–767
    OpenUrlAbstract
    1. Kyte J.,
    2. Doolittle R. F.
    (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol 157, 133–148
    OpenUrlCrossRefPubMed
    1. Lee J. J.,
    2. von Kessler D. P.,
    3. Parks S.,
    4. Beachy P. A.
    (1992) Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71, 33–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Mahoney P. A.,
    2. Weber U.,
    3. Onofrechuk P.,
    4. Biessmann H.,
    5. Bryant P.J.,
    6. Goodman C. S.
    (1991) The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily. Cell 67, 853–868
    OpenUrlCrossRefPubMedWeb of Science
    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. Massague J.,
    2. Pandiella A.
    (1993) Membrane-anchored growth factors. Annu. Rev. Biochem 62, 515–541
    OpenUrlCrossRefPubMedWeb of Science
    1. Ready D. F.,
    2. Hansen T. J. E.,
    3. Benzer S.
    (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol 53, 217–240
    OpenUrlCrossRefPubMedWeb of Science
    1. Robertson H. M.,
    2. Preston C. R.,
    3. Phillis R. W.,
    4. Johnson-Schlitz D. M.,
    5. Benz W. K.,
    6. Engels W. R.
    (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470
    OpenUrlAbstract/FREE Full Text
    1. Rogers S.,
    2. Wells R.,
    3. Rechsteiner M.
    (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234, 364–368
    OpenUrlAbstract/FREE Full Text
    1. Schneitz K.,
    2. Spielmann P.,
    3. Noll M.
    (1993) Molecular genetics of aristaless, a prd-type homeo box gene involved in the morphogenesis of proximal and distal pattern elements in a subset of appendages in Drosophila. Genes Dev 7, 114–129
    OpenUrlAbstract/FREE Full Text
    1. Smith J. C.
    (1994) Hedgehog, the floor plate, and the zone of polarizing activity. Cell 76, 193–196
    OpenUrlCrossRefPubMedWeb of Science
    1. Tabata T.,
    2. Kornberg T. B.
    (1994) Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76, 89–102
    OpenUrlCrossRefPubMedWeb of Science
    1. Tokunaga C.,
    2. Gerhart J. C.
    (1976) The effect of growth and joint formation on bristle pattern in D. melanogaster. J. Exp. Zool 198, 79–96
    OpenUrlCrossRefPubMed
    1. Van Vactor D. L., Jr.,
    2. Cagan R. L.,
    3. Kramer H.,
    4. Zipursky S. L.
    (1991) Induction in the developing compound eye of Drosophila: multiple mechanisms restrict R7 induction to a single retinal precursor cell. Cell 67, 1145–1155
    OpenUrlCrossRefPubMedWeb of Science
    1. von Heijne G.
    (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14, 4683–4690
    OpenUrlAbstract/FREE Full Text
    1. Waddington C. H.
    (1943) The development of some ‘leg genes’ in Drosophila. J. Genet 45, 29–43
    OpenUrl
    1. Walter P.,
    2. Blobel G.
    (1983) Preparation of microsomal membranes for cotranslational protein translocation. Meth. Enzymol 96, 682–691
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilson C.,
    2. Pearson R. K.,
    3. Bellen H. J.,
    4. O'Kane C. J.,
    5. Grossniklaus U.,
    6. Gehring W. J.
    (1989) P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev 3, 1301–1313
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila
J.L. Villano, F.N. Katz
Development 1995 121: 2767-2777;
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