Abstract
The Notch signaling cascade is involved in many developmental decisions, a paradigm of which has been the selection between epidermal and neural cell fates in both invertebrates and vertebrates. Notch has also been implicated as a regulator of myogenesis, although its precise function there has remained controversial. Here we show that the muscle-determining factor MyoD is a direct, positive regulator of the Notch ligand Delta-1 in prospective myoblasts of the pre-involuted mesoderm in Xenopus gastrulae. Injection of a dominant MyoD repressor variant ablates mesodermal Delta-1 expression in vivo. Furthermore, MyoD-dependent Delta-1 induction is sufficient to activate transcription from promoters of E(spl)-related genes in a Notch-dependent manner. These results indicate that a hallmark of neural cell fate determination, i.e. the feedback loop between differentiation promoting basic helix-loop-helix proteins and the Notch regulatory circuitry, is conserved in myogenesis, supporting a direct involvement of Notch in muscle determination.
Full Text
The Full Text of this article is available as a PDF (302.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Artavanis-Tsakonas S., Matsuno K., Fortini M. E. Notch signaling. Science. 1995 Apr 14;268(5208):225–232. doi: 10.1126/science.7716513. [DOI] [PubMed] [Google Scholar]
- Baylies M. K., Bate M., Ruiz Gomez M. Myogenesis: a view from Drosophila. Cell. 1998 Jun 12;93(6):921–927. doi: 10.1016/s0092-8674(00)81198-8. [DOI] [PubMed] [Google Scholar]
- Bettenhausen B., Hrabe de Angelis M., Simon D., Guénet J. L., Gossler A. Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta. Development. 1995 Aug;121(8):2407–2418. doi: 10.1242/dev.121.8.2407. [DOI] [PubMed] [Google Scholar]
- Chitnis A., Henrique D., Lewis J., Ish-Horowicz D., Kintner C. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature. 1995 Jun 29;375(6534):761–766. doi: 10.1038/375761a0. [DOI] [PubMed] [Google Scholar]
- Coffman C., Harris W., Kintner C. Xotch, the Xenopus homolog of Drosophila notch. Science. 1990 Sep 21;249(4975):1438–1441. doi: 10.1126/science.2402639. [DOI] [PubMed] [Google Scholar]
- Conlon R. A., Reaume A. G., Rossant J. Notch1 is required for the coordinate segmentation of somites. Development. 1995 May;121(5):1533–1545. doi: 10.1242/dev.121.5.1533. [DOI] [PubMed] [Google Scholar]
- Corbin V., Michelson A. M., Abmayr S. M., Neel V., Alcamo E., Maniatis T., Young M. W. A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell. 1991 Oct 18;67(2):311–323. doi: 10.1016/0092-8674(91)90183-y. [DOI] [PubMed] [Google Scholar]
- Cossu G., Tajbakhsh S., Buckingham M. How is myogenesis initiated in the embryo? Trends Genet. 1996 Jun;12(6):218–223. doi: 10.1016/0168-9525(96)10025-1. [DOI] [PubMed] [Google Scholar]
- Doe C. Q., Skeath J. B. Neurogenesis in the insect central nervous system. Curr Opin Neurobiol. 1996 Feb;6(1):18–24. doi: 10.1016/s0959-4388(96)80004-3. [DOI] [PubMed] [Google Scholar]
- George-Weinstein M., Gerhart J., Reed R., Flynn J., Callihan B., Mattiacci M., Miehle C., Foti G., Lash J. W., Weintraub H. Skeletal myogenesis: the preferred pathway of chick embryo epiblast cells in vitro. Dev Biol. 1996 Jan 10;173(1):279–291. doi: 10.1006/dbio.1996.0023. [DOI] [PubMed] [Google Scholar]
- Greenwald I. Structure/function studies of lin-12/Notch proteins. Curr Opin Genet Dev. 1994 Aug;4(4):556–562. doi: 10.1016/0959-437x(94)90072-b. [DOI] [PubMed] [Google Scholar]
- Gridley T. Notch signaling in vertebrate development and disease. Mol Cell Neurosci. 1997;9(2):103–108. doi: 10.1006/mcne.1997.0610. [DOI] [PubMed] [Google Scholar]
- Haddon C., Smithers L., Schneider-Maunoury S., Coche T., Henrique D., Lewis J. Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development. 1998 Feb;125(3):359–370. doi: 10.1242/dev.125.3.359. [DOI] [PubMed] [Google Scholar]
- Henrique D., Adam J., Myat A., Chitnis A., Lewis J., Ish-Horowicz D. Expression of a Delta homologue in prospective neurons in the chick. Nature. 1995 Jun 29;375(6534):787–790. doi: 10.1038/375787a0. [DOI] [PubMed] [Google Scholar]
- Henrique D., Hirsinger E., Adam J., Le Roux I., Pourquié O., Ish-Horowicz D., Lewis J. Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina. Curr Biol. 1997 Sep 1;7(9):661–670. doi: 10.1016/s0960-9822(06)00293-4. [DOI] [PubMed] [Google Scholar]
- Hollenberg S. M., Cheng P. F., Weintraub H. Use of a conditional MyoD transcription factor in studies of MyoD trans-activation and muscle determination. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8028–8032. doi: 10.1073/pnas.90.17.8028. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hopwood N. D., Pluck A., Gurdon J. B. MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. EMBO J. 1989 Nov;8(11):3409–3417. doi: 10.1002/j.1460-2075.1989.tb08505.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jarriault S., Brou C., Logeat F., Schroeter E. H., Kopan R., Israel A. Signalling downstream of activated mammalian Notch. Nature. 1995 Sep 28;377(6547):355–358. doi: 10.1038/377355a0. [DOI] [PubMed] [Google Scholar]
- Jen W. C., Wettstein D., Turner D., Chitnis A., Kintner C. The Notch ligand, X-Delta-2, mediates segmentation of the paraxial mesoderm in Xenopus embryos. Development. 1997 Mar;124(6):1169–1178. doi: 10.1242/dev.124.6.1169. [DOI] [PubMed] [Google Scholar]
- Kato H., Taniguchi Y., Kurooka H., Minoguchi S., Sakai T., Nomura-Okazaki S., Tamura K., Honjo T. Involvement of RBP-J in biological functions of mouse Notch1 and its derivatives. Development. 1997 Oct;124(20):4133–4141. doi: 10.1242/dev.124.20.4133. [DOI] [PubMed] [Google Scholar]
- Kato K., Gurdon J. B. Single-cell transplantation determines the time when Xenopus muscle precursor cells acquire a capacity for autonomous differentiation. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1310–1314. doi: 10.1073/pnas.90.4.1310. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kidd S., Lieber T., Young M. W. Ligand-induced cleavage and regulation of nuclear entry of Notch in Drosophila melanogaster embryos. Genes Dev. 1998 Dec 1;12(23):3728–3740. doi: 10.1101/gad.12.23.3728. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kolm P. J., Sive H. L. Efficient hormone-inducible protein function in Xenopus laevis. Dev Biol. 1995 Sep;171(1):267–272. doi: 10.1006/dbio.1995.1279. [DOI] [PubMed] [Google Scholar]
- Kopan R., Nye J. S., Weintraub H. The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Development. 1994 Sep;120(9):2385–2396. doi: 10.1242/dev.120.9.2385. [DOI] [PubMed] [Google Scholar]
- Kopan R., Turner D. L. The Notch pathway: democracy and aristocracy in the selection of cell fate. Curr Opin Neurobiol. 1996 Oct;6(5):594–601. doi: 10.1016/s0959-4388(96)80090-0. [DOI] [PubMed] [Google Scholar]
- Lecourtois M., Schweisguth F. Indirect evidence for Delta-dependent intracellular processing of notch in Drosophila embryos. Curr Biol. 1998 Jun 18;8(13):771–774. doi: 10.1016/s0960-9822(98)70300-8. [DOI] [PubMed] [Google Scholar]
- Lewis J. Neurogenic genes and vertebrate neurogenesis. Curr Opin Neurobiol. 1996 Feb;6(1):3–10. doi: 10.1016/s0959-4388(96)80002-x. [DOI] [PubMed] [Google Scholar]
- Lindsell C. E., Shawber C. J., Boulter J., Weinmaster G. Jagged: a mammalian ligand that activates Notch1. Cell. 1995 Mar 24;80(6):909–917. doi: 10.1016/0092-8674(95)90294-5. [DOI] [PubMed] [Google Scholar]
- Ma Q., Kintner C., Anderson D. J. Identification of neurogenin, a vertebrate neuronal determination gene. Cell. 1996 Oct 4;87(1):43–52. doi: 10.1016/s0092-8674(00)81321-5. [DOI] [PubMed] [Google Scholar]
- McGrew M. J., Pourquié O. Somitogenesis: segmenting a vertebrate. Curr Opin Genet Dev. 1998 Aug;8(4):487–493. doi: 10.1016/s0959-437x(98)80122-6. [DOI] [PubMed] [Google Scholar]
- Myat A., Henrique D., Ish-Horowicz D., Lewis J. A chick homologue of Serrate and its relationship with Notch and Delta homologues during central neurogenesis. Dev Biol. 1996 Mar 15;174(2):233–247. doi: 10.1006/dbio.1996.0069. [DOI] [PubMed] [Google Scholar]
- Nye J. S., Kopan R., Axel R. An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development. 1994 Sep;120(9):2421–2430. doi: 10.1242/dev.120.9.2421. [DOI] [PubMed] [Google Scholar]
- Oka C., Nakano T., Wakeham A., de la Pompa J. L., Mori C., Sakai T., Okazaki S., Kawaichi M., Shiota K., Mak T. W. Disruption of the mouse RBP-J kappa gene results in early embryonic death. Development. 1995 Oct;121(10):3291–3301. doi: 10.1242/dev.121.10.3291. [DOI] [PubMed] [Google Scholar]
- Rusconi J. C., Corbin V. Evidence for a novel Notch pathway required for muscle precursor selection in Drosophila. Mech Dev. 1998 Dec;79(1-2):39–50. doi: 10.1016/s0925-4773(98)00170-1. [DOI] [PubMed] [Google Scholar]
- Schroeter E. H., Kisslinger J. A., Kopan R. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature. 1998 May 28;393(6683):382–386. doi: 10.1038/30756. [DOI] [PubMed] [Google Scholar]
- Shawber C., Nofziger D., Hsieh J. J., Lindsell C., Bögler O., Hayward D., Weinmaster G. Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. Development. 1996 Dec;122(12):3765–3773. doi: 10.1242/dev.122.12.3765. [DOI] [PubMed] [Google Scholar]
- Steinbach O. C., Ulshöfer A., Authaler A., Rupp R. A. Temporal restriction of MyoD induction and autocatalysis during Xenopus mesoderm formation. Dev Biol. 1998 Oct 15;202(2):280–292. doi: 10.1006/dbio.1998.8993. [DOI] [PubMed] [Google Scholar]
- Struhl G., Adachi A. Nuclear access and action of notch in vivo. Cell. 1998 May 15;93(4):649–660. doi: 10.1016/s0092-8674(00)81193-9. [DOI] [PubMed] [Google Scholar]
- Weinmaster G. The ins and outs of notch signaling. Mol Cell Neurosci. 1997;9(2):91–102. doi: 10.1006/mcne.1997.0612. [DOI] [PubMed] [Google Scholar]
- Wettstein D. A., Turner D. L., Kintner C. The Xenopus homolog of Drosophila Suppressor of Hairless mediates Notch signaling during primary neurogenesis. Development. 1997 Feb;124(3):693–702. doi: 10.1242/dev.124.3.693. [DOI] [PubMed] [Google Scholar]
- de la Pompa J. L., Wakeham A., Correia K. M., Samper E., Brown S., Aguilera R. J., Nakano T., Honjo T., Mak T. W., Rossant J. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development. 1997 Mar;124(6):1139–1148. doi: 10.1242/dev.124.6.1139. [DOI] [PubMed] [Google Scholar]