Abstract
Chicken embryo neural crest cells that migrate into a paraxial mesoderm constructed of multiple rostral half-somites from quail embryos form unsegmented "polyganglia," instead of distinct dorsal root ganglia (DRG). We report here that the environment that is created by grafting rostral somitic (RS) moieties not only is permissive for neural crest cell migration and consequent DRG formation but also is mitogenic for the DRG precursor cells. On embryonic day 3.5 (E3.5), 1 day after surgery, there is a 42% average increase in volume of the polyganglia compared with the corresponding DRG on the unoperated side. The volume increase is accounted for by an increased number of DRG cells--an average of 46% more cells are found in the polyganglia. The increases in volume and cell number are still present a day later at E4.5 (38% and 52%, respectively) and are observed in both limb-forming and non-limb-forming regions of the embryonic axis. The mechanism for this increase in cell number and volume in the polyganglia is enhanced proliferative activity. On E3.5 the proportion of cells incorporating thymidine of the total DRG cell number is 45% higher in the polyganglia than the control side, when embryos are given a short pulse before sacrifice. This indicates that rostral sclerotomal environment stimulates the crest cells to proliferate. The difference in volume between the polyganglia and the normal DRG continues to grow until at least E8, when the polyganglia are twice as large as the control DRG. The continued increase in volume can also be accounted for by the mitogenic effect of the RS grafts, since on E4.5 the percentage of thymidine-labeled cells compared with the total cell number in DRG is 28% higher in the polyganglia than in control ganglia. This study demonstrates that the somitic microenvironment regulates the proliferation of neural crest cells in the nascent DRG.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- Carr V. M., Simpson S. B., Jr Proliferative and degenerative events in the early development of chick dorsal root ganglia. I. Normal development. J Comp Neurol. 1978 Dec 15;182(4):727–739. doi: 10.1002/cne.901820410. [DOI] [PubMed] [Google Scholar]
- Davies A. M., Thoenen H., Barde Y. A. The response of chick sensory neurons to brain-derived neurotrophic factor. J Neurosci. 1986 Jul;6(7):1897–1904. doi: 10.1523/JNEUROSCI.06-07-01897.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hamburger V., Brunso-Bechtold J. K., Yip J. W. Neuronal death in the spinal ganglia of the chick embryo and its reduction by nerve growth factor. J Neurosci. 1981 Jan;1(1):60–71. doi: 10.1523/JNEUROSCI.01-01-00060.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hofer M. M., Barde Y. A. Brain-derived neurotrophic factor prevents neuronal death in vivo. Nature. 1988 Jan 21;331(6153):261–262. doi: 10.1038/331261a0. [DOI] [PubMed] [Google Scholar]
- Kalcheim C., Barde Y. A., Thoenen H., Le Douarin N. M. In vivo effect of brain-derived neurotrophic factor on the survival of developing dorsal root ganglion cells. EMBO J. 1987 Oct;6(10):2871–2873. doi: 10.1002/j.1460-2075.1987.tb02589.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kalcheim C. Basic fibroblast growth factor stimulates survival of nonneuronal cells developing from trunk neural crest. Dev Biol. 1989 Jul;134(1):1–10. doi: 10.1016/0012-1606(89)90072-9. [DOI] [PubMed] [Google Scholar]
- Kalcheim C., Gendreau M. Brain-derived neurotrophic factor stimulates survival and neuronal differentiation in cultured avian neural crest. Brain Res. 1988 Jun 1;469(1-2):79–86. doi: 10.1016/0165-3806(88)90171-x. [DOI] [PubMed] [Google Scholar]
- Kalcheim C., Le Douarin N. M. Requirement of a neural tube signal for the differentiation of neural crest cells into dorsal root ganglia. Dev Biol. 1986 Aug;116(2):451–466. doi: 10.1016/0012-1606(86)90146-6. [DOI] [PubMed] [Google Scholar]
- Kalcheim C., Teillet M. A. Consequences of somite manipulation on the pattern of dorsal root ganglion development. Development. 1989 May;106(1):85–93. doi: 10.1242/dev.106.1.85. [DOI] [PubMed] [Google Scholar]
- 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]
- Landmesser L., Honig M. G. Altered sensory projections in the chick hind limb following the early removal of motoneurons. Dev Biol. 1986 Dec;118(2):511–531. doi: 10.1016/0012-1606(86)90023-0. [DOI] [PubMed] [Google Scholar]
- Le Douarin N. M. A Feulgen-positive nucleolus. Exp Cell Res. 1973 Mar 15;77(1):459–468. doi: 10.1016/0014-4827(73)90600-9. [DOI] [PubMed] [Google Scholar]
- 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]
- Marusich M. F., Pourmehr K., Weston J. A. A monoclonal antibody (SN1) identifies a subpopulation of avian sensory neurons whose distribution is correlated with axial level. Dev Biol. 1986 Dec;118(2):494–504. doi: 10.1016/0012-1606(86)90021-7. [DOI] [PubMed] [Google Scholar]
- Newgreen D. F., Scheel M., Kastner V. Morphogenesis of sclerotome and neural crest in avian embryos. In vivo and in vitro studies on the role of notochordal extracellular material. Cell Tissue Res. 1986;244(2):299–313. doi: 10.1007/BF00219205. [DOI] [PubMed] [Google Scholar]
- Oppenheim R. W., Cole T., Prevette D. Early regional variations in motoneuron numbers arise by differential proliferation in the chick embryo spinal cord. Dev Biol. 1989 Jun;133(2):468–474. doi: 10.1016/0012-1606(89)90050-x. [DOI] [PubMed] [Google Scholar]
- 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]
- Rothman T. P., Gershon M. D., Fontaine-Pérus J. C., Chanconie M., Le Douarin N. M. The effect of back-transplants of the embryonic gut wall on growth of the neural tube. Dev Biol. 1987 Dec;124(2):331–346. doi: 10.1016/0012-1606(87)90486-6. [DOI] [PubMed] [Google Scholar]
- Stern C. D., Keynes R. J. Interactions between somite cells: the formation and maintenance of segment boundaries in the chick embryo. Development. 1987 Feb;99(2):261–272. doi: 10.1242/dev.99.2.261. [DOI] [PubMed] [Google Scholar]
- Stirling R. V., Summerbell D. The segmentation of axons from the segmental nerve roots to the chick wing. Nature. 1979 Apr 12;278(5705):640–642. doi: 10.1038/278640a0. [DOI] [PubMed] [Google Scholar]
- Swanson G. J., Lewis J. Sensory nerve routes in chick wing buds deprived of motor innervation. J Embryol Exp Morphol. 1986 Jun;95:37–52. [PubMed] [Google Scholar]
- Teillet M. A., Kalcheim C., Le Douarin N. M. Formation of the dorsal root ganglia in the avian embryo: segmental origin and migratory behavior of neural crest progenitor cells. Dev Biol. 1987 Apr;120(2):329–347. doi: 10.1016/0012-1606(87)90236-3. [DOI] [PubMed] [Google Scholar]
- Teillet M. A., Le Douarin N. M. Consequences of neural tube and notochord excision on the development of the peripheral nervous system in the chick embryo. Dev Biol. 1983 Jul;98(1):192–211. doi: 10.1016/0012-1606(83)90349-4. [DOI] [PubMed] [Google Scholar]
- Tosney K. W. The early migration of neural crest cells in the trunk region of the avian embryo: an electron microscopic study. Dev Biol. 1978 Feb;62(2):317–333. doi: 10.1016/0012-1606(78)90219-1. [DOI] [PubMed] [Google Scholar]
- WESTON J. A. A radioautographic analysis of the migration and localization of trunk neural crest cells in the chick. Dev Biol. 1963 Jun;6:279–310. doi: 10.1016/0012-1606(63)90016-2. [DOI] [PubMed] [Google Scholar]
- Weston J. A. The migration and differentiation of neural crest cells. Adv Morphog. 1970;8:41–114. doi: 10.1016/b978-0-12-028608-9.50006-5. [DOI] [PubMed] [Google Scholar]
- Ygge J., Aldskogius H., Grant G. Asymmetries and symmetries in the number of thoracic dorsal root ganglion cells. J Comp Neurol. 1981 Nov 1;202(3):365–372. doi: 10.1002/cne.902020306. [DOI] [PubMed] [Google Scholar]