Advertisement
JOURNAL ARTICLES
Timing and pattern of cell fate restrictions in the neural crest lineage
P.D. Henion, J.A. Weston
Development 1997 124: 4351-4359;

Summary

The trunk neural crest of vertebrate embryos is a transient collection of precursor cells present along the dorsal aspect of the neural tube. These cells migrate on two distinct pathways and give rise to specific derivatives in precise embryonic locations. One group of crest cells migrates early on a ventral pathway and generates neurons and glial cells. A later-dispersing group migrates laterally and gives rise to melanocytes in the skin. These observations raise the possibility that the appearance of distinct derivatives in different embryonic locations is a consequence of lineage restrictions specified before or soon after the onset of neural crest cell migration. To test this notion, we have assessed when and in what order distinct cell fates are specified during neural crest development. We determined the proportions of different types of precursor cells in cultured neural crest populations immediately after emergence from the neural tube and at intervals as development proceeds. We found that the initial neural crest population was a heterogeneous mixture of precursors almost half of which generated single-phenotype clones. Distinct neurogenic and melanogenic sublineages were also present in the outgrowth population almost immediately, but melanogenic precursors dispersed from the neural tube only after many neurogenic precursors had already done so. A discrete fate-restricted neuronal precursor population was distinguished before entirely separate fate-restricted melanocyte and glial precursor populations were present, and well before initial neuronal differentiation. Taken together, our results demonstrate that lineage-restricted subpopulations constitute a major portion of the initial neural crest population and that neural crest diversification occurs well before overt differentiation by the asynchronous restriction of distinct cell fates. Thus, the different morphogenetic and differentiative behavior of neural crest subsets in vivo may result from earlier cell fate-specification events that generate developmentally distinct subpopulations that respond differentially to environmental cues.

REFERENCES

    1. Anderson D. J.,
    2. Axel R.
    (1986) A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. Cell 47, 1079–1090
    OpenUrlCrossRefPubMedWeb of Science
    1. Baroffio A.,
    2. Dupin E.,
    3. Le Douarin N. M.
    (1988) Clone-forming ability and differentiation potential of migratory neural crest cells. Proc. Natl. Acad. Sci. USA 85, 5325–5329
    OpenUrlAbstract/FREE Full Text
    1. Baroffio A.,
    2. Dupin E.,
    3. Le Douarin N. M.
    (1991) Common precursors for neural and mesectodermal derivatives in the cephalic neural crest. Development 112, 301–305
    OpenUrlAbstract
    1. Bronner-Fraser M.,
    2. Fraser S.
    (1988) Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 355, 161–164
    1. Davidson E. H.
    (1990) How embryos work: a comparative view of diverse modes of cell fate specification. Development 108, 365–389
    OpenUrlAbstract
    1. Dupin E.,
    2. Baroffio A.,
    3. Dulac C.,
    4. Cameron-Curry P.,
    5. Le Douarin N. M.
    (1990) Schwann-cell differentiation in clonal cultures of the neural crest, as evidenced by the anti-Schwann cell myelin protein monoclonal antibody. Proc. Natl. Acad. Sci. USA 87, 1119–1123
    OpenUrlAbstract/FREE Full Text
    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 embryos. 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 on the dorsolateral path only if they are specified as melanocytes. Development 121, 915–924
    OpenUrlAbstract
    1. Fagotto F.,
    2. Gumbiner B. M.
    (1996) Cell contact-dependent Signaling. Dev. Biol 180, 445–454
    OpenUrlCrossRefPubMedWeb of Science
    1. Frank E.,
    2. Sanes J. R.
    (1991) Lineage of neurons and glia in chick dorsal root ganglia: analysis in vivo with a recombinant retrovirus. Development 111, 895–908
    OpenUrlAbstract/FREE Full Text
    1. Fraser S. E.,
    2. Bronner-Fraser M.
    (1991) Migrating neural crest cells in the trunk of avian embryos are multipotent. Development 112, 913–920
    OpenUrlAbstract
    1. Girdlestone J.,
    2. Weston J. A.
    (1985) Identification of early neuronal subpopulations in avian neural crest cell cultures. Dev. Biol 109, 274–287
    OpenUrlCrossRefPubMedWeb of Science
    1. Henion P. D.,
    2. Landis S. C.
    (1992) Developmental regulation of leucine-enkephalin expression in adrenal chromaffin cells by glucocorticoids and innervation. J. Neurosci 12, 3818–3827
    OpenUrlAbstract
    1. Henion P. D.,
    2. Weston J. A.
    (1994) Retinoic acid selectively promotes the survival and proliferation of neurogenic precursors in cultured neural crest cell populations. Dev. Biol 161, 243–250
    OpenUrlCrossRefPubMedWeb of Science
    1. Henion P. D.,
    2. Garner A. S.,
    3. Large T. H.,
    4. Weston J. A.
    (1995) trk C-mediated NT-3 signaling is required for the early development of a subpopulation of neurogenic neural crest cells. Dev. Biol 172, 602–613
    OpenUrlCrossRefPubMedWeb of Science
    1. Hökfelt T.,
    2. Johansson O.,
    3. Ljungdahl,
    4. Lundberg J.,
    5. Schultzberg M.
    (1980) Peptidergic neurones. Nature 284, 515–521
    OpenUrlCrossRefPubMed
    1. Ito K.,
    2. Sieber-Blum M.
    (1991) In vitro clonal analysis of quail cardiac neural crest development. Dev. Biol 148, 95–106
    OpenUrlCrossRefPubMedWeb of Science
    1. Kahane N.,
    2. Kalcheim C.
    (1994) Expression of trkC receptor mRNA during development of the avian nervous system. J. Neurobiol 25, 571–584
    OpenUrlCrossRefPubMedWeb of Science
    1. Kitamura K.,
    2. Takiguchi-Hayashi K.,
    3. Sezaki M.,
    4. Yamamoto H.,
    5. Tekeuchi T.
    (1992) Avian neural crest cells express a melanogenic trait during early migration from the neural tube: observations with the new monoclonal antibody MEBL-1. Development 114, 367–378
    OpenUrlAbstract
    1. Le Douarin N.,
    2. Ziller C.,
    3. Couly G.
    (1993) Patterning of neural crest derivatives in the avian embryo: In vivo and in vitro studies. Dev. Biol 159, 24–49
    OpenUrlCrossRefPubMedWeb of Science
    1. Marusich M. F.,
    2. Weston J. A.
    (1992) Identification of early neurogenic cells in the neural crest lineage. Dev. Biol 149, 295–306
    OpenUrlCrossRefPubMedWeb of Science
    1. Marusich M.,
    2. Pourmehr K.,
    3. Weston J. A.
    (1986) A monoclonal antibody (SN1) identifies a subpopulation of avian sensory neurons whose distribution is correlated with axial level. Dev. Biol 118, 494–504
    OpenUrlCrossRefPubMedWeb of Science
    1. Marusich M. F.,
    2. Furneaux H. M.,
    3. Henion P. D.,
    4. Weston J. A.
    (1994) Hu neuronal proteins are expressed in proliferating Neurogenic Cells. J. Neurobiol 25, 143–155
    OpenUrlCrossRefPubMedWeb of Science
    1. Maxwell G.
    (1976) Cell cycle changes during neural crest cell differentiation in vitro. Dev. Biol 49, 66–79
    OpenUrlCrossRefPubMed
    1. Oakley R. A.,
    2. Lasky C. J.,
    3. Erickson C. A.,
    4. Tosney K. W.
    (1994) Glycoconjugates mark a transient barrier to neural crest migration in the chicken embryo. Development 120, 103–114
    OpenUrlAbstract
    1. Raible D. W.,
    2. Eisen J. S.
    (1994) Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development 120, 495–503
    OpenUrlAbstract
    1. Reedy M. V.,
    2. Faraco C. D.,
    3. Erickson C. A.
    (1997) Temporal differences in developmental potential underlie the unique morphogenetic behaviors of early-and late-migrating avian trunk neural crest cells. Dev. Biol 186, 322–.
    OpenUrl
    1. Schilling T. F.,
    2. Kimmel C. B.
    (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120, 483–494
    OpenUrlAbstract
    1. Selleck M.,
    2. Scherson T.,
    3. Bronner-Fraser M.
    (1993) Origins of neural crest cell diversity. Dev. Biol 159, 1–11
    OpenUrlCrossRefPubMedWeb of Science
    1. Serbedzija G. N.,
    2. Bronner-Fraser M.,
    3. Fraser S. E.
    (1989) A vital dye analysis of the timing and pathways of neural crest cell migration. Development 106, 809–819
    OpenUrlAbstract/FREE Full Text
    1. Serbedzija G. N.,
    2. Bronner-Fraser M.,
    3. Fraser S. E.
    (1994) Developmental potential of trunk neural crest cells in the mouse. Development 120, 1709–1718
    OpenUrlAbstract
    1. Shah N. M.,
    2. Marchionni M. A.,
    3. Isaacs I.,
    4. Stroobant P.,
    5. Anderson D. J.
    (1994) Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77, 349–360
    OpenUrlCrossRefPubMedWeb of Science
    1. Shah N. M.,
    2. Groves A. K.,
    3. Anderson D. J.
    (1996) Alternative neural crest cell fates are instructively promoted by TGFsuperfamily members. Cell 85, 331–343
    OpenUrlCrossRefPubMedWeb of Science
    1. Sieber-Blum M.,
    2. Cohen A.
    (1980) Clonal analysis of quail neural crest cells: They are pluripotent and differentiate in vitro in the absence of non-neuronal crest cells. Dev. Biol 80, 96–106
    OpenUrlCrossRefPubMedWeb of Science
    1. Sieber-Blum M.
    (1989) Commitment of neural crest cells to the sensory neuron lineage. Science 243, 1608–1611
    OpenUrlAbstract/FREE Full Text
    1. Stemple D. L.,
    2. Anderson D. J.
    (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71, 973–985
    OpenUrlCrossRefPubMedWeb of Science
    1. Stemple D. L.,
    2. Anderson D. J.
    (1993) Lineage diversification of the neural crest: In vitro investigations. Dev. Biol 159, 12–23
    OpenUrlCrossRefPubMedWeb of Science
    1. Tanaka H.,
    2. Agata A.,
    3. Obata K.
    (1989) A new membrane antigen revealed by monoclonal antibodies is associated with motoneuron axonal pathways. Dev. Biol 132, 419–435
    OpenUrlCrossRefPubMedWeb of Science
    1. Tessarollo L.,
    2. Tsouflas P.,
    3. Martin-Zanca D.,
    4. Gilbert D. J.,
    5. Jenkins N. A.,
    6. Copeland N. G.,
    7. Parada L. F.
    (1993) trkC, a receptor forneurotrophin-3, is widely expressed in the developing nervous system and in non-neuronal tissues. Development 118, 463–475
    OpenUrlAbstract
    1. Verdi J. M.,
    2. Groves A. K.,
    3. Farinas I.,
    4. Jones K.,
    5. Marchionni M. A.,
    6. Reichardt L. F.,
    7. Anderson D. J.
    (1996) A reciprocal cell-cell interaction mediated by NT-3 and neuregulins controls the early survival and development of sympathetic neuroblasts. Neuron 16, 515–527
    OpenUrlCrossRefPubMedWeb of Science
    1. Vogel K. S.,
    2. Weston J. A.
    (1988) A subpopulation of cultured avian neural crest cells has transient neurogenic potential. Neuron 1, 569–577
    OpenUrlCrossRefPubMed
    1. Vogel K. S.,
    2. Weston J. A.
    (1990) The sympathoadrenal lineage in avian embryos. Dev. Biol 139, 1–12
    OpenUrlCrossRefPubMed
    1. Wehrle-Haller B.,
    2. Weston J. A.
    (1995) Soluble and cell-bound forms of steel factor activity play distinct roles in melanocyte precursor dispersal and survival on the lateral neural crest migration pathway. Development 121, 731–742
    OpenUrlAbstract
    1. Weston J. A.
    (1991) Sequential segregation and fate of developmentally restricted intermediate cell populations in the neural crest lineage. Curr. Top. Dev. Biol 25, 133–153
    OpenUrlPubMedWeb of Science
    1. Yao K.-M.,
    2. Samson M.-L.,
    3. Reeves R.,
    4. White K.
    (1993) Gene elav of Drosophila melanogaster: a prototype for neuronal-specific RNA binding protein gene family that is conserved in flies and humans. J. Neurobiol 24, 723–739
    OpenUrlCrossRefPubMedWeb of Science
    1. Zacchei A. M.
    (1961) Lo sviluppo embrionale della quaglia giapponese (Coturnix coturnix japonica). Arch. Ital. Anat. Embriol 66, 36–72
    1. Zhang D.,
    2. Yao L.,
    3. Bernd P.
    (1994) Expression of trk and neurotrophin mRNA in dorsal root and sympathetic ganglia of the quail during development. J. Neurobiol 25, 1517–1532
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Timing and pattern of cell fate restrictions in the neural crest lineage
P.D. Henion, J.A. Weston
Development 1997 124: 4351-4359;
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.