Advertisement
JOURNAL ARTICLES
Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo
A. Streit, K.J. Lee, I. Woo, C. Roberts, T.M. Jessell, C.D. Stern
Development 1998 125: 507-519;

Summary

We have investigated the role of Bone Morphogenetic Protein 4 (BMP-4) and a BMP antagonist, chordin, in primitive streak formation and neural induction in amniote embryos. We show that both BMP-4 and chordin are expressed before primitive streak formation, and that BMP-4 expression is downregulated as the streak starts to form. When BMP-4 is misexpressed in the posterior area pellucida, primitive streak formation is inhibited. Misexpression of BMP-4 also arrests further development of Hensen's node and axial structures. In contrast, misexpression of chordin in the anterior area pellucida generates an ectopic primitive streak that expresses mesoderm and organizer markers. We also provide evidence that chordin is not sufficient to induce neural tissue in the chick. Misexpression of chordin in regions outside the future neural plate does not induce the early neural markers L5, Sox-3 or Sox-2. Furthermore, neither BMP-4 nor BMP-7 interfere with neural induction when misexpressed in the presumptive neural plate before or after primitive streak formation. However, chordin can stabilise the expression of early neural markers in cells that have already received neural inducing signals. These results suggest that the regulation of BMP signalling by chordin plays a role in primitive streak formation and that chordin is not sufficient to induce neural tissue.

REFERENCES

    1. Bally-Cuif L.,
    2. Gulisano M.,
    3. Broccoli V.,
    4. Boncinelli E.
    (1995) c-otx2 is expressed in two different phases of gastrulation and is sensitive to retinoic acid treatment in chick embryo. Mech. Dev 49, 49–63
    OpenUrlCrossRefPubMedWeb of Science
    1. Biehs B.,
    2. François V.,
    3. Bier E.
    (1996) The Drosophila short gastrulation gene prevents dpp from autoactivating and suppressing neurogenesis in the neuroectoderm. Genes Dev 10, 2922–2934
    OpenUrlAbstract/FREE Full Text
    1. Callebaut M.,
    2. Van Nueten E.
    (1994) Rauber's (Koller's) sickle: the early gastrulation organizer of the avian blastoderm. Eur. J. Morphol 32, 35–48
    OpenUrlPubMed
    1. Collignon J.,
    2. Sockanathan S.,
    3. Hacker A.,
    4. Cohen-Tannoudji M.,
    5. Norris D.,
    6. Rastan S.,
    7. Stevanovic M.,
    8. Goodfellow P. N.,
    9. Lovell-Badge R.
    (1996) A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. Development 122, 506–520
    OpenUrl
    1. Connolly D. J.,
    2. Patel K.,
    3. Cooke J.
    (1997) Chick noggin is expressed in the organizer and neural plate during axial development, but offers no evidence of involvement in primary axis formation. Int. J. Dev. Biol 41, 389–396
    OpenUrlPubMedWeb of Science
    1. Connolly D. J.,
    2. Patel K.,
    3. Seleiro E. A.,
    4. Wilkinson D. G.,
    5. Cooke J.
    (1995) Cloning, sequencing and expressional analysis of the chick homologue of follistatin. Dev. Genetics 17, 65–77
    OpenUrlCrossRefPubMedWeb of Science
    1. Cooke J.,
    2. Takada S.,
    3. McMahon A.
    (1994) Experimental contol of axial pattern in the chick blastoderm by local expression of Wnt and activin: the role of HNK-1 positive cells. Dev. Biol 164, 513–527
    OpenUrlCrossRefPubMed
    1. Dale L.,
    2. Howes G.,
    3. Price B. M.,
    4. Smith J. C.
    (1992) Bone morphogenetic protein 4: A ventralizing factor in early Xenopus development. Development 115, 573–585
    OpenUrlAbstract
    1. De Robertis E. M.,
    2. Sasai Y.
    (1996) A common plan for dorsoventral patterning in Bilateria. Nature 380, 37–40
    OpenUrlCrossRefPubMed
    1. Eyal-Giladi H.,
    2. Khaner O.
    (1989) The chick's marginal zone and primitive streak formation. II. Quantification of the marginal zone's potencies—temporal and spatial aspects. Dev. Biol 134, 215–221
    OpenUrlCrossRefPubMed
    1. Eyal-Giladi H.,
    2. Kochav S.
    (1976) From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick. Dev. Biol 49, 321–337
    OpenUrlCrossRefPubMedWeb of Science
    1. Fainsod A.,
    2. Deissler K.,
    3. Yelin R.,
    4. Marom K.,
    5. Epstein M.,
    6. Pillemer G.,
    7. Steinbeisser H.,
    8. Blum M.
    (1997) The dorsalizing and neural inducing gene follistatin is an antagonist of BMP-4. Mech. Dev 63, 39–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Fainsod A.,
    2. Steinbeisser H.,
    3. De Robertis E. M.
    (1994) On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J 13, 5015–5025
    OpenUrlPubMedWeb of Science
    1. Ferguson E. L.
    (1996) Conservation of dorsal-ventral patterning in arthropods and chordates. Curr. Opin. Genet. Dev 6, 424–431
    OpenUrlCrossRefPubMedWeb of Science
    1. Foley A. C.,
    2. Storey K. G.,
    3. Stern C. D.
    (1997) The prechordal plate region lacks neural inducing activity, but can confer anterior character to more posterior neuroepithelium. Development 124, 2983–2996
    OpenUrlAbstract
    1. François V.,
    2. Soloway M.,
    3. O'Neill J. W.,
    4. Emery J.,
    5. Bier E.
    (1994) Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev 8, 2602–2616
    OpenUrlAbstract/FREE Full Text
    1. George-Weinstein M.,
    2. Gerhart J.,
    3. Reed R.,
    4. Flynn J.,
    5. Callihan B.,
    6. Battiacci M.,
    7. Miehle C.,
    8. Foti G.,
    9. Lash J. W.,
    10. Weintraub H.
    (1996) Skeletal myogenesis: the preferred pathway of chick embryo epiblast cells in vitro. Dev. Biol 173, 279–291
    OpenUrlCrossRefPubMedWeb of Science
    1. Hamburger V.,
    2. Hamilton H. L.
    (1951) A series of normal stages in the development of the chick embryo. J. Morph 88, 49–92
    OpenUrlCrossRefPubMedWeb of Science
    1. Hammerschmidt M.,
    2. Serbedzija G. N.,
    3. McMahon A. P.
    (1996) Genetic analysis of dorsoventral pattern formation in the zebrafish: requirement of a BMP-like ventralizing activity and its dorsal repressor. Genes Dev 10, 2452–2461
    OpenUrlAbstract/FREE Full Text
    1. Hatada Y.,
    2. Stern C. D.
    (1994) A fate map of the epiblast of the early chick embryo. Development 120, 2879–2890
    OpenUrlAbstract
    1. Hawley S. H. B.,
    2. Wunnenberg-Stapleton K.,
    3. Hashimoto C.,
    4. Laurent M. N.,
    5. Watabe T.,
    6. Blumberg B. W.,
    7. Cho K. W. Y.
    (1995) Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev 9, 2923–2935
    OpenUrlAbstract/FREE Full Text
    1. Hemmati-Brivanlou A.,
    2. Thomsen G. H.
    (1995) Ventral mesodermal patterning in Xenopus embryos: expression patterns and activities of BMP-2 and BMP-4. Dev. Genet 17, 78–89
    OpenUrlCrossRefPubMedWeb of Science
    1. Hemmati-Brivanlou A.,
    2. Kelly O. G.,
    3. Melton D. A.
    (1994) Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77, 238–295
    OpenUrl
    1. Holley S. A.,
    2. Ferguson E. L.
    (1997) Fish are like flies are like frogs but different from chickens: conservation of dorsal-ventral patterning mechanisms. BioEssays 19, 281–284
    OpenUrlCrossRefPubMedWeb of Science
    1. Holley S. A.,
    2. Jackson P. D.,
    3. Sasai Y.,
    4. Lu B.,
    5. De Robertis E. M.,
    6. Hoffmann F. M.,
    7. Ferguson E. L.
    (1995) A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249–253
    OpenUrlCrossRefPubMed
    1. Holley S. A.,
    2. Neul J. L.,
    3. Attisano L.,
    4. Wrana J. L.,
    5. Sasai Y.,
    6. O'Connor M. B.,
    7. De Robertis E. M.,
    8. Ferguson E. L.
    (1996) The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor. Cell 86, 607–617
    OpenUrlCrossRefPubMedWeb of Science
    1. Izpisúa-Belmonte J. C.,
    2. De Robertis E. M.,
    3. Storey K. G.,
    4. Stern C. D.
    (1993) The homeobox gene goosecoid and the origin of the organizer cells in the early chick blastoderm. Cell 74, 645–659
    OpenUrlCrossRefPubMedWeb of Science
    1. Jones C. M.,
    2. Dale L.,
    3. Hogan B. L.,
    4. Wright C. V.,
    5. Smith J. C.
    (1996) Bone morphogenetic protein-4 (BMP-4) acts during gastrula stages to cause ventralization of Xenopus embryos. Development 122, 1545–1554
    OpenUrlAbstract
    1. Jones C. M.,
    2. Lyons K. M.,
    3. Lapan P. M.,
    4. Wright C. V.,
    5. Hogan B. L.
    (1992) DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction. Development 115, 639–647
    OpenUrlAbstract
    1. Khaner O.,
    2. Eyal-Giladi H.
    (1989) The chick's marginal zone and primitive streak formation. I. Coordinative effect of induction and inhibition. Dev. Biol 134, 206–214
    OpenUrlCrossRefPubMed
    1. Kishimoto Y.,
    2. Lee K.,
    3. Zon L.,
    4. Hammerschmidt M.,
    5. Schulte-Merker S.
    (1997) The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development 124, 4457–4466
    OpenUrlAbstract
    1. Knecht A. K.,
    2. Harland R. M.
    (1997) Mechanisms of dorsal-ventral patterning in noggin-induced neural tissue. Development 124, 2477–2488
    OpenUrlAbstract
    1. Lamb T. M.,
    2. Knecht A. K.,
    3. Smith W. C.,
    4. Stachel S. E.,
    5. Economides A. N.,
    6. Stahl N.,
    7. Yancopoulos G. D.,
    8. Harland R. M.
    (1993) Neural induction by the secreted polypeptide noggin. Science 262, 713–718
    OpenUrlAbstract/FREE Full Text
    1. Liem K. F.,
    2. Tremml G.,
    3. Roelink H.,
    4. Jessell T. M.
    (1995) Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969–979
    OpenUrlCrossRefPubMedWeb of Science
    1. Lumsden A.,
    2. Krumlauf R.
    (1996) Patterning the vertebrate neuraxis. Science 274, 1109–1114
    OpenUrlAbstract/FREE Full Text
    1. Mitrani E.,
    2. Ziv T.,
    3. Thomsen G.,
    4. Shimoni Y.,
    5. Melton D. A.,
    6. Bril A.
    (1990) Activin can induce the formation of axial structures and is expressed in the hypoblast of the chick. Cell 63, 495–501
    OpenUrlCrossRefPubMedWeb of Science
    1. New D. A. T.
    (1955) A new technique for the cultivation of the chick embryo in vitro. J. Embryol. Exp. Morph 3, 326–331
    OpenUrl
    1. Pannett C. A.,
    2. Compton A.
    (1924) The cultivation of tissues in saline embryonic juice. Lancet 206, 381–384
    OpenUrl
    1. Piccolo S.,
    2. Sasai Y.,
    3. Lu B.,
    4. De Robertis E. M.
    (1996) Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589–598
    OpenUrlCrossRefPubMedWeb of Science
    1. Re'em-Kalma Y.,
    2. Lamb T.,
    3. Frank D.
    (1995) Competition between noggin and bone morphogenetic protein 4 activities may regulate dorsalization during Xenopus development. Proc. natn. Acad. Sci. USA 92, 12141–12145
    OpenUrlAbstract/FREE Full Text
    1. Ruiz i Altaba A.,
    2. Placzek M.,
    3. Baldassare M.,
    4. Dodd J.,
    5. Jessell T. M.
    (1995) Early stages of notochord and floor plate development in the chick embryo defined by normal and induced expression of HNF-3. Dev. Biol 170, 299–313
    OpenUrlCrossRefPubMedWeb of Science
    1. Sasai Y.,
    2. De Robertis E. M.
    (1997) Ectodermal patterning in vertebrate embryos. Dev. Biol 182, 5–20
    OpenUrlCrossRefPubMedWeb of Science
    1. Sasai Y.,
    2. Lu B.,
    3. Steinbeisser H.,
    4. De Robertis E. M.
    (1995) Regulation of neural induction by the Chd and BMP-4 antagonistic patterning signals in Xenopus. Nature 376, 333–336
    OpenUrlCrossRefPubMed
    1. Sasai Y.,
    2. Lu B.,
    3. Steinbeisser H.,
    4. Geissert D.,
    5. Gont L. K.,
    6. De Robertis E. M.
    (1994) Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79, 779–790
    OpenUrlCrossRefPubMedWeb of Science
    1. Schmidt J. E.,
    2. Suzuki A.,
    3. Ueno N.,
    4. Kimelman D.
    (1995) Localized BMP-4 mediates dorso/ventral patterning in the early Xenopus embryo. Dev. Biol 169, 37–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Schmidt J. E.,
    2. Von Dassow G.,
    3. Kimelman D.
    (1996) Regulation of dorsal-ventral patterning: the ventralizing effects of the novel Xenopus homeobox gene vox. Development 122, 1711–1721
    OpenUrlAbstract
    1. Schulte-Merker S.,
    2. Lee K. J.,
    3. McMahon A. P.,
    4. Hammerschmidt M.
    (1997) The zebrafish organizer requires chordino. Nature 387, 862–863
    OpenUrlCrossRefPubMed
    1. Schultheiss T. M.,
    2. Burch J. B.,
    3. Lassar A. B.
    (1997) A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev 11, 451–462
    OpenUrlAbstract/FREE Full Text
    1. Seleiro E. A.,
    2. Connolly D. J.,
    3. Cooke J.
    (1996) Early developmentalexpression and experimental axis determination by the chicken Vg1 gene. Curr. Biol 6, 1476–1486
    OpenUrlCrossRefPubMed
    1. Shah S. B.,
    2. Skromne I.,
    3. Hume C. R.,
    4. Kessler D. S.,
    5. Lee K. J.,
    6. Stern C. D.,
    7. Dodd J.
    (1997) Chick Vg1 reveals multiple steps in primitive streak formation. Development 124, 5127–5138
    OpenUrlAbstract
    1. Smith W. C.,
    2. Knecht A. K.,
    3. Wu M.,
    4. Harland R. M.
    (1993) Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm. Nature 361, 547–549
    OpenUrlCrossRefPubMed
    1. Smith W. C.,
    2. Harland R. M.
    (1992) Expression cloning of noggin a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829–840
    OpenUrlCrossRefPubMedWeb of Science
    1. Steinbeisser H.,
    2. Fainsod A.,
    3. Niehrs C.,
    4. Sasai Y.,
    5. De Robertis E. M.
    (1995) The role of gsc and BMP-4 in dorsal-ventral patterning of the marginal zone in Xenopus: a loss of function study using antisense RNA. EMBO J 14, 5230–5243
    OpenUrlPubMedWeb of Science
    1. Stern C. D.
    (1990) The marginal zone and its contribution to the hypoblast and primitive streak of the chick embryo. Development 109, 667–682
    OpenUrlAbstract
    1. Stern C. D.,
    2. Ireland G. W.
    (1981) An integrated experimental study of endoderm formation in avian embryos. Anat. Embryol 163, 245–263
    OpenUrlCrossRefPubMed
    1. Storey K. G.,
    2. Crossley J. M.,
    3. De Robertis E. M.,
    4. Norris W. E.,
    5. Stern C. D.
    (1992) Neural induction and regionalisation in the chick embryo. Development 114, 729–741
    OpenUrlAbstract
    1. Streit A.,
    2. Sockanathan S.,
    3. Perez L.,
    4. Rex M.,
    5. Scotting P. J.,
    6. Sharpe P. T.,
    7. Lovell-Badge R.,
    8. Stern C. D.
    (1997) Preventing the loss of competence for neural induction: HGF/SF, L5 and Sox-2. Development 124, 1191–1202
    OpenUrlAbstract
    1. Streit A.,
    2. Stern C. D.,
    3. Thery C.,
    4. Ireland G. W.,
    5. Aparicio S.,
    6. Sharpe M.,
    7. Gherardi E.
    (1995) A role for HGF/SF in neural induction and its expression in Hensen's node during gastrulation. Development 121, 813–824
    OpenUrlAbstract
    1. Suzuki A.,
    2. Thies R. S.,
    3. Yamaji N.,
    4. Song J. J.,
    5. Wozney J. M.,
    6. Murakami K.,
    7. Ueno N.
    (1994) A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. USA 91, 10255–10259
    OpenUrlAbstract/FREE Full Text
    1. Tanabe Y.,
    2. Jessell T. M.
    (1996) Diversity and pattern in the developing spinal cord. Science 274, 1115–1123
    OpenUrlAbstract/FREE Full Text
    1. Thery C.,
    2. Sharpe M. J.,
    3. Batley S. J.,
    4. Stern C. D.,
    5. Gherardi E.
    (1995) Expression of HGF/SF, HGFl/MSP and c-met suggests new functions during early chick development. Dev. Genetics 17, 90–101
    OpenUrlCrossRefPubMedWeb of Science
    1. Tonegawa A.,
    2. Funayama N.,
    3. Ueno N.,
    4. Takahashi Y.
    (1997) Mesodermal subdivision along the mediolateral axis in chicken controlled by different concentrations of BMP-4. Development 124, 1975–1984
    OpenUrlAbstract
    1. Uwanogho D.,
    2. Rex M.,
    3. Cartwright E. J.,
    4. Pearl G.,
    5. Healy C.,
    6. Scotting P.,
    7. Sharpe P. T.
    (1995) Embryonic expression of the chicken Sox-2, Sox-3 and Sox-11 genes suggests an interactive role in neuronal development. Mech. Dev 49, 23–36
    OpenUrlCrossRefPubMedWeb of Science
    1. Vakaet L.
    (1973) Inductions par le noeud posterieur de la ligne primitive des oiseaux. C. R. Soc. Biol 167, 1053–1055
    OpenUrlPubMed
    1. Vakaet L.
    (1984) The initiation of gastrular ingression in the chick blastoderm. Amer. Zool 24, 555–562
    OpenUrl
    1. Watanabe Y.,
    2. Le Douarin N. M.
    (1996) A role for BMP-4 in the development of subcutaneous cartilage. Mech. Dev 57, 69–78
    OpenUrlCrossRefPubMedWeb of Science
    1. Weinstein D. C.,
    2. Hemmati-Brivanlou A.
    (1997) Neural induction in Xenopus laevis: evidence for the default model. Curr. Opin. Neurobiol 7, 7–12
    OpenUrlCrossRefPubMed
    1. Wilson I. A.,
    2. Niman H. L.,
    3. Houghten R. A.,
    4. Cherenson A. R.,
    5. Connolly M. L.,
    6. Lerner R. A.
    (1984) The structure of an antigenic determinant in a protein. Cell 37, 767–778
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilson P. A.,
    2. Hemmati-Brivanlou A.
    (1995) Induction of epidermis and inhibition of neural fate by BMP-4. Nature 376, 331–333
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilson P. A.,
    2. Hemmati-Brivanlou A.
    (1997) Vertebrate neural induction: inducers, inhibitors and a new synthesis. Neuron 18, 699–710
    OpenUrlCrossRefPubMedWeb of Science
    1. Xu R. H.,
    2. Kim J.,
    3. Taira M.,
    4. Zhan S.,
    5. Sredni D.,
    6. Kung H. F.
    (1995) A dominant negative bone morphogenetic protein 4 receptor causes neuralization in Xenopus ectoderm. Biochem. Biophys. Res. Commun 212, 212–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Yu K.,
    2. Sturtevant M. A.,
    3. Biehs B.,
    4. François V.,
    5. Padgett R. W.,
    6. Blackman R. K.,
    7. Bier E.
    (1996) The Drosophila decapentaplegic and short gastrulation genes function antagonistically during wing vein development. Development 122, 4033–4044
    OpenUrlAbstract
    1. Zimmermann L. B.,
    2. De Jesús-Escobar J. M.,
    3. Harland R. M.
    (1996) The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599–606
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo
A. Streit, K.J. Lee, I. Woo, C. Roberts, T.M. Jessell, C.D. Stern
Development 1998 125: 507-519;
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.