Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Aug 1;88(15):6398–6402. doi: 10.1073/pnas.88.15.6398

Cytotactin expression in somites after dorsal neural tube and neural crest ablation in chicken embryos.

S S Tan 1, A L Prieto 1, D F Newgreen 1, K L Crossin 1, G M Edelman 1
PMCID: PMC52092  PMID: 1713677

Abstract

The spatiotemporal expression of the extracellular matrix protein cytotactin/tenascin during somitogenesis suggests that it plays a role in the morphogenetic events that give rise to the pattern of neural crest (NC) development. In the present study, the spatial distribution and molecular forms of cytotactin in somites were examined using in situ hybridization, Western blotting, and immunohistochemistry during normal development and after injury. In situ hybridization showed that prior to NC cell invasion cytotactin mRNA was restricted to the caudal half of the newly formed epithelial somites. As each epithelial somite matured, giving rise to a sclerotome and dermamyotome, the mRNA was first restricted to the dermamyotome and later restricted to the rostral protion of the sclerotome, consistent with the previously reported protein distribution. Immunocytochemical analysis of the distribution of cytotactin and NC cells in embryos with ablations that removed NC cells, or with simple wounds that left NC cells in place, demonstrated that the presence of NC cells is neither necessary nor sufficient for the correct positioning of cytotactin. Immunoblotting analysis showed that cytotactin synthesized by sclerotomes in the absence of NC cells was of similar molecular mass to that produced in their presence. These findings are in accord with the notion that the abnormalities of cytotactin distribution are related to the wounding process. We conclude that, contrary to the suggestion of Stern et al. [Stern, C. D., Norris, W. E., Bronner-Fraser, M., Carlson, G. J., Faissner, A., Keynes, R. J. & Schachner, M. (1989) Development 107, 309-319], there is no causal link between the presence of NC cells and the distribution and molecular mass of sclerotomal cytotactin.

Full text

PDF
6398

Images in this article

6399Image
on p.6399
6399Image
on p.6399
6400Image
on p.6400
6402Image
on p.6402

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bellairs R. The mechanism of somite segmentation in the chick embryo. J Embryol Exp Morphol. 1979 Jun;51:227–243. [PubMed] [Google Scholar]
  2. Boxberg Y. V. Protein analysis on two-dimensional polyacrylamide gels in the femtogram range: use of a new sulfur-labeling reagent. Anal Biochem. 1988 Mar;169(2):372–375. doi: 10.1016/0003-2697(88)90298-9. [DOI] [PubMed] [Google Scholar]
  3. Bronner-Fraser M. Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Dev Biol. 1986 May;115(1):44–55. doi: 10.1016/0012-1606(86)90226-5. [DOI] [PubMed] [Google Scholar]
  4. Bronner-Fraser M. Distribution and function of tenascin during cranial neural crest development in the chick. J Neurosci Res. 1988 Oct-Dec;21(2-4):135–147. doi: 10.1002/jnr.490210206. [DOI] [PubMed] [Google Scholar]
  5. Chiquet-Ehrismann R., Mackie E. J., Pearson C. A., Sakakura T. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell. 1986 Oct 10;47(1):131–139. doi: 10.1016/0092-8674(86)90374-0. [DOI] [PubMed] [Google Scholar]
  6. Crossin K. L., Hoffman S., Grumet M., Thiery J. P., Edelman G. M. Site-restricted expression of cytotactin during development of the chicken embryo. J Cell Biol. 1986 May;102(5):1917–1930. doi: 10.1083/jcb.102.5.1917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Daniloff J. K., Crossin K. L., Pinçon-Raymond M., Murawsky M., Rieger F., Edelman G. M. Expression of cytotactin in the normal and regenerating neuromuscular system. J Cell Biol. 1989 Feb;108(2):625–635. doi: 10.1083/jcb.108.2.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Davies J. A., Cook G. M., Stern C. D., Keynes R. J. Isolation from chick somites of a glycoprotein fraction that causes collapse of dorsal root ganglion growth cones. Neuron. 1990 Jan;4(1):11–20. doi: 10.1016/0896-6273(90)90439-m. [DOI] [PubMed] [Google Scholar]
  9. Duband J. L., Dufour S., Hatta K., Takeichi M., Edelman G. M., Thiery J. P. Adhesion molecules during somitogenesis in the avian embryo. J Cell Biol. 1987 May;104(5):1361–1374. doi: 10.1083/jcb.104.5.1361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Faissner A., Kruse J., Chiquet-Ehrismann R., Mackie E. The high-molecular-weight J1 glycoproteins are immunochemically related to tenascin. Differentiation. 1988;37(2):104–114. doi: 10.1111/j.1432-0436.1988.tb00802.x. [DOI] [PubMed] [Google Scholar]
  11. Friedlander D. R., Hoffman S., Edelman G. M. Functional mapping of cytotactin: proteolytic fragments active in cell-substrate adhesion. J Cell Biol. 1988 Dec;107(6 Pt 1):2329–2340. doi: 10.1083/jcb.107.6.2329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Halfter W., Chiquet-Ehrismann R., Tucker R. P. The effect of tenascin and embryonic basal lamina on the behavior and morphology of neural crest cells in vitro. Dev Biol. 1989 Mar;132(1):14–25. doi: 10.1016/0012-1606(89)90200-5. [DOI] [PubMed] [Google Scholar]
  13. Hoffman S., Edelman G. M. A proteoglycan with HNK-1 antigenic determinants is a neuron-associated ligand for cytotactin. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2523–2527. doi: 10.1073/pnas.84.8.2523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jones F. S., Crossin K. L., Cunningham B. A., Edelman G. M. Identification and characterization of the promoter for the cytotactin gene. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6497–6501. doi: 10.1073/pnas.87.17.6497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jones F. S., Hoffman S., Cunningham B. A., Edelman G. M. A detailed structural model of cytotactin: protein homologies, alternative RNA splicing, and binding regions. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1905–1909. doi: 10.1073/pnas.86.6.1905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kessel M., Gruss P. Murine developmental control genes. Science. 1990 Jul 27;249(4967):374–379. doi: 10.1126/science.1974085. [DOI] [PubMed] [Google Scholar]
  17. Keynes R. J., Stern C. D. Segmentation in the vertebrate nervous system. 1984 Aug 30-Sep 5Nature. 310(5980):786–789. doi: 10.1038/310786a0. [DOI] [PubMed] [Google Scholar]
  18. Lightner V. A., Gumkowski F., Bigner D. D., Erickson H. P. Tenascin/hexabrachion in human skin: biochemical identification and localization by light and electron microscopy. J Cell Biol. 1989 Jun;108(6):2483–2493. doi: 10.1083/jcb.108.6.2483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Loring J. F., Erickson C. A. Neural crest cell migratory pathways in the trunk of the chick embryo. Dev Biol. 1987 May;121(1):220–236. doi: 10.1016/0012-1606(87)90154-0. [DOI] [PubMed] [Google Scholar]
  20. Mackie E. J., Halfter W., Liverani D. Induction of tenascin in healing wounds. J Cell Biol. 1988 Dec;107(6 Pt 2):2757–2767. doi: 10.1083/jcb.107.6.2757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mackie E. J., Tucker R. P., Halfter W., Chiquet-Ehrismann R., Epperlein H. H. The distribution of tenascin coincides with pathways of neural crest cell migration. Development. 1988 Jan;102(1):237–250. doi: 10.1242/dev.102.1.237. [DOI] [PubMed] [Google Scholar]
  22. Neff A. W., Malacinski G. M., Chung H. M. Amphibian (urodele) myotomes display transitory anterior/posterior and medial/lateral differentiation patterns. Dev Biol. 1989 Apr;132(2):529–543. doi: 10.1016/0012-1606(89)90248-0. [DOI] [PubMed] [Google Scholar]
  23. Neukirchen R. O., Schlosshauer B., Baars S., Jäckle H., Schwarz U. Two-dimensional protein analysis at high resolution on a microscale. J Biol Chem. 1982 Dec 25;257(24):15229–15234. [PubMed] [Google Scholar]
  24. Newgreen D. F., Powell M. E., Moser B. Spatiotemporal changes in HNK-1/L2 glycoconjugates on avian embryo somite and neural crest cells. Dev Biol. 1990 May;139(1):100–120. doi: 10.1016/0012-1606(90)90282-n. [DOI] [PubMed] [Google Scholar]
  25. Newgreen D., Thiery J. P. Fibronectin in early avian embryos: synthesis and distribution along the migration pathways of neural crest cells. Cell Tissue Res. 1980;211(2):269–291. doi: 10.1007/BF00236449. [DOI] [PubMed] [Google Scholar]
  26. Perris R., Krotoski D., Lallier T., Domingo C., Sorrell J. M., Bronner-Fraser M. Spatial and temporal changes in the distribution of proteoglycans during avian neural crest development. Development. 1991 Feb;111(2):583–599. doi: 10.1242/dev.111.2.583. [DOI] [PubMed] [Google Scholar]
  27. Prieto A. L., Crossin K. L., Cunningham B. A., Edelman G. M. Localization of mRNA for neural cell adhesion molecule (N-CAM) polypeptides in neural and nonneural tissues by in situ hybridization. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9579–9583. doi: 10.1073/pnas.86.23.9579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Prieto A. L., Jones F. S., Cunningham B. A., Crossin K. L., Edelman G. M. Localization during development of alternatively spliced forms of cytotactin mRNA by in situ hybridization. J Cell Biol. 1990 Aug;111(2):685–698. doi: 10.1083/jcb.111.2.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ranscht B., Bronner-Fraser M. T-cadherin expression alternates with migrating neural crest cells in the trunk of the avian embryo. Development. 1991 Jan;111(1):15–22. doi: 10.1242/dev.111.1.15. [DOI] [PubMed] [Google Scholar]
  30. Rickmann M., Fawcett J. W., Keynes R. J. The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J Embryol Exp Morphol. 1985 Dec;90:437–455. [PubMed] [Google Scholar]
  31. Spring J., Beck K., Chiquet-Ehrismann R. Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments. Cell. 1989 Oct 20;59(2):325–334. doi: 10.1016/0092-8674(89)90294-8. [DOI] [PubMed] [Google Scholar]
  32. Stern C. D., Norris W. E., Bronner-Fraser M., Carlson G. J., Faissner A., Keynes R. J., Schachner M. J1/tenascin-related molecules are not responsible for the segmented pattern of neural crest cells or motor axons in the chick embryo. Development. 1989 Oct;107(2):309–319. doi: 10.1242/dev.107.2.309. [DOI] [PubMed] [Google Scholar]
  33. Tan S. S., Crossin K. L., Hoffman S., Edelman G. M. Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution. Proc Natl Acad Sci U S A. 1987 Nov;84(22):7977–7981. doi: 10.1073/pnas.84.22.7977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tucker G. C., Aoyama H., Lipinski M., Tursz T., Thiery J. P. 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. 1984 Aug;14(3):223–230. doi: 10.1016/0045-6039(84)90049-6. [DOI] [PubMed] [Google Scholar]
  35. Wehrle B., Chiquet M. Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowth in vitro. Development. 1990 Oct;110(2):401–415. doi: 10.1242/dev.110.2.401. [DOI] [PubMed] [Google Scholar]
  36. Weston J. A., Butler S. L. Temporal factors affecting localization of neural crest cells in tbe chicken embryo. Dev Biol. 1966 Oct;14(2):246–266. doi: 10.1016/0012-1606(66)90015-7. [DOI] [PubMed] [Google Scholar]
  37. Youn B. W., Malacinski G. M. Somitogenesis in the amphibian Xenopus laevis: scanning electron microscopic analysis of intrasomitic cellular arrangements during somite rotation. J Embryol Exp Morphol. 1981 Aug;64:23–43. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES