Published by the Royal Society under the terms of the Creative Commons Attribution License, which permits unrestricted use, provided the original author and source are credited. Scale bar represents 50 µm. In particular, it has recently been implicated in regulating the morphogenesis of the developing neural tube [21–23] and neocortex [24], directly impacting the shape of these developing neural tissues. The cortical delamination defects observed after the loss of reelin in mice are in-line with the effects of mutations in reelin (RELN) observed in human patients. If the density, pattern and gradient of ECM components can direct progenitor and neuronal cell behaviour, could this play a role in the development and expansion of the human neocortex? Combined with the data on decorin in the chick, this suggests that the ECM can coordinate the movement of cells and tissues in key morphogenetic events in neural tube development. These data suggested that the activation state of integrins may be an important factor in responding to the ECM environment [78], and could potentially provide a way of the cell to regulate its own response to the ECM environment. Enter your email address below and we will send you your username, If the address matches an existing account you will receive an email with instructions to retrieve your username, Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstraße 108, D-01307 Dresden, Germany. National Center for Biotechnology Information, Unable to load your collection due to an error, Unable to load your delegates due to an error, ECM, integrins and progenitor cell behaviour. How the extracellular matrix shapes neural development, Neural tube closure: cellular, molecular and biomechanical mechanisms, The unfolding story of two lissencephaly genes and brain development, Genetic malformations of the human cerebral cortex, Polymicrogyria: pathology, fetal origins and mechanisms, The extracellular matrix: not just pretty fibrils, Extracellular matrix and neurite outgrowth. Laminins have been suggested to play a role in this process in the zebrafish neural tube. (d) Images showing GFP in the neocortex of E11 wild-type (left) and Itgb1flox/flox (knockout) (right) mice that were electroporated with CRE-IRES-eGFP and analysed after 24 h. White dashed lines delineate the basal surface. The content shown may differ from the edition of this book sold on Mighty Ape. By contrast, when the environment was made stiffer, by applying a constant pressure using the AFM probe, the axons then avoided this area [113]. It is associated with the structural stabilization of neuronal processes and synaptic contacts during the maturation of the central nervous system. Several recent papers have started to probe how the stiffness of tissue and ECM can alter neural development. In more complex mammalian systems, with more progenitor cell types and germinal zones, it is highly likely that the ECM uses an even further complex network, in coordination with signalling factors and receptors, to regulate progenitor behaviour. (a) Images showing E14.5 mouse neocortex after 24 h of whole hemisphere (HERO) culture with either control IgG antibody (left panels) or the integrin αvβ3 activating antibody, LIBS-6 (right panels), with DAPI staining (blue, upper panels) and immunofluorescence for the mitotic marker PH3 (white, lower panels). Annu. While we have tried to include all the relevant work within the field, we apologize to anyone we have missed. development; extracellular matrix; tissue shape. Bidirectional extracellular matrix signaling during tissue morphogenesis. The ECM plays fundamental developmental and physiological roles in health and disease, including processes underlying the development, maintenance, and regeneration of the nervous system. For instance, the ECM may … Laminins are thought to promote these responses in two ways. Note the apical division of the nucleus in the wild-type, but the more basal division in the tab mutant. They include brevican, neurocan, versican and aggrecan, of which versican has been shown to inhibit neural crest cell migration in Xenopus embryos [91]. Purple arrows indicate the nuclear division. The extracellular matrix in neural crest-cell migration. Neurosci. 2020 May 28;147(10):dev175596. 2020 Dec 3;8:604448. doi: 10.3389/fcell.2020.604448. The ECM comes in a variety of forms, including the more “standard” ECM that is internal to the animal and on the basal side of epithelial sheets, as well as the apical ECM, which is especially elaborated in the invertebrates to form the exoskeleton. While many aspects of neural development have been uncovered, there are still several open questions concerning the mechanisms governing cell and tissue shape. Notably, the response of any cell to a specific ECM component will be greatly affected by the other factors and receptors acting on it. In this review, we discuss the role of the extracellular matrix (ECM) in these processes. Get the latest public health information from CDC:, Get the latest research information from NIH:, Find NCBI SARS-CoV-2 literature, sequence, and clinical content: 2020 Nov 30;10:586946. doi: 10.3389/fcimb.2020.586946. Knockout of integrin β1 in the developing mouse CNS resulted in the detachment of the aRG basal processes from the pial basement membrane in the neocortex, causing subsequent apoptosis of these progenitors [65] (figure 1d,e). Scale bar represents 50 µm. This specific chain appears to be required for differentiation, as plating of the neuroepithelial cells onto laminin lacking the alpha 1 chain only promoted proliferation of these cells [72]. laminin-111 comprises the subunits alpha 1, beta 1 and gamma 1). Extracellular matrix (ECM) and matrix receptors are intimately involved in most biological processes. Additionally, these neurospheres also showed a reduced response to EGF, FGF and nerve growth factor signalling [63]. The HA receptor RHAMM was shown to be expressed by cranial neural crest cells in Xenopus [88] and quail [89]. Published by the Royal Society under the terms of the Creative Commons Attribution License This general laminin is thought to have contained a mixture of different laminins, but was often predominantly laminin-111. This is true on multiple scales, ranging from the shape of cell processes to the shape of entire tissues. Cell Tissue Res. Curr Top Dev Biol. Integrin α6β1 is not the only integrin dimer to have such an effect on cortical progenitor proliferation. Interestingly, these effects of integrin αvβ3 activation required the binding of thyroid hormones to integrin αvβ3, providing a possible explanation for the impairment of cortical development upon lack of thyroid hormones during pregnancy [64]. Genetic malformations of the human cerebral cortex. Red arrows indicate the marginal zone in the wild-type (b′) and abnormal organisation in the laminin gamma 1 mutant (c,c′). In addition to regulating proliferation and differentiation, ECM can also alter the shape of neural progenitors and neurons. Scale bar represents 100 µm. Buy The Extracellular Matrix in Neural Development and Regeneration at Mighty Ape NZ. Neural tube closure: cellular, molecular and biomechanical mechanisms. Neural tube defects. Scale bars represent 500 µm (b,c) and 50 µm (b′,c′). W.B.H. This is particularly interesting, as the proliferative capacity of BPs is thought to be partly responsible for the evolutionary expansion of the neocortex. However, mutations in perlecan also show disruption of cortical plate lamination [38], but this effect is probably caused by the changes in basement membrane structure and altered proliferation observed (which are described above in §2.1). A 2020 view of tension-based cortical morphogenesis. Adapted from [23]. Reelin has also been shown to regulate neuronal migration via the classical pathway; binding to the transmembrane receptors apolipoprotein E receptor 2 (ApoER2) and the very low-density lipoprotein receptor (VLDLR), leading to phosphorylation of the downstream adaptor protein Disabled-1 [98]. This suggested that decorin plays a role in regulating both cell polarization and tissue morphogenesis during chick neural tube formation. During neurulation, the developing neural plate and mesoderm move in a coordinated manner, and are connected by laminin and fibronectin [22]. The Extracellular Matrix in Neural Development and Regeneration close. Scale bar represents 50 µm. Blocking laminin gamma 1 function in these organoids, with a functional-blocking antibody, resulted in abnormal lamination and organization of the developing retina, as well a later degeneration of the shape of the retinal organoids [104]. One such recent example is the function of laminin gamma 1 in human retinal organoids [104]. Compared with mouse, the ferret has an increased number of proliferative BPs, and therefore a more expanded and folded neocortex. -, Walsh CA. Download Structure And Function Of The Extracellular Matrix Book For Free in PDF, EPUB. Summary: This Review discusses our current understanding of how the extracellular matrix helps guide developing tissues by influencing cell adhesion, migration, shape and differentiation, … However, in addition to this, many other ECM components have also been shown to influence the migration of both progenitors and newborn neurons during cortical development. ( a ) Images showing E14.5 mouse…, ECM and cell migration. Would you like email updates of new search results? In particular, laminin has long been associated with promoting neurite outgrowth [75]; reviewed in [76]). doi: 10.1007/s00441-011-1313-4 Another HSPG, syndecan 4, has been shown to regulate proliferation of neuroepithelial cells within the developing zebrafish neural tube [40]. Neural crest cells have also been shown to modulate their ECM environment to affect their own migration. The field of neural development draws on both neuroscience and developmental biology to describe and provide insight into the cellular and … During development, the surrounding glia secrete the ECM that forms the neural lamella around the nerve cord. During early neural development, the ECM and its related receptors have been shown to have many functions. The most well-known ECM component that regulates neuronal migration is the glycoprotein Reelin [80–82]. Tenascin glycoproteins in developing neural tissues: only decoration? For example, the ECM microenvironment in the germinal zones could direct progenitor cell fate, direct neuronal migration, or aid the tangential migration of neurons observed in species with a folded neocortex [110,119–121]. While the ECM typically provides a supportive … Scale bar represents 50 µm. Reelin is thought to mediate neuronal migration by promoting the branching of migrating neurons, allowing greater interaction with the ECM and radial glial scaffold [95]. We show the extracellular matrix components laminin and fibronectin that lie between mesoderm and neural plate act to couple the movements of neural plate and mesoderm during early stages of neurulation and to maintain the close apposition of these two tissues. It also increased the proliferation and survival of human neural stem cells (NSCs) [54,55], and promoted the differentiation of NSCs from human embryonic stem cells (ESCs) [56]. White boxes delineate areas shown in b′ and c′. Development. If the address matches an existing account you will receive an email with instructions to reset your password. Together with the data showing a role of integrin signalling in BP expansion, these data suggest that the changes in ECM expression observed in the developing human neocortex may have contributed to its evolutionary expansion via the regulation of progenitor proliferation. This folding was induced by the addition of recombinant HAPLN1, recombinant lumican and purified collagen I to these neocortex explants cultures as soluble components, and required this specific combination of all three ECM components. There are several major types of proteoglycans (reviewed in [33]) but in this section, we will focus on the heparan sulfate (HS) and chondroitin sulfate proteoglycans (CSPGs). ECM and morphogenesis. These are all key characteristics of mammalian species with an expanded neocortex, suggesting that integrins may play an important role in regulating neocortical size. In particular, the regulation of progenitor proliferation, differentiation and effect on cell shape appear to be highly conserved. Achetez neuf ou d'occasion This is evident in the developing neocortex, where attachment of the apical radial glia (aRG) endfeet to the basement membrane via integrin β1 is important for the bipolar shape of these progenitors. During development, both cells and tissues must acquire the correct shape to allow their proper function. eCollection 2020. For example, in contrast to the above studies in mouse, loss of CSPGs in rat neurospheres via chondroitinase ABC increased both proliferation and neuronal differentiation [48]. Adapted from [77]. ellular matrix, a complex glycoprotein network known to play important roles throughout development, is a critical regulator of optic cup morphogenesis and, as recent work is revealing, the underlying cellular dynamics. This was also the case for differentiating neurons from human ESCs; neurite extension was again increased when plated on laminin compared to various other ECM substrates [56]. Epub 2019 Jun 10. Find Other Styles Note that from the first issue of 2016, MDPI journals use article numbers instead of page numbers. Evidence for this is found in the Drosophila nerve cord. Thus, integrin α6β1 was also shown to be expressed in the early chick neuroepithelium [61] and to be a marker of NSCs in the developing human neocortex [55,62]. Reelin has also been shown to be involved in the switch of neuronal migration from locomotion, when neurons migrate radially along radial glial processes up to the cortical plate, to terminal translocation, when neurons migrate quickly and independent of radial glial processes [96,97]. Taken together, these data strongly indicate that the ECM plays a key role in regulating the morphogenesis of the developing nervous system (figure 3c). Loss of perlecan caused a lengthening of the G1 phase of the cell cycle. (b,c) Quantification of PH3 positive (mitotic) cells in the (b) VZ (APs) and (c) SVZ (BPs). The extracellular matrix (ECM) and its receptors impact the development and function of every cell type in the developing, adult and aging nervous systems. This expansion was due to an over-migration of neurons past the disrupted basement membrane, leading to the presence of ectopic neurons in the meningeal layers and, in half of the embryos studied, exencephaly (malformation of neural tube formation resulting in extrusion of the brain from the skull) [37].
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