Elsevier

Developmental Biology

Volume 136, Issue 2, December 1989, Pages 296-303
Developmental Biology

Full paper
The survival of chick retinal ganglion cells in response to brain-derived neurotrophic factor depends on their embryonic age

https://doi.org/10.1016/0012-1606(89)90256-XGet rights and content

Abstract

The survival effects of brain-derived neurotrophic factor (BDNF) on the ganglion cells of the chick retina were studied in vitro at different embryonic ages. We found these effects to be strongly age-dependent: at E5, when the first ganglion cell axons have crossed the optic chiasm, but not yet reached the tectum, ganglion cells survived on a laminin substrate irrespective of the presence or absence of BDNF. At E6, when the axons of the first-generated ganglion cells reached the rostral pole of the tectum, the ganglion cells began to show a dependency on BDNF for survival, but the majority of them were alive after 2 days in vitro in the absence of BDNF. With increasing age, the BDNF dependency for survival increased, and at E11, the majority of the ganglion cells plated were dependent on BDNF for survival. It is at this age that the maximal number of axons can be found in vivo in the optic nerve, the subsequent elimination of ganglion cells and their axons resulting in the loss of hundreds of thousands of them over the next few days. Taken together, these data indicate that retinal ganglion cells depend on BDNF for survival only when their axons have reached their target in vivo. This situation is reminiscent of that described in the peripheral nervous system for the nerve growth factor responsiveness of mouse trigeminal sensory neurons during the period of innervation of their target.

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      The commonly held view is that RGCs compete for neurotrophic support; those that in some way fail to obtain sufficient support die, resulting in activation of proapoptotic pathways and the loss of over half the RGC population during the developmental period. Thus, early postnatal removal of a central target such as the SC during the period of naturally occurring cell death causes a rapid and massive increase in RGC death, while addition of factors such as BDNF or NT-4/5 results in increased RGC survival (Caleo, Menna, Chierzi, Cenni, & Maffei, 2000; Cui & Harvey, 1994, 1995; Ma, Hsieh, Forbes, Johnson, & Frost, 1998; Rodriguez-Tebar, Jeffrey, Thoenen, & Barde, 1989; Spalding, Cui, & Harvey, 1998; Vanselow, Dutting, & Thanos, 1990). Consistent with the concept of target-derived support, BDNF is synthesized by cells in the SC and is retrogradely transported back to RGCs (Frost, 2001; Ma et al., 1998; Marotte, Vidovic, Wheeler, & Jhaveri, 2004; Pease, McKinnon, Quigley, Kerrigan-Baumrind, & Zack, 2000).

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      When deprived of retrograde transported NTs derived from target organs, developing neurons have been shown to die by apoptosis (Raff et al., 1993). Also, RGCs have been shown to be maintained by exogenous brain-derived neurotrophic factor (BDNF) in vitro (Johnson et al., 1986; Rodriguez-Tebar et al., 1989; Cohen-Cory and Fraser, 1994). However, the role of target-derived NTs in maintaining mature neurons is less clear.

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    A.R.-T. is a recipient of a fellowship from the Max-Planck Society.

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