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Previous Article | Next Article
The Journal of Neuroscience, January 1, 1998, 18(1):356-370
Peripheral Target Regulation of the Development and Survival of Spinal Sensory and Motor Neurons in the Chick Embryo
Jordi Calderó1, David Prevette2, Xun Mei2, Robert A. Oakley3, Ling Li2, Carol Milligan2, Lucien Houenou2, Michael Burek2, and Ronald W. Oppenheim2 1 Department of Basic Medical Sciences, University of Lleida, Lleida 25198, Catalonia, Spain, 2 Department of Neurobiology and Anatomy, and the Neuroscience Program, Wake Forest University School of Medicine, Winston-Salem, North Carolina 27157, 3 Department of Neurobiology, University of Pittsburgh, Pittsburgh, Pennsylvania 15261
Unilateral limb-bud removal (LBR) before the outgrowth of sensory or motor neurons to the leg of chick embryos was used to examine the role of limb (target)-derived signals in the development and survival of lumbar motoneurons and sensory neurons in the dorsal root ganglia (DRG). After LBR, motor and sensory neurons underwent normal initial histological differentiation, and cell growth in both populations was unaffected. Before their death, target-deprived motoneurons also expressed a cell-specific marker, the homeodomain protein islet-1. Proliferation of sensory and motor precursor cells was also unaffected by LBR, and the migration of neural crest cells to the DRG and of motoneurons into the ventral horn occurred normally. During the normal period of programmed cell death (PCD), increased numbers of both sensory and motor neurons degenerated after LBR. However, whereas motoneuron loss increased by 40-50% (90% total), only ~25% more sensory neurons degenerated after LBR. A significant number of the surviving sensory neurons projected to aberrant targets in the tail after LBR, and many of these were lost after ablation of both the limb and tail. Treatment with neurotrophic factors (or muscle extract) rescued sensory and motor neurons from cell death after LBR without affecting precursor proliferation of either population. Activity blockade with curare failed to rescue motoneurons after LBR, and combined treatment with curare plus muscle extract was no more effective than muscle extract alone. Treatment with the antioxidant N-acetylcysteine rescued motoneurons from normal cell death but not after LBR. Two specific inhibitors of the interleukin
1 converting enzyme (ICE) family of cysteine proteases also failed to prevent motoneuron death after LBR. Taken together these data provide definitive evidence that the loss of spinal neurons after LBR cannot be attributed to altered proliferation, migration, or differentiation. Rather, in the absence of limb-derived trophic signals, the affected neurons fail to survive and undergo PCD. Although normal cell death and cell death after target deprivation share many features in common, the intracellular pathways of cell death in the two may be distinct.
Key words: cell death; chick embryo; spinal cord; motoneurons; sensory neurons; target deprivation; trophic factors
Copyright © 1998 Society for Neuroscience 0270-6474/98/181356-15$05.00/0
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