Lineage of neurons and glia in chick dorsal root ganglia: analysis in vivo with a recombinant retrovirus.

We used retrovirus-mediated gene transfer to study the lineage of neural crest cells in chick embryos. Individual crest cells were infected before they migrated from the neural tube, and their clonal progeny were subsequently revealed in sensory ganglia and associated structures by a histochemical stain for the viral gene product (lacZ). We found that crest cells were multipotential in several respects. (1) Many clones contained both ventrolateral (VL) and dorsomedial (DM) neurons, which had been suggested to be lineally distinct. (2) Many clones contained both large and small neurons, which are known to innervate distinct targets. (3) Many clones contained multiple glial subtypes, e.g. both Schwann cells, which ensheath axons, and satellite cells, which ensheath neuronal somata. (4) Many clones contained both neurons and glial cells. On the other hand, a sizeable minority of clones was homogenous, e.g. they contained only neurons or only glial cells--suggesting that some progenitors may be, or become, restricted in potential. Finally, this study provides the first opportunity to compare directly the two methods currently available for tracing cell lineage in vertebrate embryos, retroviral infection and tracer injection: our results and those of Bronner-Fraser and Fraser (1989), who used the latter method, provide complementary but consistent views of crest lineage.

[1]  E. Frank,et al.  Times of origin of brachial sensory neurons are not correlated with neuronal phenotype , 1990, The Journal of comparative neurology.

[2]  S. Landis Target regulation of neurotransmitter phenotype , 1990, Trends in Neurosciences.

[3]  J. Sanes,et al.  Lineage, arrangement, and death of clonally related motoneurons in chick spinal cord , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  S. Fraser,et al.  Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions , 1990, Nature.

[5]  J. Sanes,et al.  Neurons and glia arise from a common progenitor in chicken optic tectum: demonstration with two retroviruses and cell type-specific antibodies. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[6]  S. Fraser,et al.  Developmental potential of avian trunk neural crest cells in situ , 1989, Neuron.

[7]  K. Barald Culture conditions affect the cholinergic development of an isolated subpopulation of chick mesencephalic neural crest cells. , 1989, Developmental biology.

[8]  M. Sieber-Blum SSEA-1 is a specific marker for the spinal sensory neuron lineage in the quail embryo and in neural crest cell cultures. , 1989, Developmental biology.

[9]  F. Watt,et al.  Stem cells: the generation and maintenance of cellular diversity. , 1989, Development.

[10]  S. Fraser,et al.  A vital dye analysis of the timing and pathways of avian trunk neural crest cell migration. , 1989, Development.

[11]  David J. Anderson,et al.  The neural crest cell lineage problem: Neuropoiesis? , 1989, Neuron.

[12]  M. Sieber-Blum Commitment of neural crest cells to the sensory neuron lineage. , 1989, Science.

[13]  M. Raff Glial cell diversification in the rat optic nerve. , 1989, Science.

[14]  J. Sanes Analysing cell lineage with a recombinant retrovirus , 1989, Trends in Neurosciences.

[15]  N. L. Le Douarin,et al.  Developmental potentialities in the nonneuronal population of quail sensory ganglia. , 1989, Developmental biology.

[16]  J. Sanes,et al.  Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a Recombinant Retrovirus , 1988, Neuron.

[17]  S. Fraser,et al.  Cell lineage analysis reveals multipotency of some avian neural crest cells , 1988, Nature.

[18]  D. S. Christie,et al.  Analysis of the development of cellular subsets present in the neural crest using cell sorting and cell culture , 1988, Neuron.

[19]  E. Dupin,et al.  Clone-forming ability and differentiation potential of migratory neural crest cells. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[20]  M. Bronner‐Fraser,et al.  A spatial and temporal analysis of dorsal root and sympathetic ganglion formation in the avian embryo. , 1988, Developmental biology.

[21]  C. Dulac,et al.  A surface protein expressed by avian myelinating and nonmyelinating Schwann cells but not by satellite or enteric glial cells , 1988, Neuron.

[22]  Y. Charnay,et al.  Development and distribution of substance P in the spinal cord and ganglia of embryonic and newly hatched chick: An immunofluorescence study , 1987, The Journal of comparative neurology.

[23]  J. Loring,et al.  Neural crest cell migratory pathways in the trunk of the chick embryo. , 1987, Developmental biology.

[24]  N. L. Le Douarin,et al.  Formation of the dorsal root ganglia in the avian embryo: segmental origin and migratory behavior of neural crest progenitor cells. , 1987, Developmental biology.

[25]  C. Cepko,et al.  Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. Sanes,et al.  Use of a recombinant retrovirus to study post‐implantation cell lineage in mouse embryos. , 1986, The EMBO journal.

[27]  J. Yip Migratory patterns of sympathetic ganglioblasts and other neural crest derivatives in chick embryos , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  A. Mudge,et al.  Distribution and ontogeny of SP, CGRP, SOM, and VIP in chick sensory and sympathetic ganglia. , 1986, Developmental biology.

[29]  N. L. Douarin Cell line segregation during peripheral nervous system ontogeny. , 1986, Science.

[30]  K. H. Lee,et al.  Correlation of cell body size, axon size, and signal conduction velocity for individually labelled dorsal root ganglion cells in the cat , 1986, The Journal of comparative neurology.

[31]  A. Cameron,et al.  The electrophysiological and morphological characteristics of feline dorsal root ganglion cells , 1986, Brain Research.

[32]  N. L. Le Douarin Cell line segregation during peripheral nervous system ontogeny. , 1986, Science.

[33]  J. A. Weston,et al.  Identification of early neuronal subpopulations in avian neural crest cell cultures. , 1985, Developmental biology.

[34]  B. Droz,et al.  Expression of myelin-associated glycoprotein by small neurons of the dorsal root ganglion in chickens. , 1985, Science.

[35]  S. Lawson,et al.  Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. , 1985, The Journal of physiology.

[36]  N. L. Le Douarin,et al.  Embryonic origin of substance P containing neurons in cranial and spinal sensory ganglia of the avian embryo. , 1985, Developmental biology.

[37]  N. L. Le Douarin,et al.  Restrictions of developmental capacities in the dorsal root ganglia during the course of development. , 1983, Cell differentiation.

[38]  D. Noden,et al.  Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. , 1983, The American journal of anatomy.

[39]  G. Ciment,et al.  Early appearance in neural crest and crest-derived cells of an antigenic determinant present in avian neurons. , 1982, Developmental biology.

[40]  M. G. Honig,et al.  The development of sensory projection patterns in embryonic chick hind limb. , 1982, The Journal of physiology.

[41]  A. d'Amico-Martel Temporal patterns of neurogenesis in avian cranial sensory and autonomic ganglia. , 1982, The American journal of anatomy.

[42]  N. L. Le Douarin,et al.  The early development of cranial sensory ganglia and the potentialities of their component cells studied in quail-chick chimeras. , 1982, Developmental biology.

[43]  V. Hamburger,et al.  Neuronal death in the spinal ganglia of the chick embryo and its reduction by nerve growth factor , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  J. Till,et al.  Hemopoietic stem cell differentiation. , 1980, Biochimica et biophysica acta.

[45]  M. Sieber-Blum,et al.  Clonal analysis of quail neural crest cells: they are pluripotent and differentiate in vitro in the absence of noncrest cells. , 1980, Developmental biology.

[46]  N. L. Le Douarin,et al.  Restrictions of developmental capabilities in neural crest cell derivatives as tested by in vivo transplantation experiments. , 1980, Developmental biology.

[47]  W. Harris,et al.  Lysophosphatidyl choline facilitates labeling of CNS projections with horseradish peroxidase , 1980, Journal of Neuroscience Methods.

[48]  N. L. Le Douarin Migration and differentiation of neural crest cells. , 1980, Current topics in developmental biology.

[49]  S. Simpson,et al.  Proliferative and degenerative events in the early development of chick dorsal root ganglia. II. Responses to altered peripheral fields , 1978, The Journal of comparative neurology.

[50]  M. Jacobson,et al.  Origin of the retina from both sides of the embryonic brain: a contribution to the problem of crossing at the optic chiasma. , 1978, Science.

[51]  Kathryn W. Tosney The early migration of neural crest cells in the trunk region of the avian embryo: an electron microscopic study. , 1978, Developmental biology.

[52]  J. A. Weston The migration and differentiation of neural crest cells. , 1970, Advances in morphogenesis.

[53]  E. Pannese Electron microscopical study on the development of the satellite cell sheath in spinal ganglia , 1969, The Journal of comparative neurology.

[54]  J. Rothstein An Introduction to Probability Theory and Its Application . vol. 1. William Feller. Wiley, New York; Chapman and Hall, London, ed. 2, 1957. xv + 461 pp. Illus. $10.75. , 1959, Science.

[55]  Viktor Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1992, Journal of morphology.

[56]  V. Hamburger,et al.  Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. , 1949, The Journal of experimental zoology.