Advertisement
JOURNAL ARTICLES
The Notch ligand, X-Delta-2, mediates segmentation of the paraxial mesoderm in Xenopus embryos
W.C. Jen, D. Wettstein, D. Turner, A. Chitnis, C. Kintner
Development 1997 124: 1169-1178;

Summary

Segmentation of the vertebrate embryo begins when the paraxial mesoderm is subdivided into somites, through a process that remains poorly understood. To study this process, we have characterized X-Delta-2, which encodes the second Xenopus homolog of Drosophila Delta. Strikingly, X-Delta-2 is expressed within the presomitic mesoderm in a set of stripes that corresponds to prospective somitic boundaries, suggesting that Notch signaling within this region establishes a segmental prepattern prior to somitogenesis. To test this idea, we introduced antimorphic forms of X-Delta-2 and Xenopus Suppressor of Hairless (X-Su(H)) into embryos, and assayed the effects of these antimorphs on somite formation. In embryos expressing these antimorphs, the paraxial mesoderm differentiated normally into somitic tissue, but failed to segment properly. Both antimorphs also disrupted the segmental expression of X-Delta-2 and Hairy2A, a basic helix-loop-helix (bHLH) gene, within the presomitic mesoderm. These observations suggest that X-Delta-2, via X-Notch-1, plays a role in segmentation, by mediating cell-cell interactions that underlie the formation of a segmental prepattern prior to somitogenesis.

REFERENCES

    1. Amakawa R.,
    2. Jing W.,
    3. Ozawa K.,
    4. Matsunami N.,
    5. Hamaguchi Y.,
    6. Matsuda F.,
    7. Kawaichi M.,
    8. Honjo T.
    (1993) Human Jk recombination signal binding protein gene (IGKJRB): comparison with its mouse homologue. Genomics 17, 306–315
    OpenUrlCrossRefPubMedWeb of Science
    1. Artavanis-Tsakonas S.,
    2. Matsuno K.,
    3. Fortini M. E.
    (1995) Notch signaling. Science 268, 225–232
    OpenUrlAbstract/FREE Full Text
    1. Bailey A. M.,
    2. Posakony J. W.
    (1995) Suppressor of hairless directly activates transcription of enhancer of split complex genes in response to Notch receptor activity. Genes Dev 9, 2609–2622
    OpenUrlAbstract/FREE Full Text
    1. Bettenhausen B.,
    2. de Angelis M.H.,
    3. Simon D.,
    4. Guenet J. L.,
    5. Gossler A.
    (1995) Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta. Development 121, 2407–2418
    OpenUrlAbstract
    1. Campos-Ortega J. A.
    (1994) Cellular interactions in the developing nervous system of Drosophila. Cell 77, 969–75
    OpenUrlCrossRefPubMedWeb of Science
    1. Chitnis A.,
    2. Henrique D.,
    3. Lewis J.,
    4. Ish-Horowicz D.,
    5. Kintner C.
    (1995) Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375, 761–766
    OpenUrlCrossRefPubMedWeb of Science
    1. Christensen S.,
    2. Kodoyianni V.,
    3. Bosenberg M.,
    4. Friedman L.,
    5. Kimble J.
    (1996) lag-1, a gene required for lin-12 and glp-1 signaling in Caenorhabditis elegans, is homologous to human CBF1 and Drosophila Su(H). Development 122, 1373–1383
    OpenUrlAbstract
    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. Couso J. P.,
    2. Knust E.,
    3. Martinez Arias A.
    (1995) Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Curr. Biol 5, 1437–1448
    OpenUrlCrossRefPubMedWeb of Science
    1. de Celis J.,
    2. Garcia-Bellido A.,
    3. Bray S. J.
    (1996) Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc. Development 122, 359–369
    OpenUrlAbstract
    1. Del Amo 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. Doherty D.,
    2. Feger G.,
    3. Younger S. S.,
    4. Jan L. Y.,
    5. Jan Y. N.
    (1996) Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation. Genes Dev 10, 421–434
    OpenUrlAbstract/FREE Full Text
    1. Fortini M. E.,
    2. Artavanis-Tsakonas S.
    (1994) The suppressor of hairless protein participates in notch receptor signaling. Cell 79, 273–282
    OpenUrlCrossRefPubMedWeb of Science
    1. Frank D.,
    2. Harland R. M.
    (1991) Transient expression of XMyoD in non-somitic mesoderm of Xenopus gastrulae. Development 113, 1387–1393
    OpenUrlAbstract
    1. Gurdon J. B.,
    2. Mohun T. J.,
    3. Brennan S.,
    4. Cascio S.
    (1985) Actin genes in Xenopus and their developmental control. J. Embryol. Exp. Morphol 89, 125–136
    1. Hamilton L.
    (1969) The formation of somites in Xenopus. J. Embryol. Exp. Morphol 22, 253–264
    OpenUrlPubMed
    1. Harland R. M.
    (1991) In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol 36, 685–695
    OpenUrlCrossRefPubMedWeb of Science
    1. Harvey R. P.
    (1992) MyoD protein expression in Xenopus embryos closely follows a mesoderm induction-dependent amplification of MyoD transcription and is synchronous across the future somite axis. Mech. Dev 37, 141–149
    OpenUrlCrossRefPubMed
    1. Hemmati-Brivanlou A.,
    2. Harland R. M.
    (1989) Expression of an engrailed-related protein is induced in the anterior neural ectoderm of early Xenopus embryos. Development 106, 611–617
    OpenUrlAbstract
    1. Henrique D.,
    2. Adam J.,
    3. Myat A.,
    4. Chitnis A.,
    5. Lewis J.,
    6. Ish-Horowicz. D.
    (1995) Expression of a Delta homologue in prospective neurons in the chick [see comments]. Nature 375, 787–790
    OpenUrlCrossRefPubMed
    1. Hopwood N. D.,
    2. Pluck A.,
    3. Gurdon J. B.,
    4. Dilworth S. M.
    (1992) Expression of XMyoD protein in early Xenopuslaevis embryos. Development 114, 31–38
    OpenUrlAbstract
    1. Jarriault S.,
    2. Brou C.,
    3. Logeat F.,
    4. Schroeder E. H.,
    5. Kopan R.,
    6. Israel A.
    (1995) Signaling downstream of activated mammalian Notch [see comments]. Nature 377, 355–358
    OpenUrlCrossRefPubMedWeb of Science
    1. Keynes R. J.,
    2. Stern C. D.
    (1984) Segmentation in the vertebrate nervous system. Nature 310, 786–9
    OpenUrlCrossRefPubMedWeb of Science
    1. Kim J.,
    2. Irvine K. D.,
    3. Carroll S. B.
    (1995) Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell 82, 795–802
    OpenUrlCrossRefPubMedWeb of Science
    1. Kintner C. R.,
    2. Brockes J. P.
    (1985) Monoclonal antibodies to the cells of a regenerating limb. J. Embryol. Exp. Morphol 89, 37–55
    OpenUrlPubMedWeb of Science
    1. Kintner C. R.,
    2. Melton D. A.
    (1987) Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. Development 99, 311–325
    OpenUrlAbstract
    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, 364–372
    OpenUrlCrossRefPubMedWeb of Science
    1. Lecourtois M.,
    2. Schweisguth F.
    (1995) The neurogenic suppressor of hairless DNA-binding protein mediates the transcriptional activation of the enhancer of split complex genes triggered by Notch signaling. Genes Dev 9, 2598–2608
    OpenUrlAbstract/FREE Full Text
    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. Matsunami N.,
    2. Hamaguchi Y.,
    3. Yamamoto Y.,
    4. Kuze K.,
    5. Kangawa K.,
    6. Matsuo H.,
    7. Kawaichi M.,
    8. Honjo T.
    (1989) A protein binding to the Jrecombination sequence of immunoglobulin genes contains a sequence related to the integrase motif. Nature 342, 934–937
    OpenUrlCrossRefPubMed
    1. Meier S.
    (1979) Development of the chick embryo mesoblast. Formation of the embryonic axis and establishment of the metameric pattern. Dev. Biol 73, 24–45
    OpenUrlCrossRefPubMed
    1. Muller M.v.,
    2. Weizsäcker E.,
    3. Campos-Ortega J. A.
    (1996) Expression domains of a zebrafish homologue of the Drosophila pair-rule gene hairy correspond to primordia of alternating somites. Development 122, 2071–2078
    OpenUrlAbstract
    1. Oka C.,
    2. Nakano T.,
    3. Wakeham A.,
    4. de la, Pompa, Jl,
    5. Mori C.,
    6. Sakai T.,
    7. Okazaki S.,
    8. Kawaichi M.,
    9. Shiota K.,
    10. Mak T. W.,
    11. Honjo T.
    (1995) Disruption of the mouse RBP-Jgene results in early embryonic death. Development 121, 3291–3301
    OpenUrlAbstract
    1. Pearson M.,
    2. Elsdale T.
    (1979) Somitogenesis in amphibian embryos. I. Experimental evidence for an interaction between two temporal factors in the specification of somite pattern. J. Embryol. Exp. Morphol 51, 27–50
    OpenUrlPubMed
    1. Posakony J. W.
    (1994) Nature versus nurture: asymmetric cell divisions in Drosophila bristle development [comment]. Cell 76, 415–418
    OpenUrlCrossRefPubMedWeb of Science
    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. Schmidt J.,
    2. Francois V.,
    3. Bier E.,
    4. Kimelman D.
    (1995) Drosophila short gastrulation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning. Development 121, 4319–4328
    OpenUrlAbstract
    1. Schweisguth F.,
    2. Posakony J. W.
    (1992) Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein gene, controls sensory organ cell fates. Cell 69, 1199–1212
    OpenUrlCrossRefPubMedWeb of Science
    1. St Johnston D.,
    2. Nusslein-Volhard C.
    (1992) The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Sun X.,
    2. Artavanis-Tsakonas S.
    (1996) The intracellular deletions of DELTA and SERRATE define dominant negative forms of the Drosophila Notch ligands. Development 122, 2465–24474
    OpenUrlAbstract
    1. Swiatek P. J.,
    2. Lindsell C. E.,
    3. Franco del Amo F.,
    4. Weinmaster G.,
    5. Gridley T.
    (1994) Notch 1 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. Turner D. L.,
    2. Weintraub H.
    (1994) Expression of acheate-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev 8, 1434–1447
    OpenUrlAbstract/FREE Full Text
    1. Wettstein D.,
    2. Turner D.,
    3. Kintner C.
    (1997) The Xenopus homolog of Drosophila Supressor of Hairless mediates Notch signaling during primary neurogenesis. Development 124, 693–702
    OpenUrlAbstract
    1. Wilkinson H. A.,
    2. Fitzgerald K.,
    3. Greenwald I.
    (1994) Reciprocal changes in expression of the receptor lin-12 and its ligand lag-2 prior to commitment in a C. elegans cell fate decision. Cell 79, 1187–1198
    OpenUrlCrossRefPubMedWeb of Science
    1. Youn B. W.,
    2. Malacinski G. M.
    (1981) Somitogenesis in the amphibian Xenopuslaevis: scanning electron microscopic analysis of intrasomitic cellular arrangements during somite rotation. J. Embryol. Exp. Morphol 64, 23–43
    OpenUrlPubMed
Back to top

 Download PDF

Email
JOURNAL ARTICLES
The Notch ligand, X-Delta-2, mediates segmentation of the paraxial mesoderm in Xenopus embryos
W.C. Jen, D. Wettstein, D. Turner, A. Chitnis, C. Kintner
Development 1997 124: 1169-1178;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

A new society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.

Upcoming special issue: call for papers

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.