Tubulpgenesis in Drosophila: A requirement for the trachealess gene product

Genes and Development

Volumn 10, Issue 1, 1996, Pages 103-117

  Isaac, Daniel D ^a   Andrew, Deborah J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Drosophila; Trachealess gene; Transcription factors; Tubulogenesis

Indexed keywords

COMPLEMENTARY DNA; GENE PRODUCT; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ARTICLE; DEVELOPMENTAL GENETICS; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; NONHUMAN; PRIORITY JOURNAL; SALIVARY GLAND; TRACHEA; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CENTRAL NERVOUS SYSTEM; CONNEXINS; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EPITHELIAL CELLS; EPITHELIUM; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC COMPLEMENTATION TEST; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INSECT HORMONES; MEMBRANE PROTEINS; MICROTUBULES; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; RNA, MESSENGER; SALIVARY DUCTS; SEQUENCE HOMOLOGY, AMINO ACID; TRACHEA; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 0030049584     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.10.1.103     Document Type: Article

References (73)

1. Anderson, M.G., G.L. Perkins, P. Chittick, R.J. Shrigley, and W.A. Johnson. 1995. drifter, a Drosophila POU-domain transcription factor, is required for correct differentiation and migration of tracheal cells and midline glia. Genes & Dev. 9: 123-137.
2. Andrew, D.J. and M.P. Scott 1992. Downstream of the homeotic genes. New Biol. 4: 5-15.
3. Andrew, D.J., M.A. Horner, M.G. Petitt, S.M. Smolik, and M.P. Scott. 1994. Setting limits oil homeotic gene function: Restraint of Sex combs reduced activity by teashirt and other homeotic genes. EMBO J. 13: 1132-1144.
4. Bard, J. 1992. Morphogenesis. The cellular and molecular processes of developmental anatomy. Cambridge University Press, Cambridge, UK.
5. Bargiello, T.A., L. Saez, M.K. Bayhes, G. Gasic, M.W. Young, and D.C. Spray. 1987. The Drosophila clock gene per affects intercellular junctional communication. Nature 328: 686-691.
6. Barros, E.J.G., O.F.P. Santos, K. Matsumoto, T. Nakamura, and S.K. Nigam. 1995. Differential tubulogenic and branching morphogenetic activities of growth factors: Implications for epithelial tissue development. Proc. Natl. Acad. Sci. 92: 4412-4416.
7. Birchmeier, C. and W. Birchmeier. 1993. Molecular aspects of mesenchymal-epithelial interactions. Annu. Rev. Cell Biol. 9: 511-540.
8. Biönner, G., Q. Chu-LaGraff, C.Q. Doe, B. Cohen, D. Weigel, H. Taubert, and H. Jäckle. 1994. Spi/egr-like zinc-finger protein required for endoderm specification and germ-layer formation in Drosophila Nature 369: 664-668.
9. Bussoltno, F., M.F. Di Renzo, M. Ziche, E. Bocchietto, M. Olivero, L. Naldini, G. Gaudino, L. Tamagnone, A. Coffer, and P.M. Comogho. 1992. Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J. Cell Biol. 119: 629-641.
10. Campos-Ortega, J.A. and V. Hartenstein. 1985. The embryonic development of Drosophila melanogaster. Springer-Verlag, Berlin/Heidelberg, Germany.
11. Cantley, L.G., E.J.G. Barros, M. Gandhi, M. Rauchman, and S.K. Nigam 1994. Regulation of mitogenesis, motogenesis, and tubulogenesis by hepatocyte growth factor in renal collecting duct cells. Am. J. Physiol. 267: F271-F280.
12. Courcy, A.J. and R. Tjian. 1988 Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation domain. Cell 55: 887-898.
13. Davis, R.L., P.-F Cheng, A.B Lassar, and H. Weintraub. 1990. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60: 733-746.
14. Ettensohn, C.A. 1985 Mechanisms of epithelial invagination. Q Rev. Biol 60: 289-307.
15. Fasano, L., L. Röder, N. Coré, E. Alexandre, C. Vola, B. Jacq, and S. Kerridge. 1991. The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc fingers. Cell 64: 63-79.
16. Galimi, F., G.P. Bagnara, L. Bonxi, E. Coltone, A. Follenzi, A Simeone, and P.M. Comoglio. 1994. Hepatocyte growth factor induces proliferation and differation of multipotent and erythroid hemopoietic progenitors. J. Cell Biol 127: 1743-1754.
17. Giniger, E., L.Y. Jan, and Y.N. Jan. 1993. Specifying the path of the intersegmental nerve of the Drosophila embryo: A role for Delta and Notch. Development 117: 431-440.
18. Glazer, L. and B.-Z. Shilo. 1991. The Diosophila FGF-R homolog is expressed in the embryonic tracheal system and appears to be required for directed tracheal cell extension. Genes & Dev. 5: 697-705.
19. Grant, D.S., H. Kleinman, I.D. Goldberg, M.M Bhargava, B.J. Nickoloff, J.L. Kinsella, P. Polverini, and E.M. Rosen. 1993. Scatter factor induces blood vessel formation in vivo. Proc. Natl. Acad. Sci. 90: 1937-1941.
20. Gumbiner, B.M. 1992. Epithelial morphogenesis. Cell 69: 385-387.
21. Hamilton, B.A. and K. Zinn. 1994. From clone to mutant gene. In Methods in cell biology (ed. L.S.B. Goldstein and E.A Fyrberg), pp. 89-93. Academic Press, New York, NY.
22. Higgins, D.G. 1993. ClustalV: Multiple alignment of DNA and protein sequence. In Methods in Molecular Biology, pp. 307-318. Humana Press, Totowa, NJ.
23. Hirai, Y., K. Takebe, M. Takashina, S. Kobayashi, and M. Takeichi 1992. Epimorphin: A mesenchymal protein essential for epithelial morphogenesis. Cell 69: 471-481.
24. Hoffman, E.G., H. Reyes, F.-F. Chu, F. Sander, L.H. Conley, B.A. Brooks, and O. Hankinson. 1991. Cloning of a factor for activity of the Ah (dioxin) receptor. Science 252: 54-958.
25. Jackson, F.R., T.A. Bargiello, S.-H. Yun, and M.W. Young. 1986. Product of the per locus of Diosophila shares homology with proteoglycans. Nature 320: 185-188.
26. Jürgens, G. and D. Weigel. 1989. Terminal versus segmental development in the Diosophila embryo: The role of the homeotic gene fork head. Wilhelm Roux's Arch. Dev. Biol. 197: 345-354.
27. Jürgens, G., E. Wieschaus, C. Nüsslein-Volhard, and H. Kluding. 1984. Mutations affecting the pattern of the larval cuticle in Diosophila melanogaster II. Zygotic loci on the third chromosome. Wilhelm Roux's Arch. Dev. Biol. 193: 283-295.
28. Karp, S.L., A. Ortiz-Ardvan, S. Li, and E.G. Nielson. 1984. Epithelial differentiation of metanephric mesenchymal cells after stimulation with hepatocyte growth factor or embryonic spinal cord. Proc. Natl Acad. Sci. 91: 5286-5290.
29. Karpen, G.H. and A.C. Spradling. 1992. Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dpi 187 by single P element insertional mutagenesis Genetics 132: 737-753.
30. Kinsella, J.L., D.S. Grant, B.S. Weeks, and H.K. Kleinman. 1992. Protein kinase C regulates endothelial cell tube formation on basement membrane matrix, matrigel. Exp. Cell Res. 199: 56-62.
31. Klambt, C., L. Glazer, and B.-Z. Shilo. 1992. breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes & Dev. 6: 1668-1678.
32. Konopka, R.J. and S. Benzer. 1971. Clock mutants of Drosophila melanogaster. Proc Natl. Acad. Sci. 68: 2112-2116.
33. Levine, M. and T. Hoey. 1988. Homeobox proteins as sequence-specific transcription factors. Cell 55: 537-540.
34. Lindsley, D.L. and G.G. Zimm. 1992. The genome of Drosophila melanogaster. Academic Press, San Diego, CA.
35. Maheshwari, R.K., V. Srikantan, D. Bhartiya, H.K. Kleinman, and D.S. Grant. 1991. Differential effects of interferon gamma and alpha on in vitro model of angiogenesis. J. Cell. Physiol. 146: 164-169.
36. Manning, G and M. Krasnow, M. 1993. Tracheal Development. In The development of Drosophila melanogaster (ed. M. Bate and A. Martinez Arias), pp. 609-685. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Montesano, R., J.-D. Vassalli, A. Baird, R. Guillemin, and L. Orci. 1986. Basic fibroblast growth factor induces angiogenesis in vitro. Proc. Natl. Acad. Sci. 83: 7297-7301.
38. Montesano, R., K. Matsumoto, K., T. Nakamura, and L. Orci. 1991a Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67: 901-908.
39. Montesano, R., G. Schaller, and L. Orci. 1991b. Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 66: 697-711.
40. Murre, C., P.S. McCaw, H.Vaessin, M. Caudy, L.Y. Jan, Y.N. Jan, C.V. Cabrera, J.N. Buskin, S.D. Hauschka, A.B. Lassar, H. Weintraub, and D. Baltimore. 1989. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58: 537-544.
41. Nambu, J.R., R.G. Franks, S. Hu, and S.T. Crews. 1990. The single-minded gene of Drosophila is required for the expression of genes important for the development of CNS midline cells. Cell 63: 63-75.
42. Nambu, J.R., J.O. Lewis, K.A.J. Wharton, and S.T. Crews. 1991. The Drosophila single-minded gene encodes a helix-loop-helix protein that acts as a master regulator of CNS midline development. Cell 67: 1157-1167.
43. Ono, M., K. Okamura, Y. Nakayama, M. Toniita, Y. Sata, Y. Komatsu, and M. Kuwano. 1992. Induction of human microvascular endothehal tubular morphogenesis by human keratinocytes: Involvement of transforming growth factor-α. Biochem. Biophys. Res. Comm. 189: 601-609.
44. Panzer, S , D. Weigel, and S.K. Beckendorf. 1992. Organogenesis m Drosophila melanogaster: Embryonic salivary gland determination is controlled by homeotic and dorsoventral patterning genes. Development 114: 49-57.
45. Patel, N.H., E. Martin-Blanco, K.G. Coleman, S.J. Poole, M.C. Ellis, T.B. Kornberg, and C.S. Goodman. 1989. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58: 955-968.
46. Reddy, P., A.C. Jacquier, N. Abovich, G. Peterson, and M. Rosbash. 1986. The period clock locus of D. melanogaster codes for a proteoglycan. Cell 46: 53-61.
47. Reichman-Fried, M., B. Dickson, E. Hafen, and B.-Z. Shilo. 1994. Elucidation of the role of breathless, a Drosophila FGF receptor homolog, in tracheal migration. Genes & Dev. 8: 428-439
48. Reuter, R., G.E.F. Panganiban, F.M. Hoffmann, and M.P. Scott. 1990. Homeotic genes regulate the spatial expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development 110: 1031-1040.
49. Rogers, S.A., G. Ryan, and M.R. Hammerman. 1992. Metanephric transforming growth factor-α is required for renal Organogenesis in vitro. Am. J. Physiol. 264: 963-967.
50. Rogers, S.A., G. Ryan, A.F. Purchio, and M.R. Hammerman 1993. Metanephric transforming growth factor-β1 regulates nephrogenesis in vitro. Am. J. Physiol 264: 996-1002.
51. Rosen, E.M., D. Grant, H. Kleinman, S. Jaken, M.A. Donovan, E. Setter, P.M. Luckett, W. Carley, M. Bhargava, and I.D. Goldberg. 1991. Scatter factor stimulates migration of vascular endothelium and capillary-like tube formation. In Cell motility factors (ed. I.D. Goldberg), pp. 76-88. Birkhäuser Verlag, Basel, Switzerland.
52. Sanger, F., S. Nicklen, and A R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors Proc. Natl. Acad. Sci 74: 5463-5467.
53. Santos, O.F.P and S.K. Nigam. 1993. HGF-induced tubulogenesis and branching of epithelial cells is modulated by extracellular matrix and TGF-β. Dev. Biol. 160: 293-302.
54. Schmidt, C. P. Bladt, S. Goedecke, V. Brinkmann, W. Zschiesche, M. Sharpe, E. Gherardi, and C. Birchmeier. 1995. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373: 699-702.
55. Scott, M.P., J.W. Tamkun, and G.W. Hartzell III. 1989. The structure and function of the homcodomain. BBA Rev Cancer 989: 25-48.
56. Soriano, J.V., M.S. Pepper, T. Nakamura, L. Orci, L. Montesano, and R. Montesano. 1995. Hepatocyte growth factor stimulates extensive development of branching duct-like structures by cloned mammary gland epithelial cells. J. Cell Sci 108: 413-430.
57. Stamatoglou, S.C. and R.C. Hughes. 1994 Cell adhesion molecules in liver function and pattern formation. FASEB J. 8: 420-427.
58. Sweeton, D., S. Parks, M. Costa, and E. Wieschaus. 1991. Gastrulation m Drosophila: The formation of the ventral furrow and posterior midgut invaginations. Development 112: 775-789.
59. Tamkun, J.W , R.A. Kahn, M. Kissinger, B.J. Bruzuela, C. Rulka, M.P. Scott, and J.A. Kennison. 1991. The arflike gene encodes an essential GTP-binding protein in Drosophila Proc. Natl. Acad. Sci. 88: 3120-3124.
60. Taub, M., Y. Wang, T.M. Szczesny, and H K Kleinman. 1990. Epidermal growth factor or transforming growth factor α is required for kidney tubulogenesis in matrigel cultures in serum-free medium. Proc. Natl. Acad. Sci. 87: 4002-4006.
61. Tautz, D. and C. Pfeifle. 1989. A non-radioactive in situ hybridization method for localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback Chromosoma 98: 81-85.
62. Tepass, U., C, Theres, and E. Knust. 1990a. crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61: 787-799.
63. _. 1990b. Phenotypic and developmental analysis of mutations at the crumbs locus, a gene required for the development of epithelia in Drosophila melanogaster Wilhelm Roux's Arch. Dev. Biol. 199: 189-206.
64. Uehara, Y., O. Minowa, C. Mon, K Shiota, J. Kuno, T. Noda, and N. Kitamura. 1995. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373: 72-705
65. 2 tension Proc. Natl. Acad. Sci. 92: 5510-5514.
66. Weigel, D. and H. Jäckle. 1990. The fork head domain: A novel DNA binding motif of eukaryotic transcription factors? Cell 63: 455-456.
67. Weigel, D., G. Jürgens, F. Küttner, E. Seifert, and H. Jackle. 1989. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57: 645-658.
68. White, F C., S.M. Carroll, A. Magnet, and C.M. Bloor. 1992. Coronary collateral development in swine after coronary artery occlusion. Circ. Res. 71: 1490-1500
69. Wodarz, A., U. Hinz, M. Engelbert, and E. Knust. 1995. Expression of Crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosopbila. Cell 82: 67-76.
70. Younossi-Hartenstem, A. and V Hartenstein. 1993. The role of the tracheae and musculature during pathfinding of Drosophila embryonic sensory axons. Dev. Biol. 158: 430-447.
71. Zarnegar, R. and G.K. Michalopoulos 1995 The many faces of hepatocyte growth factor: From hepatopoiesis to hematopoiesis. J. Cell Biol. 129: 1177-1180.
72. Zeng, W., D.J. Andrew, L.D. Mathies, M.A. Homer, and M.P. Scott. 1993. Ectopic expression and function of the Antp and Scr homeotic genes: The N terminus of the homeodomain is critical to functional specificity. Development 18: 339-352.
73. Zinn, K., L. McAllister, and C.S. Goodman. 1988. Sequence analysis and neuronal expression of Fasciclin I in grasshopper and Drosophila. Cell 53: 577-587