Article

Tangential Neuronal Migration Controls Axon Guidance: A Role for Neuregulin-1 in Thalamocortical Axon Navigation

Columbia University, New York, New York, United States
Cell (Impact Factor: 32.24). 05/2006; 125(1):127-42. DOI: 10.1016/j.cell.2006.01.042
Source: PubMed

ABSTRACT

Neuronal migration and axon guidance constitute fundamental processes in brain development that are generally studied independently. Although both share common mechanisms of cell biology and biochemistry, little is known about their coordinated integration in the formation of neural circuits. Here we show that the development of the thalamocortical projection, one of the most prominent tracts in the mammalian brain, depends on the early tangential migration of a population of neurons derived from the ventral telencephalon. This tangential migration contributes to the establishment of a permissive corridor that is essential for thalamocortical axon pathfinding. Our results also demonstrate that in this process two different products of the Neuregulin-1 gene, CRD-NRG1 and Ig-NRG1, mediate the guidance of thalamocortical axons. These results show that neuronal tangential migration constitutes a novel mechanism to control the timely arrangement of guidance cues required for axonal tract formation in the mammalian brain.

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Available from: David A Talmage
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    • "One intermediate target affects the response to the next one by changing, for example, the composition of receptors at the surface of the growth cone [77, 80] . Moreover, the guidance of a particular set of axons is tightly controlled in time and space and very often is exquisitely coordinated with the migration of other axons or neurons [81]. Interestingly, the molecular mechanisms of axon guidance are not restricted to the nervous system, and they have also been found to be involved in the development of other systems, such as the vascular system (see following section). "
    [Show abstract] [Hide abstract] ABSTRACT: Our sophisticated thoughts and behaviors are based on the miraculous development of our complex nervous network system, in which many different types of proteins and signaling cascades are regulated in a temporally and spatially ordered manner. Here we review our recent attempts to grasp the principles of nervous system development in terms of general cellular phenomena and molecules, such as volume-regulated anion channels, intracellular Ca(2+) and cyclic nucleotide signaling, the Npas4 transcription factor and the FLRT family of axon guidance molecules. We also present an example illustrating that the same FLRT family may regulate the development of vascular networks as well. The aim of this review is to open up new vistas for understanding the intricacy of nervous and vascular system development.
    Full-text · Article · Feb 2016 · The Journal of Physiological Sciences
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    • "One intermediate target affects the response to the next one by changing, for example, the composition of receptors at the surface of the growth cone [77, 80] . Moreover, the guidance of a particular set of axons is tightly controlled in time and space and very often is exquisitely coordinated with the migration of other axons or neurons [81]. Interestingly, the molecular mechanisms of axon guidance are not restricted to the nervous system, and they have also been found to be involved in the development of other systems, such as the vascular system (see following section). "
    [Show abstract] [Hide abstract] ABSTRACT: Our sophisticated thoughts and behaviors are based on the miraculous development of our complex nervous network system, in which many different types of proteins and signaling cascades are regulated in a temporally and spatially ordered manner. Here we review our recent attempts to grasp the principles of nervous system development in terms of general cellular phenomena and molecules, such as volume-regulated anion channels, intracellular Ca2+ and cyclic nucleotide signaling, the Npas4 transcription factor and the FLRT family of axon guidance molecules. We also present an example illustrating that the same FLRT family may regulate the development of vascular networks as well. The aim of this review is to open up new vistas for understanding the intricacy of nervous and vascular system development.
    Full-text · Article · Oct 2015 · The Journal of Physiological Sciences
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    • "While the programs to explain these observations are far from being understood, the following two examples suggest developmental approaches directed at explaining differences in the morphology of adults between mammals and sauropsids. Formation of thalamo–telencephalic fiber tracts in amniotes In mammals, the paths of thalamo-cortical axons are influenced by ''corridor'' cells (Bielle et al. 2011; Molnár et al. 2012 ) as well as by several factors expressed in the surrounding forebrain (Braisted et al. 2000Braisted et al. , 2009 Lopez-Bendito et al. 2006; Uziel et al. 2006; Molnár et al. 2012; Garel and Lopez-Bendito 2014 ). Identification of these factors and their expression at different times during development suggests an explanation for the trajectory, course, and locus of termination in mice as opposed to chicks (Bielle et al. 2011) and turtles (Bielle et al. 2011; Tosa et al. 2015). "
    [Show abstract] [Hide abstract] ABSTRACT: Organization and development of the forebrain in crocodilians are reviewed. In juvenile Caiman crocodilus, the following features were examined: identification and classification of dorsal thalamic nuclei and their respective connections with the telencephalon, presence of local circuit neurons in the dorsal thalamic nuclei, telencephalic projections to the dorsal thalamus, and organization of the thalamic reticular nucleus. These results document many similarities between crocodilians and other reptiles and birds. While crocodilians, as well as other sauropsids, demonstrate several features of neural circuitry in common with mammals, certain striking differences in organization of the forebrain are present. These differences are the result of evolution. To explore a basis for these differences, embryos of Alligator misissippiensis were examined to address the following. First, very early development of the brain in Alligator is similar to that of other amniotes. Second, the developmental program for individual vesicles of the brain differs between the secondary prosencephalon, diencephalon, midbrain, and hindbrain in Alligator. This is likely to be the case for other amniotes. Third, initial development of the diencephalon in Alligator is similar to that in other amniotes. In Alligator, alar and basal parts likely follow a different developmental scheme. © The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.
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