Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in
  • Log out

Search

  • Advanced search
Development
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Development

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube 

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
JOURNAL ARTICLES
The role of the yolk syncytial layer in germ layer patterning in zebrafish
S. Chen, D. Kimelman
Development 2000 127: 4681-4689;
S. Chen
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
D. Kimelman
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

Formation of the three germ layers requires a series of inductive events during early embryogenesis. Studies in zebrafish indicate that the source of these inductive signals may be the extra-embryonic yolk syncytial layer (YSL). The characterization of genes encoding the nodal-related factor, Squint, and homeodomain protein, Bozozok, both of which are expressed in the YSL, suggested that the YSL has a role in mesendoderm induction. However, these genes, and a second nodal-related factor, cyclops, are also expressed in the overlying marginal blastomeres, raising the possibility that the marginal blastomeres can induce mesendodermal genes independently of the YSL. We have developed a novel technique to study signaling from the YSL in which we specifically eliminate RNAs in the YSL, thus addressing the in vivo requirement of RNA-derived signals from this region in mesendoderm induction. We show that injection of RNase into the yolk cell after the 1K cell stage (3 hours) effectively eliminates YSL transcripts without affecting ubiquitously expressed genes in the blastoderm. We also present data that indicate the stability of existing proteins in the YSL is unaffected by RNase injection. Using this technique, we show that RNA in the YSL is required for the formation of ventrolateral mesendoderm and induction of the nodal-related genes in the ventrolateral marginal blastomeres, revealing the presence of an unidentified inducing signal released from the YSL. We also demonstrate that the dorsal mesoderm can be induced independently of signals from the YSL and present evidence that this is due to the stabilization of (β)-catenin in the dorsal marginal blastomeres. Our results demonstrate that germ layer formation and patterning in zebrafish uses a combination of YSL-dependent and -independent inductive events.

REFERENCES

    1. Ault K. T.,
    2. Durmowicz G.,
    3. Galione A.,
    4. Harger P. L.,
    5. Busa W. B.
    (1996) Modulation of Xenopus embryo mesoderm-specific gene expression and dorsoanterior patterning by receptors that activate the phosphatidylinositol cycle signal transduction pathway. Development 122, 2033–2041
    OpenUrlAbstract
    1. Erter C. E.,
    2. Solnica-Krezel L.,
    3. Wright C. V.
    (1998) Zebrafish nodal-related 2 encodes an early mesendodermal inducer signaling from the extraembryonic yolk syncytial layer. Dev. Biol 204, 361–372
    OpenUrlCrossRefPubMedWeb of Science
    1. Fekany K.,
    2. Yamanaka Y.,
    3. Leung T.,
    4. Sirotkin H. I.,
    5. Topczewski J.,
    6. Gates M. A.,
    7. Hibi M.,
    8. Renucci A.,
    9. Stemple D.,
    10. Radbill A.,
    11. et al.
    (1999) The zebrafish bozozok locus encodes Dharma, a homeodomain protein essential for induction of gastrula organizer and dorsoanterior embryonic structures. Development 126, 1427–1438
    OpenUrlAbstract
    1. Feldman B.,
    2. Gates M. A.,
    3. Egan E. S.,
    4. Dougan S. T.,
    5. Rennebeck G.,
    6. Sirotkin H. I.,
    7. Schier A. F.,
    8. Talbot W. S.
    (1998) Zebrafish organizer development and germ-layer formation require Nodal-related signals. Nature 395, 181–185
    OpenUrlCrossRefPubMed
    1. Griffin K.,
    2. Patient R.,
    3. Holder N.
    (1995) Analysis of FGF function in normal and no tail zebrafish embryos reveals separate mechanisms for formation of the trunk and the tail. Development 121, 2983–2994
    OpenUrlAbstract
    1. Griffin K. J.,
    2. Amacher S. L.,
    3. Kimmel C. B.,
    4. Kimelman D.
    (1998) Molecular identification of spadetail: regulation of zebrafish trunk and tail mesoderm formation by T-box genes. Development 125, 3379–3388
    OpenUrlAbstract
    1. Gritsman K.,
    2. Talbot W. S.,
    3. Schier A. F.
    (2000) Nodal signaling patterns the organizer. Development 127, 921–932
    OpenUrlAbstract
    1. Gritsman K.,
    2. Zhang J.,
    3. Cheng S.,
    4. Heckscher E.,
    5. Talbot W. S.,
    6. Schier A. F.
    (1999) The EGF-CFC protein One-Eyed Pinhead is essential for Nodal signaling. Cell 97, 121–132
    OpenUrlCrossRefPubMedWeb of Science
    1. Hedgepeth C. M.,
    2. Conrad L. J.,
    3. Zhang J.,
    4. Huang H.,
    5. Lee V. M. Y.,
    6. Klein P.
    (1997) Activation of the Wnt signaling pathway: A molecular mechanism for lithium action. Dev. Biol 185, 82–91
    OpenUrlCrossRefPubMedWeb of Science
    1. Jesuthasan S.,
    2. Stahle U.
    (1996) Dynamic microtubules and specification of the zebrafish embryonic axis. Curr. Biol 7, 31–42
    1. Kane D. A.,
    2. Kimmel C. B.
    (1993) The zebrafish midblastula transition. Development 119, 447–456
    OpenUrlAbstract
    1. Kelly G. M.,
    2. Erezyilmaz D. F.,
    3. Moon R. T.
    (1995) Induction of a secondary embryonic axis in zebrafish following the overexpression of-catenin. Mech. Dev 53, 261–273
    OpenUrlCrossRefPubMedWeb of Science
    1. Kimelman D.,
    2. Griffin K. J.
    (1998) Mesoderm induction: a postmodern view. Cell 94, 419–421
    OpenUrlCrossRefPubMed
    1. Kimmel C. B.,
    2. Law R. D.
    (1985) Cell lineage of zebrafish blastomeres. II. Formation of the yolk syncytial layer. Dev. Biol 108, 86–93
    OpenUrlCrossRefPubMedWeb of Science
    1. Klein P. S.,
    2. Melton D. A.
    (1996) A molecular mechanism for the effectof lithium on development. Proc. Natl. Acad. Sci. USA 93, 8455–8459
    OpenUrlAbstract/FREE Full Text
    1. Koos D. S.,
    2. Ho R. K.
    (1998) The nieuwkoid gene characterizes and mediates a Nieuwkoop-center-like activity in the zebrafish. Curr. Biol 8, 1199–206
    OpenUrlCrossRefPubMedWeb of Science
    1. Koos D. S.,
    2. Ho R. K.
    (1999) The nieuwkoid/dharma homeobox gene is essential for bmp2b repression in the zebrafish pregastrula. Dev. Biol 215, 190–207
    OpenUrlCrossRefPubMedWeb of Science
    1. Melby A. E.,
    2. Kimelman D.,
    3. Kimmel C. B.
    (1997) Spatial regulation of floating head expression in the developing notochord. Dev. Dyn 209, 2225–2237
    OpenUrl
    1. Mizuno T.,
    2. Yamaha E.,
    3. Wakahara M.,
    4. Kuroiwa A.,
    5. Takeda H.
    (1996) Mesoderm induction in zebrafish. Nature 383, 131–132
    OpenUrlCrossRef
    1. Moon R. T.,
    2. Kimelman D.
    (1998) From cortical rotation to organizer gene expression: toward a molecular explanation of axis specification in Xenopus. BioEssays 20, 536–545
    OpenUrlCrossRefPubMedWeb of Science
    1. Ober E. A.,
    2. Schulte-Merker S.
    (1999) Signals from the yolk cell induce mesoderm, neuroectoderm, the trunk organizer, and the notochord in zebrafish. Dev. Biol 215, 167–181
    OpenUrlCrossRefPubMed
    1. Rebagliati M. R.,
    2. Toyama R.,
    3. Haffter P.,
    4. Dawid I. B.
    (1998) cyclops encodes a nodal -related factor involved in midline signaling. Proc. Natl. Acad. Sci. USA 95, 9932–9937
    OpenUrlAbstract/FREE Full Text
    1. Rodaway A.,
    2. Takeda H.,
    3. Koshida S.,
    4. Broadbent J.,
    5. Price B.,
    6. Smith J. C.,
    7. Patient R.,
    8. Holder N.
    (1999) Induction of the mesendoderm in the zebrafish germ ring by yolk cell-derived TGF-family signals and discrimination of mesoderm and endoderm by FGF. Development 126, 3067–3078
    OpenUrlAbstract
    1. Sampath K.,
    2. Rubinstein A. L.,
    3. Cheng A. M.,
    4. Liang J. O.,
    5. Fekany K.,
    6. Solnica-Krezel L.,
    7. Korzh V.,
    8. Halpern M. E.,
    9. Wright C. V.
    (1998) Induction of the zebrafish ventral brain and floorplate requires Cyclops/Nodal signalling. Nature 395, 185–189
    OpenUrlCrossRefPubMed
    1. Schneider S.,
    2. Steinbeisser H.,
    3. Warga R. M.,
    4. Hausen P.
    (1996) -catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech. Dev 57, 191–198
    OpenUrlCrossRefPubMedWeb of Science
    1. Schulte-Merker S.,
    2. Ho R. K.,
    3. Herrmann B. G.,
    4. Nusslein-Volhard C.
    (1992) The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development 116, 1021–1032
    OpenUrlAbstract/FREE Full Text
    1. Shimizu T.,
    2. Yamanaka Y.,
    3. Ryu S.,
    4. Hashimoto H.,
    5. Yabe T.,
    6. Hirata T.,
    7. Bae Y.,
    8. Hibi M.,
    9. Hirano T.
    (2000) Cooperative roles of Bozozok/Dharma and Nodal-related proteins in the formation of the dorsal organizer in zebrafish. Mech. Dev 91, 293–303
    OpenUrlCrossRefPubMedWeb of Science
    1. Solnica-Krezel L.,
    2. Driever W.
    (1994) Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly. Development 120, 2443–2455
    OpenUrlAbstract/FREE Full Text
    1. Stachel S. E.,
    2. Grunwald D. J.,
    3. Myers P. Z.
    (1993) Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development 117, 1261–74
    OpenUrlAbstract
    1. Stambolic V.,
    2. Ruel L.,
    3. Woodgett J. R.
    (1996) Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol 6, 1664–1668
    OpenUrlCrossRefPubMedWeb of Science
    1. Strahle U.,
    2. Jesuthasan S.
    (1993) Ultraviolet irradiation impairs epiboly in zebrafish embryos: evidence for a microtubule-dependent mechanism of epiboly. Development 119, 909–919
    OpenUrlAbstract/FREE Full Text
    1. Thisse C.,
    2. Thisse B.
    (1999) Antivin, a novel and divergent member of the TGF-superfamily, negatively regulates mesoderm induction. Development 126, 229–240
    OpenUrlAbstract
    1. Wittbrodt J.,
    2. Rosa F. M.
    (1994) Disruption of mesoderm and axis formation in fish by ectopic expression of Activin variants: the role of maternal Activin. Genes Dev 8, 1448–1462
    OpenUrlAbstract/FREE Full Text
    1. Yamaha E.,
    2. Mizuno T.,
    3. Hasebe Y.,
    4. Takeda H.,
    5. Yamazaki F.
    (1998) Dorsal specification in blastoderm at the blastula stage in the goldfish, Carassius auratus. Dev. Growth Differ 40, 267–275
    OpenUrlCrossRefPubMed
    1. Yamanaka Y.,
    2. Mizuno T.,
    3. Sasai Y.,
    4. Kishi M.,
    5. Takeda H.,
    6. Kim C. H.,
    7. Hibi M.,
    8. Hirano T.
    (1998) A novel homeobox gene, dharma, can induce the organizer in a non-cell-autonomous manner. Genes Dev 12, 2345–2353
    OpenUrlAbstract/FREE Full Text
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Development.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
The role of the yolk syncytial layer in germ layer patterning in zebrafish
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
Share
JOURNAL ARTICLES
The role of the yolk syncytial layer in germ layer patterning in zebrafish
S. Chen, D. Kimelman
Development 2000 127: 4681-4689;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
JOURNAL ARTICLES
The role of the yolk syncytial layer in germ layer patterning in zebrafish
S. Chen, D. Kimelman
Development 2000 127: 4681-4689;

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome
  • Germline and developmental roles of the nuclear transport factor importin (α)3 in C. elegans
  • Monofocal origin of telencephalic oligodendrocytes in the anterior entopeduncular area of the chick embryo
Show more JOURNAL ARTICLES

Similar articles

Other journals from The Company of Biologists

Journal of Cell Science

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

Advertisement

Interviews — Bénédicte Sanson and Kate Storey

Bénédicte Sanson and Kate Storey

Hear from Bénédicte Sanson, winner of the BSDB’s Cheryll Tickle medal, and Kate Storey, winner of the BSDB’s Waddington Medal, as they discuss their research, the future of the field and the importance of collaboration.


Review Commons launches

We're excited to be an affiliate journal for Review Commons, the ASAPbio/EMBO platform for high-quality journal-independent peer-review in the life sciences, which went live on 09 December.


Have you heard about our Travelling Fellowships?

Peter Baillie-Johnson in Switzerland

Early-career researchers can apply for up to £2,500 to offset the cost of travel and expenses to make collaborative visits to other labs around the world. Read about Peter’s experience in Switzerland, where he joined forces with the Lutolf lab to refine a protocol for producing gastruloids.


Publishing peer review reports

To continue working towards transparency around the editorial process, Development now publishes a ‘Peer review history file’ alongside published papers. Read more about the policy and see the reports for yourself in one the first papers to publish the reports (under the ‘Info & metrics’ tab).


Development at a glance — Cell interactions in collective cell migration

Extract from the poster showing specific cell-cell interactions in metastasis.

Take a look at the latest poster and accompanying article by Denise Montell and her colleagues from the University of California, where they describe a sampling of both known and new cells that migrate collectively in vivo.

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Sign up for alerts

About us

  • About Development
  • About the Node
  • Editors and board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Biology Open transfer

Journal info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact Development
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2019   The Company of Biologists Ltd   Registered Charity 277992