Abstract
The MyoD gene codes for an important regulatory factor in skeletal myogenesis. To explore the relationship between mesoderm induction in Xenopus embryos and expression of MyoD, I have monitored MyoD mRNA levels in normal embryos and cultured explants by RNase protection. Transcription from the two Xenopus MyoD gene copies is activated weakly across the whole embryo at the midblastula transition, and this activation occurs in the absence of mesoderm induction. In response to induction this basal expression is amplified 50- to 100-fold, but in animal-pole explants 6-10 hr elapse before induced mRNAs appear, and this induction requires prior protein synthesis. The promiscuous transcripts disappear from animal explants at a time when induction "competence" is lost, suggesting a link between these events. The data highlight a broad, but transient, permissiveness for MyoD expression in embryos, which is propagated and amplified only in presumptive muscle in response to induction. Moreover, muscle-specific MyoD expression is a relatively late (postgastrulation) event in the mesoderm-induction cascade.
Full text
PDF




Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Benezra R., Davis R. L., Lockshon D., Turner D. L., Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990 Apr 6;61(1):49–59. doi: 10.1016/0092-8674(90)90214-y. [DOI] [PubMed] [Google Scholar]
- Braun T., Buschhausen-Denker G., Bober E., Tannich E., Arnold H. H. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J. 1989 Mar;8(3):701–709. doi: 10.1002/j.1460-2075.1989.tb03429.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Campos-Ortega J. A., Knust E. Molecular analysis of a cellular decision during embryonic development of Drosophila melanogaster: epidermogenesis or neurogenesis. Eur J Biochem. 1990 May 31;190(1):1–10. doi: 10.1111/j.1432-1033.1990.tb15538.x. [DOI] [PubMed] [Google Scholar]
- Crescenzi M., Fleming T. P., Lassar A. B., Weintraub H., Aaronson S. A. MyoD induces growth arrest independent of differentiation in normal and transformed cells. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8442–8446. doi: 10.1073/pnas.87.21.8442. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davis R. L., Weintraub H., Lassar A. B. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 1987 Dec 24;51(6):987–1000. doi: 10.1016/0092-8674(87)90585-x. [DOI] [PubMed] [Google Scholar]
- Dworkin-Rastl E., Kelley D. B., Dworkin M. B. Localization of specific mRNA sequences in Xenopus laevis embryos by in situ hybridization. J Embryol Exp Morphol. 1986 Feb;91:153–168. [PubMed] [Google Scholar]
- Fritz A. F., Cho K. W., Wright C. V., Jegalian B. G., De Robertis E. M. Duplicated homeobox genes in Xenopus. Dev Biol. 1989 Feb;131(2):584–588. doi: 10.1016/s0012-1606(89)80029-6. [DOI] [PubMed] [Google Scholar]
- Gurdon J. B. Methods for nuclear transplantation in amphibia. Methods Cell Biol. 1977;16:125–139. doi: 10.1016/s0091-679x(08)60096-5. [DOI] [PubMed] [Google Scholar]
- Harvey R. P. The Xenopus MyoD gene: an unlocalised maternal mRNA predates lineage-restricted expression in the early embryo. Development. 1990 Apr;108(4):669–680. doi: 10.1242/dev.108.4.669. [DOI] [PubMed] [Google Scholar]
- Heasman J., Snape A., Smith J. C., Wylie C. C. The nature of developmental restrictions in Xenopus laevis embryos. J Embryol Exp Morphol. 1986 Oct;97 (Suppl):65–73. [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]
- Krieg P. A., Melton D. A. Developmental regulation of a gastrula-specific gene injected into fertilized Xenopus eggs. EMBO J. 1985 Dec 16;4(13A):3463–3471. doi: 10.1002/j.1460-2075.1985.tb04105.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krieg P. A., Melton D. A. In vitro RNA synthesis with SP6 RNA polymerase. Methods Enzymol. 1987;155:397–415. doi: 10.1016/0076-6879(87)55027-3. [DOI] [PubMed] [Google Scholar]
- Lassar A. B., Buskin J. N., Lockshon D., Davis R. L., Apone S., Hauschka S. D., Weintraub H. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell. 1989 Sep 8;58(5):823–831. doi: 10.1016/0092-8674(89)90935-5. [DOI] [PubMed] [Google Scholar]
- Lin Z. Y., Dechesne C. A., Eldridge J., Paterson B. M. An avian muscle factor related to MyoD1 activates muscle-specific promoters in nonmuscle cells of different germ-layer origin and in BrdU-treated myoblasts. Genes Dev. 1989 Jul;3(7):986–996. doi: 10.1101/gad.3.7.986. [DOI] [PubMed] [Google Scholar]
- Mueller P. R., Wold B. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science. 1989 Nov 10;246(4931):780–786. doi: 10.1126/science.2814500. [DOI] [PubMed] [Google Scholar]
- Murre C., McCaw P. S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell. 1989 Mar 10;56(5):777–783. doi: 10.1016/0092-8674(89)90682-x. [DOI] [PubMed] [Google Scholar]
- Murre C., McCaw P. S., Vaessin H., Caudy M., Jan L. Y., Jan Y. N., Cabrera C. V., Buskin J. N., Hauschka S. D., Lassar A. B. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell. 1989 Aug 11;58(3):537–544. doi: 10.1016/0092-8674(89)90434-0. [DOI] [PubMed] [Google Scholar]
- Nieuwkoop P. D. The organization center of the amphibian embryo: its origin, spatial organization, and morphogenetic action. Adv Morphog. 1973;10:1–39. doi: 10.1016/b978-0-12-028610-2.50005-8. [DOI] [PubMed] [Google Scholar]
- Olsen D. B., Eckstein F. High-efficiency oligonucleotide-directed plasmid mutagenesis. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1451–1455. doi: 10.1073/pnas.87.4.1451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pinney D. F., Pearson-White S. H., Konieczny S. F., Latham K. E., Emerson C. P., Jr Myogenic lineage determination and differentiation: evidence for a regulatory gene pathway. Cell. 1988 Jun 3;53(5):781–793. doi: 10.1016/0092-8674(88)90095-5. [DOI] [PubMed] [Google Scholar]
- Rhodes S. J., Konieczny S. F. Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev. 1989 Dec;3(12B):2050–2061. doi: 10.1101/gad.3.12b.2050. [DOI] [PubMed] [Google Scholar]
- Rosa F. M. Mix.1, a homeobox mRNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos. Cell. 1989 Jun 16;57(6):965–974. doi: 10.1016/0092-8674(89)90335-8. [DOI] [PubMed] [Google Scholar]
- Rupp R. A., Weintraub H. Ubiquitous MyoD transcription at the midblastula transition precedes induction-dependent MyoD expression in presumptive mesoderm of X. laevis. Cell. 1991 Jun 14;65(6):927–937. doi: 10.1016/0092-8674(91)90545-a. [DOI] [PubMed] [Google Scholar]
- Scales J. B., Olson E. N., Perry M. Two distinct Xenopus genes with homology to MyoD1 are expressed before somite formation in early embryogenesis. Mol Cell Biol. 1990 Apr;10(4):1516–1524. doi: 10.1128/mcb.10.4.1516. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slack J. M., Darlington B. G., Heath J. K., Godsave S. F. Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. Nature. 1987 Mar 12;326(6109):197–200. doi: 10.1038/326197a0. [DOI] [PubMed] [Google Scholar]
- Smith J. C., Price B. M., Van Nimmen K., Huylebroeck D. Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature. 1990 Jun 21;345(6277):729–731. doi: 10.1038/345729a0. [DOI] [PubMed] [Google Scholar]
- Sorrentino V., Pepperkok R., Davis R. L., Ansorge W., Philipson L. Cell proliferation inhibited by MyoD1 independently of myogenic differentiation. Nature. 1990 Jun 28;345(6278):813–815. doi: 10.1038/345813a0. [DOI] [PubMed] [Google Scholar]
- Tapscott S. J., Davis R. L., Thayer M. J., Cheng P. F., Weintraub H., Lassar A. B. MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science. 1988 Oct 21;242(4877):405–411. doi: 10.1126/science.3175662. [DOI] [PubMed] [Google Scholar]
- Taylor S. M., Jones P. A. Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell. 1979 Aug;17(4):771–779. doi: 10.1016/0092-8674(79)90317-9. [DOI] [PubMed] [Google Scholar]
- Thomsen G., Woolf T., Whitman M., Sokol S., Vaughan J., Vale W., Melton D. A. Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell. 1990 Nov 2;63(3):485–493. doi: 10.1016/0092-8674(90)90445-k. [DOI] [PubMed] [Google Scholar]
- Vriz S., Taylor M., Méchali M. Differential expression of two Xenopus c-myc proto-oncogenes during development. EMBO J. 1989 Dec 20;8(13):4091–4097. doi: 10.1002/j.1460-2075.1989.tb08593.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weintraub H., Davis R., Lockshon D., Lassar A. MyoD binds cooperatively to two sites in a target enhancer sequence: occupancy of two sites is required for activation. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5623–5627. doi: 10.1073/pnas.87.15.5623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weintraub H., Davis R., Tapscott S., Thayer M., Krause M., Benezra R., Blackwell T. K., Turner D., Rupp R., Hollenberg S. The myoD gene family: nodal point during specification of the muscle cell lineage. Science. 1991 Feb 15;251(4995):761–766. doi: 10.1126/science.1846704. [DOI] [PubMed] [Google Scholar]
- Weintraub H., Tapscott S. J., Davis R. L., Thayer M. J., Adam M. A., Lassar A. B., Miller A. D. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5434–5438. doi: 10.1073/pnas.86.14.5434. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wright W. E., Sassoon D. A., Lin V. K. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell. 1989 Feb 24;56(4):607–617. doi: 10.1016/0092-8674(89)90583-7. [DOI] [PubMed] [Google Scholar]