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JOURNAL ARTICLES
Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta
B. Bettenhausen, M. Hrabe de Angelis, D. Simon, J.L. Guenet, A. Gossler
Development 1995 121: 2407-2418;

Summary

The Drosophila Delta (Dl) gene is essential for cell-cell communication regulating the determination of various cell fates during development. Dl encodes a transmembrane protein, which contains tandem arrays of epidermal-growth-factor-like repeats in the extracellular domain and directly interacts with Notch, another transmembrane protein with similar structural features, in a ligand-receptor-like manner. Similarly, cell-cell interactions involving Delta-like and Notch-like proteins are required for cell fate determinations in C. elegans. Notch homologues were also isolated from several vertebrate species, suggesting that cell-to-cell signaling mediated by Delta- and Notch-like proteins could also underlie cell fate determination during vertebrate development. However, in vertebrates, no Delta homologues have yet been described. We have isolated a novel mouse gene, Dll1 (delta-like gene 1), which maps to the mouse t-complex and whose deduced amino acid sequence strongly suggests that Dll1 represents a mammalian gene closely related to Drosophila Delta. Dll1 is transiently expressed during gastrulation and early organogenesis, and in a tissue-restricted manner in adult animals. Between day 7 and 12.5 of development, expression was detected in the paraxial mesoderm, closely correlated with somitogenesis, and in subsets of cells in the nervous system. In adult animals, transcripts were detected in lung and heart. Dll1 expression in the paraxial mesoderm and nervous system is strikingly similar to the expression of mouse Notch1 during gastrulation and early organogenesis. The overlapping expression patterns of the Dll1 and Notch1 genes suggest that cells in these tissues can communicate by interaction of the Dll1 and Notch1 proteins. Our results support the idea that Delta- and Notch-like proteins are involved in cell-to-cell communication in mammalian embryos and suggest a role for these proteins in cellular interactions underlying somitogenesis and development of the nervous system.

Reference

    1. Altschul S. F.,
    2. Gish W.,
    3. Miller W.,
    4. Myers E. W.,
    5. Lipman D. J.
    (1990) Basic local alignment search tool. J. Molec. Biol 215, 403–410
    OpenUrlCrossRefPubMedWeb of Science
    1. Artzt K.
    (1984) Gene mapping within the T/t complex of the mouse. III: t-lethal genes are arranged in three clusters on chromosome 17. Cell 39, 565–572
    OpenUrlCrossRefPubMed
    1. Artzt K.,
    2. McCormick P.,
    3. Bennett D.
    (1982) Gene mapping within the T/t complex of the mouse. I. t-lethal genes are nonallelic. Cell 28, 463–470
    OpenUrlCrossRefPubMedWeb of Science
    1. Austin J.,
    2. 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, 589–599
    OpenUrlCrossRefPubMedWeb of Science
    1. Basler K.,
    2. Edlund T.,
    3. Jessell T. M.,
    4. Yamada T.
    (1993) Control of cell pattern in the neural tube: regulation of cell differentiation by dorsalin-1, a novel TGFfamily member. Cell 73, 687–702
    OpenUrlCrossRefPubMedWeb of Science
    1. Bennett D.
    (1975) The T-locus of the mouse. Cell 6, 441–454
    OpenUrlCrossRefWeb of Science
    1. Bennett D.,
    2. Dunn L. C.
    (1960) A lethal mutant (tw18) in the house mouse showing partial duplications. J. Exp. Zool 143, 203–219
    OpenUrlCrossRef
    1. Bierkamp C.,
    2. Campos-Ortega J. A.
    (1993) A zebrafish homologue of the Drosophila neurogenic gene Notch and its pattern of transcription during early embryogenesis. Mech. Dev 43, 87–100
    OpenUrlCrossRefPubMedWeb of Science
    1. Breen M.,
    2. Deakin L.,
    3. Macdonald B.,
    4. Miller S.,
    5. Sibson R.,
    6. Tartellin E.,
    7. Avner P.,
    8. Bourgade F.,
    9. Guenet J. L.,
    10. Montagutelli X.,
    11. Poirier C.,
    12. Simon D.,
    13. Tailor D.,
    14. Bishop M.,
    15. Kelly M.,
    16. Rysavy F.,
    17. Rastan S.,
    18. Norris D.,
    19. Shepherd D.,
    20. Abbott C.
    (1994). Towards high regulation maps of the mouse and human genomes- a facility for ordering markers to 0.1 cM resolution. Human Molecular Genetics 3, 621–627
    OpenUrlAbstract/FREE Full Text
    1. Búcan M.,
    2. Herrmann B. G.,
    3. Frischauf A.,
    4. Bautch V. L.,
    5. Bode V.,
    6. Silver L.,
    7. Martin G. L.,
    8. Lehrach H.
    (1987) Deletion and duplication ofDNA sequences is associated with the embryonic lethal phenotype of the t9complementation group of the mouse t complex. Genes Dev 1, 376–385
    OpenUrlAbstract/FREE Full Text
    1. Chomczynski P.,
    2. Sacchi N.
    (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochemistry 162, 156–159
    OpenUrlCrossRefPubMedWeb of Science
    1. Coffman C.,
    2. Harris W.,
    3. Kintner C.
    (1990) Xotch, the Xenopus homolog of Drosophila Notch. Science 249, 1438–1441
    OpenUrlAbstract/FREE Full Text
    1. Coffman C. R.,
    2. Skoglund P.,
    3. Harris W. A.,
    4. Kintner C. R.
    (1993) Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus-embryos. Cell 73, 659–671
    OpenUrlCrossRefPubMedWeb of Science
    1. Conlon R. A.,
    2. Reaume A. G.,
    3. Rossant J.
    (1995) Notch1 is required for the coordinate segmentation of somites. Development 121, 1533–1545
    OpenUrlAbstract
    1. Corbin V.,
    2. Michelson A. M.,
    3. Abmayr S. M.,
    4. Neel V.,
    5. Alcamo E.,
    6. Maniatis T.,
    7. Young M. W.
    (1991) A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67, 311–323
    OpenUrlCrossRefPubMedWeb of Science
    1. Davies J. A.,
    2. Cook G. M.,
    3. Stern C. D.,
    4. Keynes R. J.
    (1990) Isolation from chick somites of a glycoprotein fraction that causes collapse of dorsal root ganglion growth cones. Neuron 4, 11–20
    OpenUrlCrossRefPubMedWeb of Science
    1. Davis C. G.
    (1990) The many faces of epidermal growth factor repeats. New Biologist 2, 410–419
    OpenUrlPubMed
    1. del Amo F. F.,
    2. Gendron Maguire M.,
    3. Swiatek P. J.,
    4. Jenkins N. A.,
    5. Copeland N. G.,
    6. Gridley T.
    (1993) Cloning, analysis, and chromosomal localization of Notch-1, a mouse homolog of Drosophila Notch. Genomics 15, 259–264
    OpenUrlCrossRefPubMedWeb of Science
    1. del Amo F. F.,
    2. Smith D. E.,
    3. Swiatek P. J.,
    4. Gendron Maguire M.,
    5. Greenspan R. J.,
    6. McMahon A. P.,
    7. Gridley T.
    (1992) Expression pattern of Motch, a mouse homolog of Drosophila Notch, suggests an important role in early postimplantation mouse development. Development 115, 737–744
    OpenUrlAbstract/FREE Full Text
    1. Devereux J.,
    2. Haeberli P.,
    3. Smithies O.
    (1984) A comprehensive set of sequence analysis programs for the VAX. Nucl. Acid. Res 12, 387–395
    OpenUrlAbstract/FREE Full Text
    1. Ellisen L. W.,
    2. Bird J.,
    3. West D. C.,
    4. Soreng A. L.,
    5. Reynolds T. C.,
    6. Smith S. D.,
    7. Sklar J.
    (1991) TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66, 649–661
    OpenUrlCrossRefPubMedWeb of Science
    1. Fehon R. G.,
    2. Kooh P. J.,
    3. Rebay I.,
    4. Regan C. L.,
    5. Xu T.,
    6. Muskavitch M. A.,
    7. Artavanis Tsakonas S.
    (1990) Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 61, 523–534
    OpenUrlCrossRefPubMedWeb of Science
    1. Goldstein R. S.,
    2. Teillet M.-A.,
    3. Kalcheim C.
    (1990) The microenvironment created by grafting rostral half-somites is mitogenic for neural crest cells. Proc. Natl. Acad. Sci. USA 87, 4476–4480
    OpenUrlAbstract/FREE Full Text
    1. Greenwald I. S.,
    2. Sternberg P. W.,
    3. Horvitz H. R.
    (1983) The lin −12 locus specifies cell fates in Caenorhabditis elegans. Cell 34, 435–444
    OpenUrlCrossRefPubMedWeb of Science
    1. Haenlin M.,
    2. Kramatschek B.,
    3. Campos-Ortega J. A.
    (1990) The pattern of transcription of the neurogenic gene Delta of Drosophila melanogaster. Development 110, 905–914
    OpenUrlAbstract/FREE Full Text
    1. Hartenstein A. Y.,
    2. Rugendorff A.,
    3. Tepass U.,
    4. Hartenstein V.
    (1992) The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116, 1203–1220
    OpenUrlAbstract/FREE Full Text
    1. Heitzler P.,
    2. Simpson P.
    (1993) Altered epidermal growth factor-like sequences provide evidence for a role of Notch as a receptor in cell fate decisions. Development 117, 1113–1123
    OpenUrlAbstract
    1. Hogan B.,
    2. Holland P.,
    3. Schofield P.
    (1985) How is the mouse segmented?. Trends Genetics 1, 67–74
    OpenUrlCrossRef
    1. Huarte J.,
    2. Stutz A.,
    3. O'Connell M. L.,
    4. Gubler P. D.,
    5. Belin D.,
    6. Darrow A. L.,
    7. Strickland S.,
    8. Vassalli J. D.
    (1992) Tansient Translation Silencing by Reverse mRNA Deadenylation. Cell 69, 1021–1130
    OpenUrlCrossRefPubMedWeb of Science
    1. Keynes R. J.,
    2. Stern C. D.
    (1984) Segmentation in the vertebrate nervous system. Nature 310, 786–789
    OpenUrlCrossRefPubMedWeb of Science
    1. Kopczynski C. C.,
    2. Alton A. K.,
    3. Fechtel K.,
    4. Kooh P. J.,
    5. Muskavitch M. A.
    (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 2, 1723–1735
    OpenUrlAbstract/FREE Full Text
    1. Laborda J.,
    2. Sausville E. A.,
    3. Hoffman T.,
    4. Notario V.
    (1993) dlk, a putative mammalian homeotic gene differentially expressed in small cell lung carcinoma and neuroendocrine tumor cell line. J. Biol. Chem 268, 6–.
    OpenUrl
    1. Lardelli M.,
    2. Dahlstrand J.,
    3. Lendahl U.
    (1994) The novel Notchhomologue mouse Notch 3 lacks specific epidermal growth factor-repeats and is expressed in proliferating neuroepithelium. Mech. Dev 46, 123–136
    OpenUrlCrossRefPubMedWeb of Science
    1. Lardelli M.,
    2. Lendahl U.
    (1993) Motch A and motch B--two mouse Notch homologues coexpressed in a wide variety of tissues. Exp. Cell Res 204, 2–.
    OpenUrl
    1. Lieber T.,
    2. Wesley C. S.,
    3. Alcamo E.,
    4. Hassel B.,
    5. Krane J. F.,
    6. Campos-Ortega J. A.,
    7. Young M. W.
    (1992) Single amino acid substitutions in EGF-like elements of Notch and Delta modify Drosophila development and affect cell adhesion in vitro. Neuron 9, 847–859
    OpenUrlCrossRefPubMedWeb of Science
    1. Lindsell C. E.,
    2. Shawber C. J.,
    3. Boulter J.,
    4. Weinmaster G.
    (1995) Jagged: A Mammalian Ligand That Activates Notch1. Cell 80, 909–917
    OpenUrlCrossRefPubMedWeb of Science
    1. Mello C. C.,
    2. Draper B. W.,
    3. Priess J. R.
    (1994) The maternal genes apx-1 and glp-1 and establishment of dorsal-ventral polarity in the early C. elegans embryo. Cell 77, 95–106
    OpenUrlCrossRefPubMedWeb of Science
    1. Moser G. C.,
    2. Gluecksohn-Waelsch S.
    (1967) Developmental genetics of a recessive allele at the complex T-locus in the mouse. Dev. Biol 16, 564–576
    OpenUrlCrossRefPubMed
    1. Muskavitch M. A.
    (1994) Delta-notch signaling and Drosophila cell fate choice. Dev. Biol 166, 415–430
    OpenUrlCrossRefPubMedWeb of Science
    1. Muskavitch M. A.,
    2. Hoffmann F. M.
    (1990) Homologs of vertebrate growth factors in Drosophila melanogaster and other invertebrates. Curr. Top. Dev. Biol 24, 289–328
    OpenUrlPubMed
    1. Placzek M.,
    2. Yamada T.,
    3. Tessierlavigne M.,
    4. Jessell T.,
    5. Dodd J.
    (1991) Control of dorsoventral pattern in vertebrate neural development-induction and polarizing properties of the floor plate. Development 113, 105–122
    OpenUrlAbstract/FREE Full Text
    1. Reaume A. G.,
    2. Conlon R. A.,
    3. Zirngibl R.,
    4. Yamaguchi T. P.,
    5. Rossant J.
    (1992) Expression analysis of a Notch homologue in the mouse embryo. Dev. Biol 154, 377–387
    OpenUrlCrossRefPubMedWeb of Science
    1. Rebay I.,
    2. Fleming R. J.,
    3. Fehon R. G.,
    4. Cherbas L.,
    5. Cherbas P.,
    6. Artavanis Tsakonas S.
    (1991) Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell 67, 687–699
    OpenUrlCrossRefPubMedWeb of Science
    1. Shaw G.,
    2. Kamen R.
    (1986) A conserved AU sequence from the 3untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46, 659–667
    OpenUrlCrossRefPubMedWeb of Science
    1. Smas C. M.,
    2. Sul H. S.
    (1993) Pref-1, a protein containing EGF-like repeats, inhibits adipocyte differentiation. Cell 73, 725–734
    OpenUrlCrossRefPubMedWeb of Science
    1. Swiatek P. J.,
    2. Lindsell C. E.,
    3. Delamo F. F.,
    4. Weinmaster G.,
    5. Gridley T.
    (1994) Notch1 is essential for postimplantation development in mice. Genes Dev 8, 707–719
    OpenUrlAbstract/FREE Full Text
    1. Tax F. E.,
    2. Yeargers J. J.,
    3. Thomas J. H.
    (1994) Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila. Nature 368, 150–154
    OpenUrlCrossRefPubMed
    1. Technau G. M.,
    2. Campos-Ortega J. A.
    (1987) Cell autonomy of expression of neurogenic genes of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 84, 4500–4504
    OpenUrlAbstract/FREE Full Text
    1. Tepass U.,
    2. Hartenstein V.
    (1995) Neurogenic and proneural genes control cell fate specification in the Drosophila endoderm. Development 121, 393–405
    OpenUrlAbstract
    1. Vässin H.,
    2. Bremer K. A.,
    3. Knust E.,
    4. Campos-Ortega J. A.
    (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, 3431–3440
    OpenUrlPubMedWeb of Science
    1. Weinmaster G.,
    2. Roberts V. J.,
    3. Lemke G.
    (1991) A homolog of Drosophila Notch expressed during mammalian development. Development 113, 199–205
    OpenUrlAbstract
    1. Weinmaster G.,
    2. Roberts V. J.,
    3. Lemke G.
    (1992) Notch2: a second mammalian Notch gene. Development 116, 931–941
    OpenUrlAbstract/FREE Full Text
    1. Wharton K. A.,
    2. Johansen K. M.,
    3. Xu T.,
    4. Artavanis Tsakonas S.
    (1985) Nucleotide sequence from the neurogenic locus Notch implies a geneproduct that shares homology with proteins containing EGF-like repeats. Cell 43, 567–581
    OpenUrlCrossRefPubMedWeb of Science
    1. Yamada T.,
    2. Pfaff S. L.,
    3. Edlund T.,
    4. Jessell T. M.
    (1993) Control of cellpattern in the neural-tube-motor-neuron induction by diffusible factors from notochord and floor plate. Cell 73, 673–686
    OpenUrlCrossRefPubMedWeb of Science
    1. Yamada T.,
    2. Placzek M.,
    3. Tanaka H.,
    4. Dodd J.,
    5. Jessell T. M.
    (1991) Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64, 635–647
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta
B. Bettenhausen, M. Hrabe de Angelis, D. Simon, J.L. Guenet, A. Gossler
Development 1995 121: 2407-2418;
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