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Volume 16, Number 15,
Issue of August 1, 1996
pp. 4662-4672
Copyright ©1996 Society for Neuroscience
Synchronous Onset of NGF and TrkA Survival Dependence in
Developing Dorsal Root Ganglia
Received March 18, 1996; revised May 10, 1996; accepted May 13, 1996.
Fletcher A. White1,
Inmaculada Silos-Santiago2,
Derek C. Molliver1,
Merry Nishimura3,
Heidi Phillips3,
Mariano Barbacid2, and
William D. Snider1
1 Center for the Study of Nervous System Injury,
Department of Neurology, Washington University School of Medicine, St.
Louis, Missouri 63110, 2 Bristol-Myers Squibb, Princeton
University, Princeton, New Jersey 08543, and 3 Genentech
Inc., South San Francisco, California 94080
Determinations of dorsal root ganglion (DRG) neuron loss in nerve
growth factor (NGF) and neurotrophin-3 (NT-3) null mutant mice have
supported the concept that neurons can switch neurotrophin dependence
by revealing that many neurons must require both of these factors
acting either sequentially or simultaneously during development. The
situation is complex, however, in that NT-3( /) mutant
mice show far greater neuron loss than mice deficient in the NT-3
receptor TrkC, suggesting that NT-3 may support many DRG neurons via
actions on the NGF receptor TrkA. To assess the possibility of
ligand-receptor cross-talk as a developmental mechanism, we have
compared the onset of survival dependence of lumbar DRG neurons on
NT-3, TrkC, NGF, and TrkA signaling in mice deficient in these
molecules as a result of gene targeting. At embryonic day 11.5 (E11.5),
virtually all lumbar DRG cells express TrkC mRNA and many require NT-3
and TrkC signaling for survival. In contrast, although many lumbar DRG
cells also express TrkA at E11.5, there is little survival dependence
on TrkA signaling. By E13.5, most lumbar DRG cells have downregulated
TrkC mRNA. The onset of survival dependence on NGF and TrkA-signaling
is concurrent and of equal magnitude at E13.5, demonstrating that NT-3
alone does not support DRG neurons via TrkA, nor can NT-3 compensate
for the loss of NGF. We conclude that many murine DRG cells require
NT-3 for survival before exhibiting NGF dependence and that NT-3
activation of TrkA is unimportant to these early NT-3
survival-promoting actions. We suggest that the discrepancy in cell
loss between NT-3(/) and trkC(/) mutants
is attributable to the ability of NT-3 to support DRG neurons via TrkA
in the artificial situation where TrkC is absent.
Key words:
NGF;
NT-3;
TrkA;
TrkC;
DRG development;
naturally
occurring cell death
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