Oncogenes pp 1-29 | Cite as

Roles of Drosophila Proto-oncogene and Growth Factor Homologs During Development of the Fly

  • F. Michael Hoffmann
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 147)


The regulation of cell proliferation and differentiation is an essential aspect of organismal development. An important goal of investigations over the next few years will be to define the regulatory pathways of cellular proliferation and differentiation by discovering how the molecules we know about, and others that remain to be discovered, interact with one another to instruct a cell to divide or to differentiate. Growth factors, growth receptors, and the protooncogenes represent some of the components on these regulatory circuits; the challenge is to complete the “wiring-diagrams” by finding the molecular connections between the components. Molecular genetic and biochemical approaches are being applied to this problem in vertebrate cell culture and animal systems. The opportunity to use classical genetic strategies to address this problem led several groups to examine simpler organisms for the presence of proteins homologous to growth factors, growth factor receptors, or protooncogenes. It is now clear that many of these proteins have been well conserved during evolution and are found in three organisms eminently suited to genetic manipulation—yeast, Caenorhabditis elegans, and Drosophila melanogaster.


Follicle Cell Nurse Cell Drosophila Gene Germ Band Larval Cuticle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101: 1–22PubMedGoogle Scholar
  2. Alton AK, Fechtel K, Terry AL, Meikle SB, Muskavitch MAT (1988) Cytogenetic definition and morphogenetic analysis of Delta, a gene affecting neurogenesis in Drosophila melanogaster. Genetics 118: 235–245PubMedGoogle Scholar
  3. Anderson KV (1987) Dorsal-ventral embryonic pattem genes of Drosophila. Trends Genet 3: 91–97Google Scholar
  4. Anderson KV, Nüsslein-Volhard C (1984) Genetic analysis of the dorsal/ventral embryonic pattern in Drosophila. In: Malacinski GM, Bryant SV (eds) Primers in developmental biology. Macmillan, New York pp 269–289Google Scholar
  5. Anderson KV, Nüsslein-Volhard C (1984) Information for the dorsal-ventral pattem of the Drosophila embryo is stored as maternal mRNA. Nature 311: 223–227PubMedGoogle Scholar
  6. Artavanis-Tsakonas S, Muskavitch MAT, Yedvobnick B (1983) Molecular cloning of Notch, a locus affecting neurogenesis in Drosophila melanogaster. Proc Natl Acad Sci USA 80: 1977–1981PubMedGoogle Scholar
  7. Austin J, Kimble J (1987) glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51: 589–599PubMedGoogle Scholar
  8. Baker NE (1987) Molecular cloning of sequences from wingless, a segment polyrity gene in Drosophila: the spatial distribution of a transcript in embryos. EMBO J 6: 1765–1773PubMedGoogle Scholar
  9. Baker NE (1988 a) Embryonic and imaginai requirements for wingless, a segment-polarity gene in Drosophila. Dev Biol 125: 96–108PubMedGoogle Scholar
  10. Baker NE (1988 b) Transcription of the segment-polarity gene wingless in the imaginai discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. Development 102: 489–497PubMedGoogle Scholar
  11. Baker NE (1988c) Localization of transcripts from the wingless gene in whole Drosophila embryos. Development 103: 289–298PubMedGoogle Scholar
  12. Baneijee U, Renfranz PJ, Pollack JA, Benzer S (1987 a) Molecular characterization and expression of sevenless, a gene involved in neuronal pattern formation in the Drosophila eye. Cell 49: 281–291Google Scholar
  13. Banerjee U, Renfranz PJ, Hinton DR, Rabin BA, Benzer S (1987b) The sevenless + protein is expressed apically in cell membranes of developing Drosophila retina; it is not restricted to cell R7. Cell 51: 151–158PubMedGoogle Scholar
  14. Basler K, Hafen E (1988 a) Control of photoreceptor cell fate by the sevenless protein requires a functional tyrosine kinase domain. Cell 54: 299–311PubMedGoogle Scholar
  15. Basler K, Hafen E (1988b) Sevenless and Drosophila eye development: a tyrosine kinase controls cell fate. Trends Genet 4: 74–79PubMedGoogle Scholar
  16. Bennett RL, Hoffmann FM (in preparation) Expression of the Drosophila Abelson tyrosine kinase is associated with differentiation of neuronal cellsGoogle Scholar
  17. Bishop JG III, Corees VG (1988) Expression of an activated ras gene causes developmental abnormalities in transgenic Drosophila melanogaster. Genes Dev 2: 567–577PubMedGoogle Scholar
  18. Blackman RK, Gramaila R, Koehler MMD, Gelbart WM (1987) Mobilization of hobo elements residing within the decapentaplegic gene complex: suggestion of a new hybrid dysgenesis system in Drosophila melanogaster. Cell 49: 497–505PubMedGoogle Scholar
  19. Brock HW (1987) Sequence and genomic structure of ras homologues Dmras85D and Dmras64B and Drosophila melanogaster. Gene 51: 129–137PubMedGoogle Scholar
  20. Bryant PJ (1987) Experimental and genetic analysis of growth and cell proliferation in Drosophila imaginai disks. In: Loomis, WF (ed) Genetic regulation of development: 45th Annual Symposium of the Society for Developmental Biology. AR Liss, New York pp 339–372.Google Scholar
  21. Bryant PJ (1988) Localized cell death caused by mutations in a Drosophila gene coding for a transforming growth factor-ß homolog. Dev Biol 128: 386–395PubMedGoogle Scholar
  22. Bryant PJ, Simpson P (1984) Intrinsic and extrinsic control of growth in developing organs. Q Rev Biol 59:387–415PubMedGoogle Scholar
  23. Campos-Ortega JA, Hartenstein V (1985) The Embryonic Development of Drosophila melanogaster. Springer, Berlin Heidelberg New York, pp 1–84, 144–158Google Scholar
  24. Delotto R, Spierer P (1986) A gene required for the specification of dorsal-ventral pattern in Drosophila appears to encode a serine protease. Nature 323: 688–692PubMedGoogle Scholar
  25. Dietrich U, Campos-Ortega JA (1984) The expression of neurogenic loci in imaginai epidermal cells of Drosophila melanogaster. J Neurogenet 1: 315–332PubMedGoogle Scholar
  26. Downward J, Yarden Y, Mayes E, Scrace G, Totty N, Stockwell P, Ullrich A, Schlessinger J, Waterfield MD (1984) Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences. Nature 307: 521–527PubMedGoogle Scholar
  27. Durica DS, Restrepo MA, Thomas TL, Beckingham K (1987) Isolation and characterization of abl gene sequences in Calliphora erythrocephala. Gene 59: 63–76PubMedGoogle Scholar
  28. Fukui M, Yamamoto T, Kawai S, Maruo K, Toyoshima K (1985) Detection of a raf-related and two other transforming DNA sequences in human tumors maintained in nude mice. Proc Natl Acad Sci USA 82: 5954–5958PubMedGoogle Scholar
  29. Gertler FB, Bennett RL, Clark MJ, Hoffmann FM (1989) Drosophila abl tyrosine kinase in embryonic CNS axons: a role in axonogenesis is revealed through dosage-sensitive interactions with a new gene, disabled. Cell (In press)Google Scholar
  30. Gilmore TD, Temin HM (1988) v-rel oncoproteins in the nucleus and in the cytoplasm transform chicken spleen cells. J Virol 62: 703–714PubMedGoogle Scholar
  31. Goddard JM, Weiland JJ, Capecchi MR (1986) Isolation and characterization of Caenorhabditis elegans DNA sequences homologous to the v-abl oncogene. Proc Natl Acad Sci USA 83: 2172–2176PubMedGoogle Scholar
  32. Greenwald I (1985) lin-12, a nematode homeotic gene, is homologous to a set of mammalian proteins that includes epidermal growth factor. Cell 43: 583–590PubMedGoogle Scholar
  33. Gregory RJ, Kammermeyer KL, Vincent III WS, and Wadsworth SG (1987) Primary sequence and developmental expression of a novel Drosophila melanogaster src gene. Noi Cell Biol 7: 2119–2127Google Scholar
  34. Haenlin M, Roos C, Cassab A, Mohier E (1987) Oocyte-specific transcription -of fs(l)K10: Drosophila gene affecting dorsal-ventral developmental polarity. EMBO J 6: 801–807PubMedGoogle Scholar
  35. Hafen E, Basler K, Edstroem J-E, Rubin GM (1987) Sevenless, a cell-specific homeotic gene of Drosophila, encodes a putative transmembrane receptor with a tyrosine kinase domain. Science 236:55–63PubMedGoogle Scholar
  36. Hartenstein V, Campos-Ortega JA (1985) Fate-mapping in wild-type Drosophila melanogaster. I. The spatio-temporal pattern of embryonic cell divisions. Roux’s Arch Dev Biol 194: 181–195Google Scholar
  37. Hartley DA, Xu T, Artavanis-Tsakonas S (1987) The embryonic expression of the Notch locus of Drosophila melanogaster and the implications of point mutations in the extracellular EGF-like domain of the predicted protein. EMBO J 6: 3407–3417PubMedGoogle Scholar
  38. Hartley DA, Preiss A, Artavanis-Tsakonas S (in press) A deduced gene product from the Drosophila neurogenic locus, Enhancer of split, shows homology to mammalian G-protein beta subunit. Cell 55: 785–795Google Scholar
  39. Henkemeyer MJ, Gertler FB, Goodman W, Hoffmann FM (1987) The Drosophila Abelson protooncogene homolog: identification of mutant alleles that have pleiotropic effects late in development. Cell 51: 821–828PubMedGoogle Scholar
  40. Henkemeyer MJ, Bennett RL, Gertler FB, Hoffmann FM (1988) DNA sequence, structure, and tyrosine kinase activity of the Drosophila melanogaster Abelson proto-oncogene homolog. Mol Cell Biol 8: 843–853PubMedGoogle Scholar
  41. Hoffman-Falk H, Einat P, Shilo B-Z, Hoffmann FM (1983) Drosophila melanogaster DNA clones homologous to vertebrate oncogenes: evidence for a common ancestor to the src and abl cellular genes. Cell 32: 589–598PubMedGoogle Scholar
  42. Hoffmann FM, Goodman W (1987) Identification in transgenic animals of Drosophila decapentaplegic sequences required for embryonic dorsal pattern formation. Genes Dev 1: 615–625PubMedGoogle Scholar
  43. Hoffmann FM, Fresco LD, Hoffman-Falk H, Shilo B-Z (1983) Nucleotide sequences of the Drosophila src and abl homologs: conservation and variability in the src family oncogenes. Cell 35: 393–401PubMedGoogle Scholar
  44. Hoffmann FM, Henkemeyer MJ, Bennett RL, Gertler FB (1989) The Abelson tyrosine kinase in Drosophila: application of genetic strategies to understand its normal functions. In: Arlinghaus RB, Deisseroth A (eds) Molecular approaches to the study and treatment of Philadelphia chromosome positive leukemia. Marcel Dekker, New York, pp unknownGoogle Scholar
  45. Holland PWH, Hogan BLM (1988) Expression of homebox genes during mouse development: a review. Genes Dev 2: 773–782PubMedGoogle Scholar
  46. Hoppe PE, Greenspan RJ (1986) Local function of the Notch gene for embryonic ectodermal pathway choice in Drosophila. Cell 46: 773–783PubMedGoogle Scholar
  47. Ingham PW (1988) The molecular genetic of embryonic pattern formation in Drosophila. Nature 335:25–34PubMedGoogle Scholar
  48. Irish V (1987) Cracking the Drosophila egg. Trends Genet 11: 303–304Google Scholar
  49. Irish VF, Gelbart WM (1987) The decapentaplegic gene is required for dorsal/ventral patterning of the Drosophila embryo. Genes Dev 1: 868–879PubMedGoogle Scholar
  50. Jansen HW, Patschinsky T, Bister K (1983) Avian oncovirus MH2: molecular cloning of proviral DNA and structural analysis of viral RNA and protein. J Virol 48: 61–73PubMedGoogle Scholar
  51. Jurgens G, Wieschaus E, Nusslein-Volhard C, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster: zygotic loci on the third chromosome. Roux’s Arch Dev Biol 193: 283–295Google Scholar
  52. Kammermeyer KL, Wadsworth SC (1987) Expression of Drosophila epidermal growth factor receptor homologue in mitotic cell populations. Development 100: 201–210PubMedGoogle Scholar
  53. Katzen AL, Komberg TB, Bishop JM (1985) Isolation of the proto-oncogene c-myb from D. melanogaster. Cell 41: 449–456PubMedGoogle Scholar
  54. Kidd S, Lockett TJ, Young MW (1983) The Notch locus of Drosophila melanogaster. Cell 34: 421–433PubMedGoogle Scholar
  55. Kidd S, Kelley MR, Young MW (1986) Sequence of the Notch locus of Drosophila melanogater: relationship of the encoded protein to mammalian clotting and growth factors. Mol Cell Biol 6: 3094–3108PubMedGoogle Scholar
  56. Knust E, Dietrich V, Tepass V, Bremer KA, Weigel D, Vässin H, Campos-Ortega JA (1987) EGF homologous sequences encoded in the genome of Drosophila melanogaster, and their relation to neurogenic genes. EMBO J 6: 761–766PubMedGoogle Scholar
  57. Kopczynski CC, Alton AK, Fechtel K, Kooh PJ, Muskavitch MAT (1988) Delta, a Drosophila neurogenic gene, is transcriptionally complex and encodes a protein related to blood coagulation factors and epidermal growth factor of vertebrates. Genes Dev Z: 1723–1735Google Scholar
  58. Lehmann R, Jimenez F, Dietrich U, Campos-Ortega JA (1983) On the phenotype and development of mutants of early neurogenesis in Drosophila melanogaster. Roux’s Arch Dev Biol 192: 62–74Google Scholar
  59. Lev Z, Leibovitz N, Segev O, Shilo B-Z (1984) Expression of the src and abl cellular oncogenes during development of Drosophila melanogaster. Mol Cell Biol 4: 982–984PubMedGoogle Scholar
  60. Lev Z, Shilo B-Z, Kimchie Z (1985) Developmental changes in expression of the Drosophila melanogaster epidermal growth factor receptor gene. Dev Biol 110: 499–502PubMedGoogle Scholar
  61. Livneh E, Glazer L, Segel D, Schlessinger J, Shilo B-Z (1985) The Drosophila EGF receptor gene homolog: conservation of both hormone binding and kinase domain. Cell 40: 599–607PubMedGoogle Scholar
  62. Mahowald AP, Kambysellis MP (1980) Oogenesis. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila, vol 2D. Academic, New York, pp 141–225Google Scholar
  63. Mark GE, Seeley TW, Shows TB, Mountz JD (1986) pks, a raf-related sequence in humans. Proc Natl Acad Sci USA 83: 6312–6316PubMedGoogle Scholar
  64. Mark GE, MacIntyre RJ, Digan ME, Ambrosio L, Perrimon N (1987) Drosophila melanogaster homologs of the raf oncogene. Mol Cell Biol 7: 2134–2140PubMedGoogle Scholar
  65. Martinez-Arias A, Baker NE, Ingham PW (1988) Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development 103: 157–170Google Scholar
  66. Mayer BJ, Hamaguchi M, Hanafusa H (1988) A novel viral oncogene with structural similarity to phospholipase C. Nature 332: 272–275PubMedGoogle Scholar
  67. Moelling K, Heimann B, Beimling P, Rapp UR, Sander T (1984) Serine- and threonine-specific protein kinase activities of purified gag-mil and gag-raf proteins. Nature 312: 558–560PubMedGoogle Scholar
  68. Morata G, Lawrence PA (1977) The development of wingless, a homeotic mutation of Drosophila. Dev Biol 56: 227–240PubMedGoogle Scholar
  69. Mozer B, Marlor R, Parkhurst S, Corces V (1985) Characterization and developmental expression of a Drosophila ras oncogene. Mol Cell Biol 5: 885–889PubMedGoogle Scholar
  70. Neuman-Silberberg FS, Schejter E, Hoffmann FM, Shilo B-Z (1984) The Drosophila ras oncogenes: structure and nucleotide sequence. Cell 37: 1027–1033PubMedGoogle Scholar
  71. Nishida Y, Hata M, Ayaki T, Ryo H, Yamagata M, Shimizu K, Nishizuka Y (1988) Proliferation of both somatic and germ cells is affected in the Drosophila mutants of raf proto-oncogene. EMBO J 7: 775–781PubMedGoogle Scholar
  72. Nusse R, van Ooyen A, Cox D, Fung YKT, Varmus HE (1984) Mode of proviral activation of a putative mammary oncogene (int-1) on mouse chromosomes 15. Nature 307: 131–136PubMedGoogle Scholar
  73. Nüsslein-Volhard C (1979) Maternal effect mutations that alter the spatial coordinates of the embryo of Drosophila melanogaster. In: Subtelney S, Koenigsberg IR (eds) Determination of spatial organization. Academic Press, New York, pp 185–211Google Scholar
  74. Nüsslein-Volhard C, Frohnhöfer HG, Lehmann R (1987) Determination of anteroposterior polarity in Drosophila. Science 238: 1675–1681PubMedGoogle Scholar
  75. Nüsslein-Volhard C, Wieschaus E, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Roux’s Arch. Dev Biol 193: 267–282Google Scholar
  76. Padgett RW, St Johnston RD, Gelbart WM (1987) A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family. Nature 325: 81–84PubMedGoogle Scholar
  77. Panganiban GF, Neitzel M, Hoffmann FM (in preparation) Biochemical characterization of the Drosophila decapentaplegic protein, a member of the TGF-ß family.Google Scholar
  78. Papkoff J, Brown AT, Varmus H (1987) The int-1 proto-oncogene products are glycoproteins that appear to enter the secretory pathway. Mol Cell Biol 7: 3978–3984PubMedGoogle Scholar
  79. Parks S, Spradling A (1987) Spatially regulated expression of chorion genes during Drosophila development. Genes Dev 1: 497–509Google Scholar
  80. Perrimon N, Gans M (1983) Clonal analysis of the tissue specificity of recessive female- sterile mutations of Drosophila melanogaster using a dominant female-sterile mutation Fs(l) K1237. Dev Biol 100: 365–373PubMedGoogle Scholar
  81. Perrimon N, Engstrom L, Mahowald AP (1985) A pupal lethal mutation with a paternally influenced maternal effect on embryonic development in Drosophila melanogaster. Dev Biol 110:480–491PubMedGoogle Scholar
  82. Petruzelli L, Herrera R, Arenas-Garcia R, Fernandez R, Birnbaum MJ, and Rosen OM (1986) Isolation of a Drosophila genomic sequence homologous to the kinase domain of the human insulin receptor and detection of the phosphorylated Drosophila receptor with an anti-peptide antibody. Proc Natl Acad Sci USA 83: 4710–4714Google Scholar
  83. Posakony LM (1987) The role of the DPP-C in the development of the imaginai discs in Drosophila melanogaster. PhD dissertation, Harvard UniversityGoogle Scholar
  84. Pribyl LJ, Watson DK, McWilliams MJ, Ascione R, Papas TS (1988) The Drosophila ets-2 gene: molecular structure, chromosomal localization, and developmental expression. Dev Biol 127: 45–53PubMedGoogle Scholar
  85. Price JV, Clifford RJ, Schüpbach T (1989) The maternal ventralizing locus torpedo is allelic to faint little ball, an embryonic lethal, and encodes the Drosophila EGF Receptor homolog. Cell 56: 1085–1092PubMedGoogle Scholar
  86. Priess JR, Schnabel H, Schnabel R (1987) The gip-1 locus and cellular interactions in early C. elegans embryos. Cell 51: 601–611PubMedGoogle Scholar
  87. Rapp UR, Goldsborough MD, Mark GE, Bonner TI, Groffen J, Reynolds FH Jr, Stephenson JR (1983) Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. Proc Natl Acad Sci USA 80: 4218–4222PubMedGoogle Scholar
  88. Rijsewijk F, Schuermann M, Wasenaar E, Parren P, Weigel D, Nusse R (1987) The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50: 649–657PubMedGoogle Scholar
  89. Rosenthal A, Rhee L, Yadegari R, Paro R, Ulrich A, Goeddel DV (1987) Structure and nucleotide sequence of a Drosophila melanogaster protein kinase C gene. EMBO J 6: 433–441PubMedGoogle Scholar
  90. Rothberg JM, Hartley DA, Walther Z, Artavanis-Tsakonas S (1988) slit: an EGF-homologous locus of Drosophila melanogaster involved in the development of the embryonic central nervous system. Cell 55: 1047–1059.PubMedGoogle Scholar
  91. Rushlow C, Frasch M, Doyle H, Levine M (1987) Maternal regulation of zerknüllt: a homoeobox gene controlling differentiation of dorsal tissues in Drosophila. Nature 330: 583–586PubMedGoogle Scholar
  92. Sadowski I, Stone JC, Pawson T (1986) A noncatalytic domain conserved among cytoplasmic protein-tyrosine kinases modifies the kinase function and transforming activity of Fujinami sarcoma virus P130gag, fps. Mol Cell Biol 6: 4396–4408PubMedGoogle Scholar
  93. Schechter AL, Stern DF, Vaidyanathan L, Decker SJ, Drebin JA, Greene MI, Weinberg RA (1984) The neu oncogene: an erb-B-related gene encoding a 185,000-Mr tumour antigen. Nature 312: 513–516PubMedGoogle Scholar
  94. Schejter ED, Shilo B-Z (1985) Characterization of functional domains of p21 ras by use of chimeric genes. EMBO J 4: 407–412PubMedGoogle Scholar
  95. Schejter ED, Shilo B-Z (1989) The Drosophila EGF receptor homolog (DER) gene is allelic to faint little ball, a locus essential for embryonic development. Cell 56: 1093–1104PubMedGoogle Scholar
  96. Schejter ED, Segal D, Glazer L, Shilo B-Z (1986) Alternative 5′ exons and tissue-specific expression of the Drosophila EGF receptor homolog transcripts. Cell 46: 1091–1101PubMedGoogle Scholar
  97. Schüpbach T (1987) Germline and soma cooperate during oogenesis to establish the dorsoventral pattern of eggshell and embryo in Drosophila melanogaster. Cell 49: 699–707PubMedGoogle Scholar
  98. Schüpbach T, Wieshaus E (1986) Matemal-effect mutations altering the anterior-posteroir pattern of the Drosophila embryo. Roux’s Arch Dev Biol 195: 302–317Google Scholar
  99. Scott MP, Carroll SB (1987) The segmentation and homeotic gene network in early Drosophila development. Cell 51: 689–698PubMedGoogle Scholar
  100. Segal D, Gelbart WM (1985) Shortvein, a new component of the decapentaplegic gene complex in Drosophila melanogaster. Genetics 109: 119–143PubMedGoogle Scholar
  101. Shepard SB, Broverman SA, Muskavitch MAT (1989) A tripartite interaction among neurogenic genes during Drosophila imaginai development. Genetics (in press)Google Scholar
  102. Shilo B-Z (1987) Proto-oncogenes in Drosophila melanogaster. Trends Genet 3: 69–72Google Scholar
  103. Shimizu K, Nakatsu Y, Sekiguchi M, Hokamura K, Tanaka K, Terada M, Sugimura T (1985) Molecular cloning of an activated human oncogene, homologous to v-raf, from primary stomach cancer. Proc Natl Acad Sci USA 82: 5641–5645PubMedGoogle Scholar
  104. Simon MA, Drees B, Kornberg T, Bishop JM (1985) The nucleotide sequence and the tissue- specific expression of Drosophila c-src. Cell 42: 831–840PubMedGoogle Scholar
  105. Simon MA, Kornberg TB, Bishop JM (1983) Three loci related to the src oncogene and tyrosine- specific protein kinase activity in Drosophila. Nature 302: 837–839PubMedGoogle Scholar
  106. Spencer FA (1984) The decapentaplegic gene complex and adult pattern formation in Drosophila. PhD dissertation, Harvard UniversityGoogle Scholar
  107. Spencer FA, Hoffmann FM, Gelbart WM (1982) Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28: 451–461PubMedGoogle Scholar
  108. St Johnston RD, Gelbart WM (1987) Decapentaplegic transcripts are localized along the dorsalventral axis of the Drosophila embryo. EMBO J 6: 2785–2791Google Scholar
  109. St Johnston RD, Hoffmann FM, Blackman RK, Segal D, Grimaila R, Padgett RW, Irick H, Gelbart WM (in preparation) The molecular organization of the decapentaplegic gene in Drosophila melanogaster.Google Scholar
  110. Stahl ML, Ferenz CR, Kelleher KL, Kritz RW, Knopf JL (1988) Sequence similarity of phospho- lipase C with the non-catalytic region of src. Nature 332: 269–272PubMedGoogle Scholar
  111. Steward R (1987) Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science 238: 692–694PubMedGoogle Scholar
  112. Steward R, McNally FJ, Schedi P (1984) Isolation of the dorsal locus of Drosophila. Nature 311: 262–265PubMedGoogle Scholar
  113. Steward R, Ambrose L, Schedi P (1985) Expression of the dorsal gene. Cold Spring Harbor Symp Quant Biol 50: 223–228PubMedGoogle Scholar
  114. Steward R, Zusman SB, Huang LH, Schedi P (1988) The dorsal protein is distributed in a gradient in early Drosophila embryos. Cell 55: 487–495PubMedGoogle Scholar
  115. Technau GM, Campos-Ortega JA (1987) Cell autonomy of expression of neurogenic genes of Drosophila melanogaster. Proc Natl Acad Sci USA 84: 4500–4504PubMedGoogle Scholar
  116. Telford BJJ, Butler B, Pirrotta V (1985) Alternative processing and developmental control of the transcripts of the Drosophila abl oncogene homologue. EMBO J 4: 2609–2615PubMedGoogle Scholar
  117. Thisse B, Stoetzel C, Dl Messal M, Perrin-Schmitt F (1987) Genes of the Drosophila maternal dorsal group control of specific expression of the zygotic gene twist in presumptive mesodermal, cells. Genes Dev 1: 709–715Google Scholar
  118. Tomlinson A (1985) The cellular dynamics of pattern formation in the eye of Drosophila. J Embryol Exp Morphol 89: 313–331PubMedGoogle Scholar
  119. Tomlinson A, Ready DF (1987) Neuronal differentiation in the Drosophila ommatidium. Dev Biol 120:366–376PubMedGoogle Scholar
  120. Tomlinson A, Boutwell DDL, Hafen E, Rubin GM (1987) Localization of the sevenless protein, a putative receptor for positional information, in the eye imaginai disc of Drosophila. Cell 51: 143–150PubMedGoogle Scholar
  121. Truman JW, Bate M (1988) Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 125: 145–157PubMedGoogle Scholar
  122. Vässin H, Bremer KA, Knust E, Campos-Orgeta JA (1987) The neurogenic gene Delta of Drosophila melanogaster is expressed in neurogenic territories and encodes a putative transmembrane protein with EGF-like repeats. EMBO J 6: 3431–3440PubMedGoogle Scholar
  123. Vincent WS III, Gregory RJ, Wadsworth SC (1989) Embryonic expression of a Drosophila src gene: alternate forms of the protein are expressed in segmental stripes and in the nervous system. Genes Dev 3: 334–347PubMedGoogle Scholar
  124. Wadsworth SC, Vincent WS III, Bilodeau-Wentworth D (1985) A Drosophila genomic sequence with homology to human epidermal growth factor receptor. Nature 314: 178–180PubMedGoogle Scholar
  125. Weeks DL, Melton DA (1987) A maternal mRNA localized to the vegetal hemisphere in Xenopus eggs codes for a growth factor related to TGF-ß. Cell 51: 861–867PubMedGoogle Scholar
  126. Wharton KA, Johansen KM, Xu T, Artavanis-Tsakonas S (1985) Nucleotide sequence from the neurogenic locus Notch implies a gene product that shares homology with proteins containing EGF-like repeats. Cell 43: 567–581PubMedGoogle Scholar
  127. Wilhelmsen KC, Eggleton K, Temin HM (1984) Nucleic acid sequences of the oncogene v-rel in reticuloendotheliosis virus strain T and its cellular homolog, the proto-oncogene c-rel. J Virol 52: 172–182PubMedGoogle Scholar
  128. Witte ON (1986) Functions of the abl oncogene. Cancer Surv 5: 183–197PubMedGoogle Scholar
  129. Yochem J, Weston K, Greenwald I (1988) The Caenorhabditis elegans lin-12 gene encodes a transmembrane protein with overall similarity to Drosophila Notch. Nature 335: 547–550PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1989

Authors and Affiliations

  • F. Michael Hoffmann
    • 1
  1. 1.McArdle Laboratory for Cancer ResearchUniversity of WisconsinMadisonUSA

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