Glial heterogeneity may define the three-dimensional shape of mouse mesencephalic dopaminergic neurones

Abstract

The shape of a neurone--the projection and branching pattern of axons and dendrites--appears to be determined by a combination of intrinisic and environmental influences. We have previously shown that striatal target neurones influence the biochemical maturation of ascending mesencephalic dopamine (DA) cells in culture, as well as the elongation rate of DA neurites. Using a similar approach in which the morphology of individual DA cells can be studied after 3H-DA uptake and autoradiography, we now report on in vitro neurone-glia interactions and show that glial cells exert a morphogenetic effect on DA neurones. Dopaminergic neurones from the mesencephalon were plated on glial monolayers prepared either from the striatal or the mesencephalic region of the embryonic brain. On mesencephalic glial cells the majority of DA neurones develop a great number of highly branched and varicose neurites, whereas on striatal glia they only exhibit one long, thin and rather linear neurite. These results demonstrate that glial cells from two different brain regions have distinct properties which could be used to define neuronal polarity observed in vivo.

Regional differences in glial-derived factors that promote dendritic outgrowth from mouse cortical neurons in vitro

“…A variety of coculture experiments (summarized in Table 1) have been performed by several different laboratories, and the results have for the most part been consistent with the hypotheses that homotypic astroglial cells support a greater number of more highly branched dendrites, whereas target-derived astrocytes promote axonal growth (Prochiantz et al, 1990;Rousselet et al, 1990;Qian et al, 1992). For example, Prochiantz and colleagues (Denis-Donini et al, 1984;Chamak et al, 1987;Autillo-Touati et al, 1988;Rousselet et al, 1988Rousselet et al, , 1990Prochiantz et al, 1990) have found that in the embryonic rodent CNS, both mesencephalic and striatal neurons elaborate a greater number of primary neurites when cocultured with astrocytes derived from the homotypic brain region. In addition to the effects on dendrite morphology, Rousselet et al (1990) observed that mesencephalic neurons extended longer axons in media conditioned by striatal (target)-derived astrocytes than by mesencephalon-derived astrocytes.…”

“…Several lines of evidence suggest that glia from different regions of the CNS differ in their ability to promote neurite outgrowth (Denis-Donini et al, 1984;Chamak et al, 1987;Autillo-Touati et al, 1988;Denis-Donini and Estenoz, 1988;Prochiantz et al, 1990;Qian et al, 1992). Table 1 summarizes these results.…”

“…Although in vitro studies have demonstrated that neurons may have an intrinsic ability to initiate dendrites and axons (Bartlett and Banker, 1984), other studies have provided evidence that dendritic growth of a neuron can be influenced by interactions with other cells. In vitro studies of both the autonomic nervous system and CNS indicate that differences in glia modulation of neurite outgrowth are primarily manifested in the number of neurites elaborated and, to a lesser extent, in the degree of branching or elongation (Denis- Donini et al, 1984;Chamak et al, 1987;Autillo-Touati et al, 1988;Rousselet et al, 1988Rousselet et al, , 1990Tropea et al, 1988;Johnson et al, 1989;Qian et al, 1992). The final form that dendrites develop, including their secondary and tertiary branches, may also be supported by astroglia but, in part, may be further influenced by neuronal activity (Wise et al, 1979;Hammer et al, 1981;Petit et al, 1988;Mattson et al, 1988;Schilling et al, 1991).…”

Expression of the weaver gene in dopamine-containing neural systems is dose-dependent and affects both striatal and nonstriatal regions

“…For example, neurite extension and guidance both require such interactions (Edelman, 1984). Especially pertinent here are the findings of Denis-Donini et al (1984) and Hemmendinger et al (198 l), who have found that extrinsic signals influence the outgrowth of neurites by mesencephalic neurons cultured from normal mice. Abnormal growth signals or abnormal responses to such signals might result in defects in neurite formation in the weaver midbrain, with or without subsequent death of the neurons.…”

Mesencephalic type 1 astrocytes rescue dopaminergic neurons from death induced by serum deprivation

“…Similar mechanisms are thought to be present in the CNS. The striatum is the major target for dopaminergic neurons originating in the zona compacta ofthe substantia nigra, and some apparently successful attempts have been made to identify the striatal-derived neurotrophic factors that are specific for dopaminergic neurons (Prochiantz et al, 1979, 198 1;Di Porzio et al, 1980;Denis-Donini et al, 1983, 1984. During ontogeny, before the growing axons arrive at their targets, local, glial-mediated neurotrophic support is probably important for survival of dopaminergic neurons (O'Malley et al, 199 1, 1992).…”