Advertisement
JOURNAL ARTICLES
Neural crest emigration from the neural tube depends on regulated cadherin expression
S. Nakagawa, M. Takeichi
Development 1998 125: 2963-2971;

Summary

During the emergence of neural crest cells from the neural tube, the expression of cadherins dynamically changes. In the chicken embryo, the early neural tube expresses two cadherins, N-cadherin and cadherin-6B (cad6B), in the dorsal-most region where neural crest cells are generated. The expression of these two cadherins is, however, downregulated in the neural crest cells migrating from the neural tube; they instead begin expressing cadherin-7 (cad7). As an attempt to investigate the role of these changes in cadherin expression, we overexpressed various cadherin constructs, including N-cadherin, cad7, and a dominant negative N-cadherin (cN390), in neural crest-generating cells. This was achieved by injecting adenoviral expression vectors encoding these molecules into the lumen of the closing neural tube of chicken embryos at stage 14. In neural tubes injected with the viruses, efficient infection was observed at the neural crest-forming area, resulting in the ectopic cadherin expression also in migrating neural crest cells. Notably, the distribution of neural crest cells with the ectopic cadherins changed depending on which constructs were expressed. Many crest cells failed to escape from the neural tube when N-cadherin or cad7 was overexpressed. Moreover, none of the cells with these ectopic cadherins migrated along the dorsolateral (melanocyte) pathway. When these samples were stained for Mitf, an early melanocyte marker, positive cells were found accumulated within the neural tube, suggesting that the failure of their migration was not due to differentiation defects. In contrast to these phenomena, cells expressing non-functional cadherins exhibited a normal migration pattern. Thus, the overexpression of a neuroepithelial cadherin (N-cadherin) and a crest cadherin (cad7) resulted in the same blocking effect on neural crest segregation from neuroepithelial cells, especially for melanocyte precursors. These findings suggest that the regulation of cadherin expression or its activity at the neural crest-forming area plays a critical role in neural crest emigration from the neural tube.

REFERENCES

    1. Aberle H.,
    2. Schwartz H.,
    3. Kemler R.
    (1996) Cadherin-catenin complex: protein interactions and their implications for cadherin function. J. Cell Biochem 61, 514–523
    OpenUrlCrossRefPubMedWeb of Science
    1. Akitaya T.,
    2. Bronner-Fraser M.
    (1992) Expression of cell adhesion molecules during initiation and cessation of neural crest cell migration. Dev. Dyn 194, 12–20
    OpenUrlCrossRefPubMedWeb of Science
    1. Bilozur M. E.,
    2. Hay E. D.
    (1988) Neural crest migration in 3D extracellular matrix utilizes laminin, fibronectin, or collagen. Dev. Biol 125, 19–33
    OpenUrlCrossRefPubMed
    1. Barth A. I. M.,
    2. Näthke I. S.,
    3. Nelson W. J.
    (1997) Cadherins, Catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr. Opin. Cell Biol 9, 683–690
    OpenUrlCrossRefPubMedWeb of Science
    1. Bronner-Fraser M.
    (1986) Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK1. Dev. Biol 115, 44–55
    OpenUrlCrossRefPubMedWeb of Science
    1. Duband J. L.,
    2. Volberg T.,
    3. Sabanay I.,
    4. Thiery J. P.,
    5. Geiger B.
    (1988) Spatial and temporal distribution of the adherens-junction-associated adhesion molecule A-CAM during avian embryogenesis. Development 103, 325–344
    OpenUrlAbstract
    1. Erickson C. A.,
    2. Weston J. A.
    (1983) An SEM analysis of neural crest migration in the mouse. J. Embryol. exp. Morph 74, 97–118
    OpenUrlPubMedWeb of Science
    1. Erickson C. A.,
    2. Duong T. D.,
    3. Tosney K. W.
    (1992) Descriptive and experimental analysis of the dispersion of neural crest cells along the dorsolateral path and their entry into ectoderm in the chick embryo. Dev. Biol 151, 251–272
    OpenUrlCrossRefPubMedWeb of Science
    1. Erickson C. A.,
    2. Perris R.
    (1993) The role of cell-cell and cell-matrix interactions in the morphogenesis of the neural crest. Dev. Biol 159, 60–74
    OpenUrlCrossRefPubMedWeb of Science
    1. Erickson C. A.,
    2. Goins T. L.
    (1995) Avian neural crest cells can migrate in the dorsolateral path only if they are specified as melanocytes. Development 121, 915–924
    OpenUrlAbstract
    1. Fagotto F.,
    2. Funayama N.,
    3. Gluck U.,
    4. Gumbiner B. M.
    (1996) Binding to cadherins antagonizes the signaling activity of-catenin during axis formation in Xenopus. J. Cell Biol 132, 1105–1114
    OpenUrlAbstract/FREE Full Text
    1. Fujimori T.,
    2. Takeichi M.
    (1993) Disruption of epithelial cell-cell adhesion by exogenous expression of a mutated nonfunctional N-cadherin. Mol. Biol. Cell 4, 37–47
    OpenUrlAbstract/FREE Full Text
    1. Hamburger V.,
    2. Hamilton H. L.
    (1951) A series of normal stages in the development of the chick embryo. J. Morphol 88, 49–92
    OpenUrlCrossRefPubMedWeb of Science
    1. Hatta K.,
    2. Nose A.,
    3. Nagafuchi A.,
    4. Takeichi M.
    (1988) Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family. J. Cell Biol 106, 873–881
    OpenUrlAbstract/FREE Full Text
    1. Hatta K.,
    2. Takeichi M.
    (1986) Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 320, 447–449
    OpenUrlCrossRefPubMedWeb of Science
    1. Heasman J.,
    2. Crawford A.,
    3. Goldstone K.,
    4. Garner-Hamrick P.,
    5. Gumbiner B.,
    6. McCrea P.,
    7. Kintner C.,
    8. Noro C. Y.,
    9. Wylie C.
    (1994) Overexpression of cadherins and underexpression of-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79, 791–803
    OpenUrlCrossRefPubMedWeb of Science
    1. Henion P. D.,
    2. Weston J. A.
    (1997) Timing and pattern of cell fate restrictions in the neural crest lineage. Development 124, 4351–4359
    OpenUrlAbstract
    1. Hopp T. P.,
    2. Prickett K. S.,
    3. Priice V. L.,
    4. Libby R. T.,
    5. March C. J.,
    6. Cerretti D. P.,
    7. Urdal D. L.,
    8. Conlon P. J.
    (1988) A short polypeptide marker sequence useful for recombinant protein identification and purification. Biotechnology 6, 1204–1210
    OpenUrlCrossRef
    1. Ikeya M.,
    2. Lee S. M. K.,
    3. Johnson J. E.,
    4. McMahon A. P.,
    5. Takada S.
    (1997) Wnt signaling required for expansion of neural crest and CNS progenitors. Nature 389, 966–970
    OpenUrlCrossRefPubMedWeb of Science
    1. Kanegae Y.,
    2. Makimura M.,
    3. Saito I.
    (1994) A simple and efficient method for purification of infectious recombinant adenovirus. Jpn. J. Med. Sci. Biol 47, 157–166
    OpenUrlCrossRefPubMed
    1. Kintner C.
    (1992) Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain. Cell 69, 225–236
    OpenUrlCrossRefPubMedWeb of Science
    1. Mochii M.,
    2. Mazaki Y.,
    3. Mizuno N.,
    4. Hayashi H.,
    5. Eguchi G.
    (1998) Role of Mitf in differentiation and transdifferentiation of chicken pigmented epithelial cell. Dev. Biol 193, 47–62
    OpenUrlCrossRefPubMedWeb of Science
    1. Moriyoshi K.,
    2. Richards L. J.,
    3. Akazawa C.,
    4. O'Leary D. D.,
    5. Nakanishi S.
    (1996) Labeling neural cells using adenoviral gene transfer of membrane-targeted GFP. Neuron 16, 255–260
    OpenUrlCrossRefPubMedWeb of Science
    1. Nakagawa S.,
    2. Takeichi M.
    (1995) Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development 121, 1321–1332
    OpenUrlAbstract
    1. Nagafuchi A.,
    2. Ishihara S.,
    3. Tsukita S.
    (1994) The roles of catenins in the cadherin-mediated cell-cell adhesion: Functional analysis of E-cadherin--catenin fusion molecules. J. Cell Biol 127, 235–245
    OpenUrlAbstract/FREE Full Text
    1. Nieto M. A.,
    2. Sargent M. G.,
    3. Wilkinson D. G.,
    4. Cooke J.
    (1994) Control of cell behavior during vertebrate development by slug, a zinc finger gene. Science 264, 835–839
    OpenUrlAbstract/FREE Full Text
    1. Niwa H.,
    2. Yamamura K.,
    3. Miyazaki J.
    (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193–200
    OpenUrlCrossRefPubMedWeb of Science
    1. Opdecamp K.,
    2. Nakayama A.,
    3. Nguyen M. T.,
    4. Hodgkinson C. A.,
    5. Pavan W. J.,
    6. Arnheiter H.
    (1997) Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development 124, 2377–2386
    OpenUrlAbstract
    1. Riehl R.,
    2. Johnson K.,
    3. Bradley R.,
    4. Grunwald G. B.,
    5. Cornel E.,
    6. Lilienbaum A.,
    7. Holt C. E.
    (1996) Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17, 837–848
    OpenUrlCrossRefPubMedWeb of Science
    1. Sanson B.,
    2. White P.,
    3. Vincent J. P.
    (1996) Uncoupling cadherin-based adhesion from wingless signaling in Drosophila. Nature 383, 627–630
    OpenUrlCrossRefPubMed
    1. Schorle H.,
    2. Meier P.,
    3. Buchert M.,
    4. Jaenisch R.,
    5. Mitchell P. J.
    (1996) Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature 381, 235–238
    OpenUrlCrossRefPubMedWeb of Science
    1. Shimamura K.,
    2. McMahon A. P.,
    3. Takeichi M.
    (1994) Wnt-1-dependent regulation of local E-cadherin and N-catenin expression in the embryonic mouse brain. Development 120, 2225–2234
    OpenUrlAbstract
    1. Suda T.,
    2. Nagata S.
    (1994) Purification and characterization of the Fas-ligand that induces apoptosis. J. Exp. Med 179, 873–879
    OpenUrlAbstract/FREE Full Text
    1. Takeichi M.
    (1993) Cadherins in cancer: Implication for invation and metastasis. Curr. Opin. Cell Biol 5, 806–811
    OpenUrlCrossRefPubMed
    1. Takeichi M.
    (1995) Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol 7, 619–627
    OpenUrlCrossRefPubMedWeb of Science
    1. Thiery J. P.,
    2. Delouvee A.,
    3. Gallin W. J.,
    4. Cunningham B. A.,
    5. Edelman G. M.
    (1984) Ontogenic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers. Dev. Biol 102, 61–78
    OpenUrlCrossRefPubMedWeb of Science
    1. Tosney K. W.
    (1978) The early migration of neural crest cells in the trunk region of the avian embryo: an electron microscopic study. J. Embryol. exp. Morph 62, 317–333
    OpenUrl
    1. Tremblay P.,
    2. Kessel M.,
    3. Gruss P.
    (1995) A transgenic neuroanatomical marker identifies cranial neural crest deficiencies associated with the Pax3 mutant splotch. Dev. Biol 171, 317–329
    OpenUrlCrossRefPubMedWeb of Science
    1. Tucker G. C.,
    2. Aoyama H.,
    3. Lipinski M.,
    4. Tursz T.,
    5. Thiery J. P.
    (1984) Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Differ 14, 223–230
    OpenUrlCrossRefPubMedWeb of Science
    1. Zhang J.,
    2. Hagopian-Donaldson S.,
    3. Serbedzija G.,
    4. Elsemore J.,
    5. Plehn-Dujowich D.,
    6. McMahon A. P.,
    7. Flavell R. A.,
    8. Williams T.
    (1996) Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature 381, 238–241
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Neural crest emigration from the neural tube depends on regulated cadherin expression
S. Nakagawa, M. Takeichi
Development 1998 125: 2963-2971;
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, Brandon Carpenter talks about how inherited histone methylation defines the germline versus soma decision in C. elegans. 

Sign up to join our next session:

10 March
Time: TBC
Chaired by: Thomas Lecuit