The Trophic Role of Oligodendrocytes in the Basal Forebrain

Dai, Xudong; Lercher, Lauren D.; Clinton, Patricia M.; Du, Yangzhou; Livingston, Denise L.; Vieira, Cristina; Yang, Lu; Shen, Michael M.; Dreyfus, Cheryl F.

doi:10.1523/jneurosci.23-13-05846.2003

Cited by 125 publications

(99 citation statements)

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“…For example, they have been shown to regulate transmitter release, synaptic size and stability, and to modulate shortand long-term synaptic plasticity (56)(57)(58)(59). Although neurons have long been viewed as the primary source of BDNF in the central nervous system, recent studies have reported BDNF expression in both oligodendrocytes and astrocytes (60)(61)(62). As these central glia also express erbB receptors, it is important to consider the possibility that erbB signaling regulates neurotrophin expression in these cells as well.…”

Section: Discussionmentioning

confidence: 99%

Nonneuronal cells regulate synapse formation in the vestibular sensory epithelium via erbB-dependent BDNF expression

Gómez-Casati

Murtie

Río

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Synaptogenesis is typically viewed as a process involving only the pre-and postsynaptic neurons, but recent studies suggest that astrocytes are also involved. For example, studies show that astrocytes release thrombospondins, which interact with neuronal gabapentin receptors that, upon activation, induce the formation of excitatory synapses in the central nervous system (1-3). Other studies have shown that complexes of cholesterol and apolipoprotein E-containing lipoproteins released by astrocytes are required for synaptogenesis by purified retinal ganglion cells (4). Although these studies suggest that glia may regulate synapse formation, a number of key questions remain unanswered: (i) Are astrocytes the only glia with synaptogenic activity? (ii) Are thombospondin and cholesterol/ApoE complexes the only glial-derived synaptogenic factors? (iii) Do glia produce synaptogenic factors on their own or in response to other signals? And (iv) what are the functional consequences of disruption of glial-induced synaptogenesis? Our studies on neuron-glia interactions in the vestibular system answer these questions.The vestibular organs provide information about head position and thus contribute to the maintenance of balance and posture. Linear acceleration is transformed into neural signals by mechanotransducing hair cells in sensory epithelia, called maculae, in the orthogonally oriented saccule and utricle. These hair cells synapse on primary sensory neurons that send the information to the brainstem. Vestibular hair cells and their associated sensory nerve terminals are surrounded by nonneuronal cells, called supporting cells (SCs). These SCs express glial markers such as vimentin (5), S100 (6), glutamate-aspartate transporter (7), lowaffinity neurotrophin receptor p75 (8), glial fibrillary acidic protein (GFAP) (9), and proteolipid protein (PLP) (10). They surround synaptic contacts, as astrocytes and perisynaptic Schwann cells do at central and neuromuscular synapses, respectively. Moreover, during development, these nonneuronal cells are precursors for hair cells (11,12), as radial glia are to neurons. Based on these similarities, we hypothesized that interactions of SCs with vestibular neurons and hair cells could be important for the vestibular system, and that the communication between neuronal and nonneuronal cells of the vestibular sensory epithelia could be mediated by some of the same molecules that mediate neuron-glia interactions elsewhere in the nervous system.The growth factor neuregulin 1 (NRG1) and its receptors, the erbB family of tyrosine kinase receptors, have emerged as key mediators of neuron-glia interactions throughout the nervous system (13,14). NRGs are members of the EGF family of growth factors and signal through erbB2, erbB3, and erbB4 (14, 15). NRG1 is expressed primarily by neurons, including many peripheral sensory neurons (16), whereas glial cells express erbB receptors (14,(17)(18)(19). The NRG1/erbB signaling pathway is important for axon-Schwann cell interactions that regulate myeli...

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Section: Discussionmentioning

confidence: 99%

Nonneuronal cells regulate synapse formation in the vestibular sensory epithelium via erbB-dependent BDNF expression

Gómez-Casati

Murtie

Río

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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“…Thus oligodendrocytes in the corpus callosum (Dai et al, 2003) express the neurotrophin and cultured as well in vivo astrocytes are known to express the neurotrophin (Dougherty et al, 2000;Wu et al, 2004;Jean et al, 2008). Interestingly, the nonastrocyte derived BDNF appears to dominate overall protein levels of BDNF seen in the unlesioned control since this population is reduced following cuprizone, coincident with a decrease in BDNF as defined by Western blot.…”

Section: Effects Of Other Astrocyte-derived Molecules Following a Demmentioning

confidence: 99%

Astrocyte-Derived BDNF Supports Myelin Protein Synthesis after Cuprizone-Induced Demyelination

Fulmer

VonDran

Stillman

et al. 2014

Journal of Neuroscience

168

152

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It is well established that BDNF may enhance oligodendrocyte differentiation following a demyelinating lesion, however, the endogenous sources of BDNF that may be harnessed to reverse deficits associated with such lesions are poorly defined. Here, we investigate roles of astrocytes in synthesizing and releasing BDNF. These cells are known to express BDNF following injury in vivo. In culture, they increase BDNF synthesis and release in response to glutamate metabotropic stimulation. Following cuprizone-elicited demyelination in mice, astrocytes contain BDNF and increase levels of metabotropic receptors. The metabotropic agonist, trans-(1S,3R)-1-amino-1,3-cyclopentanedicarboxylic acid (ACPD), was therefore injected into the demyelinating lesion. Increases in BDNF, as well as myelin proteins, were observed. Effects of ACPD were eliminated by coinjection of trkB-Fc to locally deplete BDNF and by deletion of astrocytederived BDNF. The data indicate that astrocyte-derived BDNF may be a source of trophic support that can be used to reverse deficits elicited following demyelination.

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“…Astrocytes also generate complement proteins that modulate synaptic pruning (78). Oligodendrocytes secrete trophic factors that influence the survival and function of neighboring neurons (79), enhance the number of functional synapses between neurons, and can directly regulate neuronal activity (80). Thus, impaired maturation of oligodendroglia may contribute to the impaired maturation of the developing gray matter and vice versa.…”

Section: Mechanisms Of Maturational Impairmentmentioning

confidence: 99%

What brakes the preterm brain? An arresting story

et al. 2013

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Children surviving premature birth have a high risk of cognitive and learning disabilities and attention deficit. In turn, adverse outcomes are associated with persistent reductions in cerebral growth on magnetic resonance imaging (MRI). It is striking that modern care has been associated with a dramatic reduction in the risk of cystic white matter damage, but modest improvements in terms of neurodevelopmental impairment. This review will explore the hypothesis that the disability is primarily associated with impaired neural connectivity rather than cell death alone. Very preterm infants exhibit reduced thalamocortical connectivity and cortical neuroplasticity compared with term-born controls. In preterm fetal sheep, moderate cerebral ischemia with no neuronal loss, but significant diffuse failure of maturation of cortical pyramidal neurons, was associated with impaired dendritic growth and synapse formation, consistent with altered connectivity. These changes were associated with delayed decline in cortical fractional anisotropy (FA) on MRI. Supporting these preclinical findings, preterm human survivors showed similar enduring impairment of microstructural development of the cerebral cortex defined by FA, consistent with delayed formation of neuronal processes. These findings offer the promise that better understanding of impairment of neural connectivity may allow us to promote normal development and growth of the cortex after preterm birth. P remature birth is one of the leading causes of morbidity and mortality. Approximately 6-13% of all births are preterm (1), and in the United States, this has been estimated to cost the community more than $26.2 billion in 2005 alone (1). Most of this cost is related not to acute care but to cerebral palsy and long-term neurodevelopmental disability in surviving very premature (≤30 wk gestation) infants. Disability is highly associated with greater prematurity (2,3), but even in "late preterm" infants at 34-36 wk gestation, the risks of injury and disability are increased sevenfold or more compared with term infants (4). Although there is evidence for modest overall improvements in survival without disability in recent cohorts (2,3), others found no apparent improvement in disability after extremely preterm (<25 wk gestation) birth (5).Historically, preterm human autopsy cases typically showed severe necrotic white matter injury (WMI) with evidence of axonal degeneration and loss of cortical neurons (6,7). This necrosis in turn was associated with cerebral palsy. The greater risk of long-term disability in boys is correlated with greater risk of WMI (8). Encouragingly, there is now evidence of a progressive reduction in the severest form of cystic WMI over time (9). In modern cohorts, severe WMI is seen in only ~1% of cases, whereas less severe (nonnecrotic), diffuse WMI is now common (9,10).It is striking that despite this apparent marked reduction in the severity of WMI, that even less severe forms of WMI injury are associated with impaired brain development and disabil...

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The Trophic Role of Oligodendrocytes in the Basal Forebrain

Cited by 125 publications

References 50 publications

Nonneuronal cells regulate synapse formation in the vestibular sensory epithelium via erbB-dependent BDNF expression

Nonneuronal cells regulate synapse formation in the vestibular sensory epithelium via erbB-dependent BDNF expression

Astrocyte-Derived BDNF Supports Myelin Protein Synthesis after Cuprizone-Induced Demyelination

What brakes the preterm brain? An arresting story

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