Advertisement
JOURNAL ARTICLES
Synergistic principles of development: overlapping patterning systems in Xenopus mesoderm induction
D. Kimelman, J. L. Christian, R. T. Moon
Development 1992 116: 1-12;

Summary

The first inductive event in Xenopus development establishes the mesoderm at the equator of the developing embryo. As part of this process, the dorsal-ventral and anterior-posterior axes of the embryo are initially established. A number of signalling molecules which may play a role in mesodermal induction and patterning have been identified in the last several years, including members of the FGF, TGF-beta and Wnt gene families. A variety of experiments, using either purified factors or injection of RNA encoding these factors, have added to the wealth of classical embryogical experimental data collected over the last century. We have synthesized some recent results with the classical data to provide a framework for examining the process of mesoderm induction, and to formulate putative roles for some of the different factors. We incorporate these ideas into a working model of mesoderm induction that provides a basis for future experimental directions. Finally, we suggest that mesoderm induction may not be a discrete set of well separated events, but instead may be a process involving partially overlapping signals that produce the same pattern.

REFERENCES

    1. Albano R. M.,
    2. Godsave S. F.,
    3. Huylebroeck D.,
    4. Van Nimmen K.,
    5. Isaacs H. V.,
    6. Slack J. M. W.,
    7. Smith J. C.
    (1990) A mesoderm-inducing factor produced by WEHI-3 murine myelomonocytic leukemia cells is activin A. Development 110, 435–443
    OpenUrlAbstract/FREE Full Text
    1. Amaya E.,
    2. Musci T. J.,
    3. Kirschner M. W.
    (1991) Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66, 257–270
    OpenUrlCrossRefPubMedWeb of Science
    1. Asashima M.,
    2. Nakano H.,
    3. Ucimaya H.,
    4. Sugino H.,
    5. Nakamura T.,
    6. Eto Y.,
    7. Ejima D.,
    8. Nisimatsu S.,
    9. Ueno N.,
    10. Kinoshita K.
    (1991) Presence of activin (erythroid differentiation factor) in unfertilized eggs and blastulae of Xenopus laevis. Proc. Natl. Acad. Sci. USA 88, 6511–6514
    OpenUrlAbstract/FREE Full Text
    1. Chisaka O.,
    2. Capecchi M. R.
    (1991). Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene hox-1.5. Nature 350, 473–479
    OpenUrlCrossRefPubMed
    1. Cho K. W. Y.,
    2. De Robertis E. M.
    (1990) Differential activation of Xenopus homeobox genes by mesoderm-inducing growth factors and retinoic acid. Genes Dev 4, 1910–1916
    OpenUrlAbstract/FREE Full Text
    1. Christian J. L.,
    2. Gavin B. J.,
    3. McMahon A. P.,
    4. Moon R. T.
    (1991) Isolation of cDNAs partially encoding four XenopusWnt −1/ int −1-related proteins and characterization of their transient expression during embryonic development. Dev. Biol 143, 230–234
    OpenUrlCrossRefPubMedWeb of Science
    1. Christian J. L.,
    2. McMahon J. A.,
    3. McMahon A. P.,
    4. Moon R. T.
    (1991) Xwnt −8, a XenopusWnt −1/ int −1-related gene responsive to mesoderm inducing factors, may play a role in ventral mesodermal patterning during embryogenesis. Development 111, 1045–1056
    OpenUrlAbstract/FREE Full Text
    1. Christian J. L.,
    2. Olson D. J.,
    3. Moon R. T.
    (1992) Xwnt −8 modifies the character of mesoderm induced by bFGF in isolated Xenopus ectoderm. EMBO J 11, 33–41
    OpenUrlPubMedWeb of Science
    1. Cooke J.
    (1989) Mesoderm inducing factors and Spemann's organiser phenomenon in amphibian development. Development 107, 229–241
    OpenUrlAbstract
    1. Dale L.,
    2. Slack J. M.
    (1987) Fate map for the 32-cell stage of Xenopus laevis. Development 99, 527–551
    OpenUrlAbstract/FREE Full Text
    1. Dale L.,
    2. Slack J. M. W.
    (1987) Regional specification within the mesoderm of early embryos of Xenopus laevis. Development 100, 279–295
    OpenUrlAbstract/FREE Full Text
    1. Dale L.,
    2. Smith J. C.,
    3. Slack J. M.
    (1985) Mesoderm induction in Xenopus laevis: a quantitative study using a cell lineage label and tissue-specific antibodies. J. Embryol. exp. Morph 89, 289–312
    OpenUrlPubMedWeb of Science
    1. Friesel R.,
    2. Dawid I. B.
    (1991) cDNA cloning and developmental expression of fibroblast growth factor receptors from Xenopus laevis. Mol. Cell. Biol 11, 2481–2488
    OpenUrlAbstract/FREE Full Text
    1. Gallagher B. C.,
    2. Hainski A. M.,
    3. Moody S. A.
    (1991) Autonomous differentiation of dorsal axial structures from an animal cap cleavage stage blastomere in Xenopus. Development 112, 1103–1114
    OpenUrlAbstract
    1. Gillespie L. L.,
    2. Paterno G. D.,
    3. Slack J. M.
    (1989) Analysis of competence: receptors for fibroblast growth factor in early Xenopus embryos. Development 106, 203–208
    OpenUrlAbstract
    1. Gimlich R. L.
    (1986) Acquisition of developmental autonomy in the equatorial region of the Xenopus embryo. Dev. Biol 115, 340–352
    OpenUrlCrossRefPubMedWeb of Science
    1. Grant P.,
    2. Wacaster J. F.
    (1972) The amphibian gray crescent region- a site of developmental information?. Dev. Biol 28, 454–471
    OpenUrlCrossRefPubMedWeb of Science
    1. Green J. B. A.,
    2. Howes G.,
    3. Symes K.,
    4. Cooke J.,
    5. Smith J. C.
    (1990) The biological effects of XTC-MIF: quantitative comparison with Xenopus bFGF. Development 108, 173–183
    OpenUrlAbstract
    1. Isaacs H. V.,
    2. Tannahill D.,
    3. Slack J. M. W.
    (1992) Expression of a novel FGF in the Xenopus embryo. A new candidate inducing factor for mesoderm formation and anteroposterior specification. Development 114, 711–720
    OpenUrlAbstract
    1. Joyner A. L.,
    2. Herrup K.,
    3. Auerbach B. A.,
    4. Davis C. A.,
    5. Rossant J.
    (1991) Subtle cerebellar phenotype in mice homozygous for a targeted deletion of the En-2 homeobox. Science 251, 1239–1243
    OpenUrlAbstract/FREE Full Text
    1. Kageura H.
    (1990) Spatial distribution of the capacity to initiate a secondary embryo in the 32-cell embryo of Xenopus laevis. Dev. Biol 142, 432–438
    OpenUrlCrossRefPubMedWeb of Science
    1. Kageura H.,
    2. Yamana K.
    (1984) Pattern regulation in defect embryos of Xenopus laevis. Dev. Biol 101, 410–415
    OpenUrlCrossRefPubMedWeb of Science
    1. Kageura H.,
    2. Yamana K.
    (1986) Pattern formation in 8-cell composite embryos of Xenopus laevis. J. Embryol. exp. Morphol 91, 79–100
    OpenUrlPubMed
    1. Kaneda T.
    (1981) Studies of the formation and state of determination of the trunk organizer in the newt, Cynops pyrrhogaster, III. Tangential induction in the dorsal marginal zone. Dev. Growth and Differ 23, 553–564
    OpenUrlCrossRef
    1. Kao K.,
    2. Elinson R. P.
    (1989) Dorsalization of mesoderm induction by lithium. Dev. Biol 132, 81–90
    OpenUrlCrossRefPubMedWeb of Science
    1. Kao K. R.,
    2. Elinson R. P.
    (1988) The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol 127, 64–77
    OpenUrlCrossRefPubMedWeb of Science
    1. Kao K. R.,
    2. Masui Y.,
    3. Elinson R. P.
    (1986) Lithium induced respecification of pattern in Xenopus laevis embryos. Nature 322, 371–373
    OpenUrlCrossRefPubMedWeb of Science
    1. Keller R.,
    2. Tibbetts P.
    (1989) Mediolateral cell intercalation in the dorsal, axial mesoderm of Xenopus laevis. Dev. Biol 131, 539–549
    OpenUrlPubMedWeb of Science
    1. Keller R. E.
    (1976) Vital dye mapping of the gastrula and neurula of Xenopus laevis. Dev. Biol 51, 118–137
    OpenUrlCrossRefPubMedWeb of Science
    1. Kimelman D.,
    2. Abraham J. A.,
    3. Haaparanta T.,
    4. Palisi T. M.,
    5. Kirschner M. W.
    (1988) The presence of fibroblast growth factor in the frog egg: its role as a natural mesoderm inducer. Science 242, 1053–1056
    OpenUrlAbstract/FREE Full Text
    1. Kimelman D.,
    2. Kirschner M.
    (1987) Synergistic induction of mesoderm by FGF and TGF-and the indentification of an mRNA coding for FGF in the early Xenopus embryo. Cell 51, 869–877
    OpenUrlCrossRefPubMedWeb of Science
    1. Kimelman D.,
    2. Maas A.
    (1992) Induction of dorsal and ventral mesoderm by ectopically expressed Xenopus basic fibroblast growth factor. Development 114, 261–269
    OpenUrlAbstract
    1. Kintner C. R.,
    2. Dodd J.
    (1991) Hensen's node induces neural tissue in Xenopus ectoderm. Implications for the action of the organizer in neural induction. Development 113, 1495–1505
    OpenUrlAbstract
    1. Kondo M.,
    2. Tashiro K.,
    3. Fujii G.,
    4. Asano M.,
    5. Miyoshi R.,
    6. Yamada R.,
    7. Muramatsu M.,
    8. Shiokawa K.
    (1991) Activin receptor mRNA is expressed early in Xenopus embryogenesis and the level of expression affects the body axis formation. Biochem. Biophys. Res. Commun 181, 684–690
    OpenUrlCrossRefPubMedWeb of Science
    1. Koster M.,
    2. Plessow S.,
    3. Clement J. H.,
    4. Lorenz A.,
    5. Tiedemann H.,
    6. Knochel W.
    (1991) Bone morphogenetic protein 4 (BMP-4), a member of the TGF- family in early embryos of Xenopus laevis: analysis of mesoderm inducing activity. Mech. Dev 33, 191–200
    OpenUrlCrossRefPubMedWeb of Science
    1. Lufkin T.,
    2. Dierich A.,
    3. LeMeur M.,
    4. Mark M.,
    5. Chambon P.
    (1991). Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression. Cell 66, 1105–1119
    OpenUrlCrossRefPubMedWeb of Science
    1. Malacinski G. M.,
    2. Brothers J.,
    3. Chung H.-M.
    (1977) Destruction of components of the neural induction system of the amphibian egg with ultraviolet irradiation. Dev. Biol 56, 24–39
    OpenUrlCrossRefPubMedWeb of Science
    1. Matthews L. S.,
    2. Vale W. W.,
    3. Kintner C. R.
    (1992) Cloning of a second type of activin receptor and functional characterization in Xenopus embryos. Science 255, 1702–1705
    OpenUrlAbstract/FREE Full Text
    1. McMahon A. P.,
    2. Bradley A.
    (1990) The Wnt −1 (int −1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62, 1073–1085
    OpenUrlCrossRefPubMedWeb of Science
    1. McMahon A. P.,
    2. Moon R. T.
    (1989) Ectopic expression of the proto-oncogene int −1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 58, 1075–1084
    OpenUrlCrossRefPubMedWeb of Science
    1. Moody S. A.
    (1987) Fates of the blastomeres of the 16-cell stage Xenopus embryo. Dev. Biol 119, 560–578
    OpenUrlCrossRefPubMedWeb of Science
    1. Moody S. A.
    (1987) Fates of the blastomeres of the 32-cell-stage Xenopus embryo. Dev. Biol 122, 300–319
    OpenUrlCrossRefPubMedWeb of Science
    1. Musci T. J.,
    2. Amaya E.,
    3. Kirschner M. W.
    (1990) Regulation of the fibroblast growth factor receptor in early Xenopus embryos. Proc. Natl. Acad. Sci. USA 87, 8365–8369
    OpenUrlAbstract/FREE Full Text
    1. Nagajski D. J.,
    2. Guthrie S. C.,
    3. Ford C. C.,
    4. Warner A. E.
    (1989). The correlation between patterns of dye transfer through gap junctions and future developmental fate in Xenopus: the consequences of u.v. irradiation and lithium treatment. Development 105, 747–752
    OpenUrlAbstract/FREE Full Text
    1. Nieuwkoop P. D.
    (1973) The “organization center” of the amphibian embryo: its origin, spatial organization and morphogenetic action. Advances in Morphogenesis 10, 1–39
    OpenUrlPubMed
    1. Noordermeer J.,
    2. Meijlink F.,
    3. Verrijzer P.,
    4. Rijsewijk F.,
    5. Destree O.
    (1989) Isolation of the Xenopus homolog of int −1/ wingless and expression during neurula stages of early development. Nucleic Acids Res 17, 11–18
    OpenUrlAbstract/FREE Full Text
    1. Olson D. J.,
    2. Christian J. L.,
    3. Moon R. T.
    (1991) Effect of wnt −1 and related proteins on gap junctional communication in Xenopus embryos. Science 252, 1173–1176
    OpenUrlFREE Full Text
    1. Pierce K. E.,
    2. Brothers J. A.
    (1988) Dorsal and ventral cells of cleavage stage embryos show the same ability to induce notochord and somite formation. Dev. Biol 126, 228–232
    OpenUrlCrossRefPubMed
    1. Roberts A. B.,
    2. Kondaiah P.,
    3. Rosa F.,
    4. Watanabe S.,
    5. Good P.,
    6. Roche N. S.,
    7. Rebbert M. L.,
    8. Dawid I. B.,
    9. Sporn M. B.
    (1990) Mesoderm induction in Xenopuslaevis distinguishes between the various TGF- isoforms. Growth factors 3, 277–286
    OpenUrlCrossRefPubMed
    1. Ruiz i Altaba A.,
    2. Jessell T.
    (1991) Retinoic acid modifies mesodermal patterning in early Xenopus embryos. Genes Dev 5, 175–87
    OpenUrlAbstract/FREE Full Text
    1. Ruiz i Altaba A.,
    2. Melton D. A.
    (1989) Interaction between peptide growth factors and homeobox genes in the establishment of antero-posterior polarity in frog embryos. Nature 341, 33–38
    OpenUrlCrossRefPubMed
    1. Scharf S. R.,
    2. Gerhart J. C.
    (1980) Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of uv-impaired eggs by oblique orientation before first cleavage. Dev. Biol 79, 181–198
    OpenUrlCrossRefPubMedWeb of Science
    1. Scharf S. R.,
    2. Gerhart J. C.
    (1983) Axis determination in eggs of Xenopus laevis: a critical period before first cleavage, indentified by the common effects of cold, pressure, and ultraviolet irradiation. Dev. Biol 99, 75–87
    OpenUrlCrossRefPubMedWeb of Science
    1. Shiurba R. A.,
    2. Jing N.,
    3. Sakakura T.,
    4. Godsave S. F.
    (1991) Nuclear translocation of fibroblast growth factor during Xenopus mesoderm induction. Development 113, 487–493
    OpenUrlAbstract
    1. Slack J. M.,
    2. Dale L.,
    3. Smith J. C.
    (1984) Analysis of embryonic induction by using cell lineage markers. Philos. Trans. R. Soc. Lond 307, 331–336
    OpenUrlAbstract/FREE Full Text
    1. Slack J. M.,
    2. Isaacs H. V.,
    3. Darlington B. G.
    (1988) Inductive effects of fibroblast growth factor and lithium ion on blastula ectoderm. Development 103, 581–590
    OpenUrlAbstract
    1. Slack J. M. W.,
    2. Darlington B. G.,
    3. Heath J. K.,
    4. Godsave S. F.
    (1987) Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. Nature 326, 197–200
    OpenUrlCrossRefPubMed
    1. Slack J. M. W.,
    2. Forman D.
    (1980) An interaction between dorsal and ventral regions of the marginal zone in early amphibian embryos. J. Embryol. exp. Morph 56, 283–299
    OpenUrlPubMedWeb of Science
    1. Slack J. M. W.,
    2. Isaacs H. V.
    (1989) Presence of basic fibroblast growth factor in the early Xenopus embryo. Development 105, 147–153
    OpenUrlAbstract
    1. Slack J. M. W.,
    2. Tannahill D.
    (1992) Mechanism of anteroposterior axis specification in vertebrates: lessons from the amphibians. Development 114, 285–302
    OpenUrlAbstract
    1. Smith J. C.
    (1987) A mesoderm-inducing factor is produced by a Xenopus cell line. Development 99, 3–14
    OpenUrlAbstract/FREE Full Text
    1. Smith J. C.,
    2. Dale L.,
    3. Slack J. M. W.
    (1985) Cell lineage of labels and region-specific markers in the analysis of inductive interactions. J. Embryol. exp. Morph 89, 317–331
    1. Smith J. C.,
    2. Price B. M. J.,
    3. Van Nimmen K.,
    4. Huylebroeck D.
    (1990) Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature 345, 729–731
    OpenUrlCrossRefPubMed
    1. Smith J. C.,
    2. Slack J. M.
    (1983) Dorsalization and neural induction: properties of the organizer in Xenopus laevis. J. Embryol. exp. Morph 78, 299–317
    OpenUrlPubMedWeb of Science
    1. Smith W. C.,
    2. Harland R. M.
    (1991) Injected Xwnt −8 acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67, 753–766
    OpenUrlCrossRefPubMedWeb of Science
    1. Sokol S.,
    2. Christian J. L.,
    3. Moon R. T.,
    4. Melton D. A.
    (1991) Injected wnt RNA induces a complete body axis in Xenopus embryos. Cell 67, 741–752
    OpenUrlCrossRefPubMedWeb of Science
    1. Sokol S.,
    2. Melton D. A.
    (1991) Pre-existent pattern in Xenopus animal pole cells revealed by induction with activin. Nature 351, 409–411
    OpenUrlCrossRefPubMedWeb of Science
    1. Sokol S.,
    2. Wong G.,
    3. Melton D. A.
    (1990) A mouse macrophage factor induces head structure and organizes a body axis in Xenopus. Science 249, 561–564
    OpenUrlAbstract/FREE Full Text
    1. Soriano P.,
    2. Montgomery C.,
    3. Geske R.,
    4. Bradley A.
    (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64, 693–702
    OpenUrlCrossRefPubMedWeb of Science
    1. Takasaki H.,
    2. Konishi H.
    (1989) Dorsal blastomeres in the equatorial region of the 32-cell Xenopus embryo autonomously produce progeny committed to the organizer. Develop. Growth and Differ 31, 147–156
    OpenUrlCrossRef
    1. Thomas K. R.,
    2. Capecchi M. R.
    (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346, 847–850
    OpenUrlCrossRefPubMedWeb of Science
    1. Thomsen G.,
    2. Woolf T.,
    3. Whitman M.,
    4. Sokol S.,
    5. Vaughan J.,
    6. Vale W.,
    7. Melton D. A.
    (1990) Activins are expressed in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 63, 485–493
    OpenUrlCrossRefPubMedWeb of Science
    1. van den Eijnden Van Raaij A. J.,
    2. van Zoelent E. J.,
    3. van Nimmen K.,
    4. Koster C. H.,
    5. Snoek G. T.,
    6. Durston A. J.,
    7. Huylebroeck D.
    (1990) Activin-like factor from a Xenopus laevis cell line responsible for mesoderm induction. Nature 345, 732–734
    OpenUrlCrossRefPubMed
    1. Vincent J. P.,
    2. Gerhart J. C.
    (1987) Subcortical rotation in Xenopus eggs: an early step in embryonic axis formation. Dev. Biol 123, 526–539
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilson P. A.,
    2. Oster G.,
    3. Keller R.
    (1989) Cell rearrangement and segmentation in Xenopus: direct observation of cultured explants. Development 105, 155–166
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Synergistic principles of development: overlapping patterning systems in Xenopus mesoderm induction
D. Kimelman, J. L. Christian, R. T. Moon
Development 1992 116: 1-12;
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

An interview with Swathi Arur

Swathi Arur joined the team at Development as an Academic Editor in 2020. Her lab uses multidisciplinary approaches to understand female germline development and fertility. We met with her over Zoom to hear more about her life, her career and her love for C. elegans.

Jim Wells and Hanna Mikkola join our team of Editors

We are pleased to welcome James (Jim) Wells and Hanna Mikkola to our team of Editors. Jim joins us a new Academic Editor, taking over from Gordan Keller, and Hanna joins our team of Associate Editors. Find out more about their research interests and areas of expertise.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

“I’d heard of Read & Publish deals and knew that many universities, including mine, had signed up to them but I had not previously understood the benefits that these deals bring to authors who work at those universities.”

Professor Sally Lowell (University of Edinburgh) shares her experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

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

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

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.