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JOURNAL ARTICLES
Genetic control of epithelial tube size in the Drosophila tracheal system
G.J. Beitel, M.A. Krasnow
Development 2000 127: 3271-3282;

Summary

The proper size of epithelial tubes is critical for the function of the lung, kidney, vascular system and other organs, but the genetic and cellular mechanisms that control epithelial tube size are unknown. We investigated tube size control in the embryonic and larval tracheal (respiratory) system of Drosophila. A morphometric analysis showed that primary tracheal branches have characteristic sizes that undergo programmed changes during development. Branches grow at different rates and their diameters and lengths are regulated independently: tube length increases gradually throughout development, whereas tube diameter increases abruptly at discrete times in development. Cellular analysis and manipulation of tracheal cell number using cell-cycle mutations demonstrated that tube size is not dictated by the specific number or shape of the tracheal cells that constitute it. Rather, tube size appears to be controlled by coordinately regulating the apical (lumenal) surface of tracheal cells. Genetic analysis showed that tube sizes are specified early by branch identity genes, and the subsequent enlargement of branches to their mature sizes and maintenance of the expanded tubes involves a new set of genes described here, which we call tube expansion genes. This work establishes a genetic system for investigating tube size regulation, and provides an outline of the genetic program and cellular events underlying tracheal tube size control.

REFERENCES

    1. Bohni R.,
    2. Riesgo-Escovar J.,
    3. Oldham S.,
    4. Brogiolo W.,
    5. Stocker H.,
    6. Andruss B. F.,
    7. Beckingham K.,
    8. Hafen E.
    (1999) Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97, 865–875
    OpenUrlCrossRefPubMedWeb of Science
    1. Buechner M.,
    2. Hall D. H.,
    3. Bhatt H.,
    4. Hedgecock E. M.
    (1999) Cystic canal mutants in Caenorhabditis elegans are defective in the apical membrane domain of the renal (excretory) cell. Dev. Biol 214, 227–241
    OpenUrlCrossRefPubMedWeb of Science
    1. Chen C. K.,
    2. Kuhnlein R. P.,
    3. Eulenberg K. G.,
    4. Vincent S.,
    5. Affolter M.,
    6. Schuh R.
    (1998) The transcription factors KNIRPS and KNIRPS RELATED control cell migration and branch morphogenesis during Drosophila tracheal development. Development 125, 4959–4968
    OpenUrlAbstract
    1. Cooley L.
    (1998) Drosophila ring canal growth requires Src and Tec kinases. Cell 93, 913–915
    OpenUrlCrossRefPubMedWeb of Science
    1. de Nooij J. C.,
    2. Letendre M. A.,
    3. Hariharan I. K.
    (1996) A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell 87, 1237–1247
    OpenUrlCrossRefPubMedWeb of Science
    1. Fankhauser G.
    (1945) Maintenance of normal structure in heteroploid salamander larvae, through compensation of changes in cell size by adjustment of cell number and cell shape. J. Exp. Zool 100, 445–455
    OpenUrlCrossRefPubMed
    1. Fehon R. G.,
    2. Dawson I. A.,
    3. Artavanis-Tsakonas S.
    (1994). A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120, 545–557
    OpenUrlAbstract
    1. Guarnieri D. J.,
    2. Dodson G. S.,
    3. Simon M. A.
    (1998) SRC64 regulates the localization of a Tec-family kinase required for Drosophila ring canal growth. Mol Cell 1, 831–840
    OpenUrl
    1. Guillemin K.,
    2. Groppe J.,
    3. Ducker K.,
    4. Treisman R.,
    5. Hafen E.,
    6. Affolter M.,
    7. Krasnow M. A.
    (1996) The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system. Development 122, 1353–1362
    OpenUrlAbstract
    1. Hacohen N.,
    2. Kramer S.,
    3. Sutherland D.,
    4. Hiromi Y.,
    5. Krasnow M.A.
    (1998) sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92, 253–263
    OpenUrlCrossRefPubMedWeb of Science
    1. Ikeya T.,
    2. Hayashi S.
    (1999) Interplay of notch and FGF signaling restricts cell fate and MAPK activation in the drosophila trachea. Development 126, 4455–4463
    OpenUrlAbstract
    1. Jarecki J.,
    2. Johnson E.,
    3. Krasnow M. A.
    (1999) Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF. Cell 99, 211–220
    OpenUrlCrossRefPubMedWeb of Science
    1. Kuhnlein R. P.,
    2. Schuh R.
    (1996) Dual function of the region-specific homeotic gene spalt during Drosophila tracheal system development. Development 122, 2215–2223
    OpenUrlAbstract
    1. Lane M. E.,
    2. Sauer K.,
    3. Wallace K.,
    4. Jan Y. N.,
    5. Lehner C. F.,
    6. Vaessin H.
    (1996) Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell 87, 1225–1235
    OpenUrlCrossRefPubMedWeb of Science
    1. Metzger R. J.,
    2. Krasnow M. A.
    (1999) Genetic control of branching morphogenesis. Science 284, 1635–1639
    OpenUrlAbstract/FREE Full Text
    1. Orsulic S.,
    2. Peifer M.
    (1996) An in vivo structure-function study of armadillo, the beta-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and for wingless signaling. J. Cell Biol 134, 1283–1300
    OpenUrlAbstract/FREE Full Text
    1. Perrimon N.,
    2. Engstrom L.,
    3. Mahowald A. P.
    (1989) Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome. Genetics 121, 333–352
    OpenUrlAbstract/FREE Full Text
    1. Perrimon N.,
    2. Noll E.,
    3. McCall K.,
    4. Brand A.
    (1991) Generating lineage-specific markers to study Drosophila development. Dev. Genet 12, 238–252
    OpenUrlCrossRefPubMedWeb of Science
    1. Reichman-Fried M.,
    2. Dickson B.,
    3. Hafen E.,
    4. Shilo B. Z.
    (1994) Elucidation of the role of breathless, a Drosophila FGF receptor homolog, in tracheal cell migration. Genes Dev 8, 428–439
    OpenUrlAbstract/FREE Full Text
    1. Roulier E. M.,
    2. Panzer S.,
    3. Beckendorf S. K.
    (1998) The Tec29 tyrosine kinase is required during Drosophila embryogenesis and interacts with Src64 in ring canal development. Mol. Cell 1, 819–829
    OpenUrl
    1. Samakovlis C.,
    2. Hacohen N.,
    3. Manning G.,
    4. Sutherland D. C.,
    5. Guillemin K.,
    6. Krasnow M. A.
    (1996) Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122, 1395–1407
    OpenUrlAbstract
    1. Samakovlis C.,
    2. Manning G.,
    3. Steneberg P.,
    4. Hacohen N.,
    5. Cantera R.,
    6. Krasnow M. A.
    (1996) Genetic control of epithelial tube fusion during Drosophila tracheal development. Development 122, 3531–3536
    OpenUrlAbstract
    1. Scholz H.,
    2. Deatrick J.,
    3. Klaes A.,
    4. Klambt C.
    (1993) Genetic dissection of pointed, a Drosophila gene encoding two ETS-related proteins. Genetics 135, 455–468
    OpenUrlAbstract/FREE Full Text
    1. Shiga Y.,
    2. Tanaka-Matakatsu M.,
    3. Hayashi S.
    (1996) A nuclear GFP/ beta-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Diff 38, 99–106
    1. Shilo B. Z.,
    2. Gabay L.,
    3. Glazer L.,
    4. Reichman-Fried M.,
    5. Wappner P.,
    6. Wilk R.,
    7. Zelzer E.
    (1997) Branching morphogenesis in the Drosophila tracheal system. Cold Spring Harb. Symp. Quant. Biol 62, 241–247
    OpenUrlAbstract/FREE Full Text
    1. Sprenger F.,
    2. Yakubovich N.,
    3. O'Farrell P. H.
    (1997) S-phase function of Drosophila cyclin A and its downregulation in G1 phase. Curr. Biol 7, 488–499
    OpenUrlCrossRefPubMedWeb of Science
    1. Steneberg P.,
    2. Englund C.,
    3. Kronhamn J.,
    4. Weaver T. A.,
    5. Samakovlis C.
    (1998) Translational readthrough in the hdc mRNA generates a novel branching inhibitor in the Drosophila trachea. Genes Dev 12, 956–967
    OpenUrlAbstract/FREE Full Text
    1. Sutherland D.,
    2. Samakovlis C.,
    3. Krasnow M. A.
    (1996) branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87, 1091–1101
    OpenUrlCrossRefPubMedWeb of Science
    1. Torok T.,
    2. Tick G.,
    3. Alvarado M.,
    4. Kiss I.
    (1993) P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes. Genetics 135, 71–80
    OpenUrlAbstract/FREE Full Text
    1. Vincent S.,
    2. Ruberte E.,
    3. Grieder N. C.,
    4. Chen C. K.,
    5. Haerry T.,
    6. Schuh R.,
    7. Affolter M.
    (1997) DPP controls tracheal cell migration along the dorsoventral body axis of the Drosophila embryo. Development 124, 2741–2750
    OpenUrlAbstract
    1. Wappner P.,
    2. Gabay L.,
    3. Shilo B. Z.
    (1997) Interactions between the EGF receptor and DPP pathways establish distinct cell fates in the tracheal placodes. Development 124, 4707–4716
    OpenUrlAbstract
    1. Whiteley M.,
    2. Noguchi P. D.,
    3. Sensabaugh S. M.,
    4. Odenwald W. F.,
    5. Kassis J. A.
    (1992) The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes. Mech. Dev 36, 117–127
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilk R.,
    2. Weizman I.,
    3. Shilo B. Z.
    (1996) trachealess encodes a bHLH-PAS protein that is an inducer of tracheal cell fates in Drosophila. Genes Dev 10, 93–102
    OpenUrlAbstract/FREE Full Text
    1. Wodarz A.,
    2. Hinz U.,
    3. Engelbert M.,
    4. Knust E.
    (1995) Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82, 67–76
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Genetic control of epithelial tube size in the Drosophila tracheal system
G.J. Beitel, M.A. Krasnow
Development 2000 127: 3271-3282;
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