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Volume 16, Number 11,
Issue of June 1, 1996
pp. 3685-3703
Copyright ©1996 Society for Neuroscience
A Novel Type of Programmed Neuronal Death in the Cervical Spinal
Cord of the Chick Embryo
Received Nov. 30, 1995; revised Feb. 26, 1996; accepted Feb. 28, 1996.
Hiroyuki Yaginuma1,
Misako Tomita1,
Noriko Takashita1,
Sharen E. McKay2,
Chareba Cardwell2,
Qin-Wei Yin2, and
Ronald W. Oppenheim2
1 Department of Anatomy, Institute of Basic Medical
Sciences, University of Tsukuba, Tsukuba, Ibaraki 305, Japan, and
2 Department of Neurobiology and Anatomy, and Neuroscience
Program, Bowman Gray School of Medicine, Wake Forest University,
Winston-Salem, North Carolina 27157
We examined the massive early cell death that occurs in the ventral
horn of the cervical spinal cord of the chick embryo between embryonic
days 4 and 5 (E4 and E5). Studies with immunohistochemistry, in
situ hybridization, and retrograde-tracing methods revealed that
many dying cells express Islet proteins and Lim-3 mRNA
(motoneuron markers) and send their axons to the somatic region of the
embryo before cell death. Together, these data strongly suggest that
the dying cells are somatic motoneurons. Cervical motoneurons die by
apoptosis and can be rescued by treatment with cycloheximide and
actinomycin D. Counts of motoneuron numbers between E3.5 and E10
revealed that, in addition to cell death between E4 and E5, motoneuron
death also occurs between E6 and E10 in the cervical cord. Studies with
[3H]thymidine autoradiography and morphological
techniques revealed that in the early cell-death phase (E4-E5),
genesis of motoneurons, axonal elongation, and innervation of muscles
is still ongoing. However, studies with [3H]thymidine
autoradiography also revealed that the cells dying between E4 and E5
become postmitotic before E3.5. Increased size of peripheral targets,
treatment with neuromuscular blockade, and treatment with partially
purified muscle or brain extracts and defined neurotrophic agents, such
as NGF, BDNF, neurotrophin-3, CNTF, bFGF, PDGF, S100- , activin,
cholinergic differentiation factor/leukemia inhibitory factor, bone
morphogenetic protein-2, IGF-I, interleukin-6, and TGF-1, were all
ineffective in rescuing motoneurons dying between E4 and E5. By
contrast, motoneurons that undergo programmed cell death at
later stages (E6-E10) in the cervical cord are
target-dependent and respond to activity blockade and trophic factors.
Experimental approaches revealed that early cell death also occurs in a
notochord-induced ectopic supernumerary motoneuron column in the
cervical cord. Transplantation of the cervical neural tube to other
segmental regions failed to alter the early death of motoneurons,
whereas transplantation of other segments to the cervical region failed
to induce early motoneuron death. These results suggest that
the mechanisms that regulate motoneuron death in the cervical spinal
cord between E4 and E5 are independent of interactions with targets.
Rather, this novel type of cell death seems to be determined by signals
that either are cell-autonomous or are derived from other cells
within the cervical neural tube.
Key words:
motoneuron;
sympathetic;
cell death;
apoptosis;
neurotrophic factors;
cervical;
chicken;
quail;
avian;
development
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