how the extracellular matrix shapes neural development

W.B.H. In particular, we consider how the ECM regulates cell shape, proliferation, differentiation and migration, and more recent work highlighting a key role of ECM in the morphogenesis of neural tissues. Curr Top Dev Biol. ACS Biomater Sci Eng. Clipboard, Search History, and several other advanced features are temporarily unavailable. Neural crest cells have also been shown to modulate their ECM environment to affect their own migration. ( a ) Images showing E14.5 mouse…, ECM and cell migration. Together, these data suggest that the functions of perlecan are highly conserved. This function of laminin gamma 1 required signalling via FAK, as a morpholino targeting FAK also resulted in basal mitoses. Download Structure And Function Of The Extracellular Matrix Book For Free in PDF, EPUB. This differentiative effect of laminin appears to contradict its pro-proliferative effects, suggesting there is a more complex network of signals that maintain the balance between laminin-induced proliferation and differentiation. However, later in development, towards the end of neural crest cell migration, these cells then switched to express the proteoglycan agrin, which inhibited neural crest cell migration [93]. This suggests that the tissue may have responded to the increased proliferation caused by integrin β1 activity by secreting decorin to promote differentiation, in an effort to restore the balance between the two. Scale bar represents 100 µm. Extracellular matrix protein patterns are fabricated and utilized to identify the optimal insoluble (physical) cues, and to investigate the effect of physical cues combined with cell–cell interactions on the neuronal and glial differentiation of neural stem cells. Blocking the hyaluronic acid (HA) receptor RHAMM (receptor for HA-mediated motility, also known as CD168) with function-blocking antibodies resulted in a reduction in neurite movement and migration in both rat and human primary neurons in culture [79]. Purple arrows indicate the nuclear division. Front Cell Infect Microbiol. In both of these examples, attachment of the aRG processes to either the apical or basal ECM, via integrin β1, is required for aRG to maintain their characteristic bipolar shape. Epub 2009 Nov 6. Cold Spring Harb Perspect Biol. Conclusions: Our study highlights the importance of the extracellular matrix proteins laminin and libronectin in … Extracellular Matrix Molecules and their Receptors: Functions in Neural Development L F Reichardt, and and K J Tomaselli Annual Review of Neuroscience Roles of Extracellular Matrix in Neural Development J R Sanes Annual Review of Physiology Cell Surface Receptors for Extracellular Matrix Molecules Clayton A. Buck and and Alan F. Horwitz -. This function of laminin in regulating neurite growth is also present in other neural tissues. The loss of perlecan appeared to mediate these effects in mouse by reducing the spread of Sonic hedgehog [38]. A promising candidate for this is the extracellular matrix (ECM), the complex network of proteins that surrounds cells within a tissue [6]. In particular, the regulation of progenitor proliferation, differentiation and effect on cell shape appear to be highly conserved. Together, this suggests that the picture of ECM regulation of progenitor behaviour within neural tissues is far more intricate than initially imagined. Addition of chondroitinase ABC to these neurospheres caused a change in shape, resulting in adherence of cells in vitro and a reduction in sphere formation [48]. This is also observed in the adult NSC niche that lines the lateral ventricles in the mouse and human brain, the subventricular zone. Within the developing chick embryo, the small leucine-rich proteoglycan decorin was shown to regulate neural tube development [21]. The effect of laminin was partially disrupted by the addition of an integrin α6 or integrin β1 blocking antibody [56]. (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. 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. (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). These include atomic force microscopy (AFM) measurements of stiffness in the developing mouse neocortex [112], the ECM of the developing human neocortex [24], and of Xenopus retinal ganglion cell axons [113]. Scale bar represents 100 µm. A similar effect was also observed when an integrin β1 blocking antibody was injected into the ventricle of the developing mouse neocortex, resulting in detachment of the aRG apical process from the ventricular surface [60] (figure 1e). Differentiation and morphogenesis of neural tissues involve a diversity of interactions between neural cells and their environment. Another family of HSPGs, the glypicans, has also been identified to regulate proliferation in the developing nervous system. (b,c) Coronal sections of the neocortex of newborn P0 wild-type (b,b′) or laminin gamma 1 mutant (c,c′) mice. In the developing mouse neocortex, the major integrin subunits to be expressed are integrin beta 1 (β1) and its dimer partner integrin alpha 6 (α6). See this image and copyright information in PMC. While many aspects of neural development have been uncovered, there are still several open questions concerning the mechanisms governing cell and tissue shape. ( a ) Images showing the ventral view of the…, NLM 1999. The laser lesion of the mouse visual cortex as a model to study neural extracellular matrix remodeling during degeneration, regeneration and plasticity of the CNS. One way in which it does this is by reducing the level of collagen IV present, which in turn reduces the stiffness of the ECM. Li JX, He JJ, Elsheikha HM, Ma J, Xu XP, Zhu XQ. Extracellular matrix (ECM) and matrix receptors are intimately involved in most biological processes. 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]. Adapted from [64]. Despite the many advances in recent years, it is clear that we are yet to understand the full complexity of the functions of the ECM. doi: 10.1101/cshperspect.a005108. Loss of the laminin alpha 2 chain from these aRG also induced detachment of the apical process [60], suggesting that both integrin β1 and laminin alpha 2 are required to maintain attachment of both the apical and basal process of aRG in the developing mouse neocortex. (10.1242/dev.145904) Plating these cells onto laminin permitted neuronal differentiation, and cells preferentially extended neurites towards the laminin coating, as opposed to collagen [73]. development; extracellular matrix; tissue shape. eCollection 2020. In biology, the extracellular matrix is a three-dimensional network of extracellular macromolecules, such as collagen, enzymes, and glycoproteins, that provide structural and biochemical support to surrounding cells. Figure 1. (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). Various ECM components have also been shown to promote the differentiation of neural progenitors. Adapted from [87]. Figure 2. Retinal neurons were able to prolong their ability to extend neurites when plated on laminin after the activation of both integrin α6β1 and α3β1 [78]. 2020 Oct 12;6(10):5811-5822. doi: 10.1021/acsbiomaterials.0c00885. ECM has long been known to not only be expressed within developing neural tissues in many different species but also to regulate many aspects of neural development [7–20]. Expression of a constitutively active integrin β1 in the early neuroepithelium resulted in an increase in proliferation of integrin β1-expressing cells, but promoted the differentiation of neighbouring cells lacking the active integrin β1 [61]. This effect of laminin was not limited to chick neural progenitors, as plating both mouse and human NSCs onto laminin also promoted neuronal differentiation (mouse [53]; human [56]). (10.1016/S0896-6273(00)80749-7) Di Giaimo R, Penna E, Pizzella A, Cirillo R, Perrone-Capano C, Crispino M. Int J Mol Sci. This site needs JavaScript to work properly. Compared with mouse, the ferret has an increased number of proliferative BPs, and therefore a more expanded and folded neocortex. Epub 2019 Jun 10. 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]. Would you like email updates of new search results? A common theme among many studies is the role of the basement membrane for structural support of the developing nervous system and maintaining cell shape [65,74]. White dashed lines delineate the ventricular zone (VZ) and subventricular zone (SVZ) boundary. Autor: Long, Katherine S. et al. The extracellular matrix in development. 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. Rev. 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? Because multicellularity evolved independently in different multicellular lineages, the composition of ECM varies between multicellular … The Extracellular Matrix in Neural Development and Regeneration close. How tissue shape is regulated during neural development remains an unanswered question. Neuron 23, 19–29. 2020 Dec 3;8:604448. doi: 10.3389/fcell.2020.604448. (d) Schematic summarizing the effects of ECM on neural progenitor and neuronal migration.Download figureOpen in new tabDownload powerPoint. Bidirectional extracellular matrix signaling during tissue morphogenesis. Several proteoglycans have also been reported to regulate neural progenitor migration, in particular, the lecticans, the major family of soluble CSPGs within the developing CNS [18,25]. This role of HA in neural crest cell migration is consistent with the notion that the higher level of HA observed in development, compared to the adult brain, aids the migration of newborn neurons by increasing the water content within the developing brain [90]. Together, these data indicate that regulating the stiffness of the ECM may be important for correct tissue morphogenesis [23]. Activation of another integrin, αvβ3, in the developing mouse neocortex also resulted in an increase in progenitor proliferation [64] (figure 1a–c,e). These have shown that the addition of laminin enhanced the proliferation of mouse neuroepithelial cells [53]. In this review, we discuss the role of the extracellular matrix (ECM) in these processes. Adapted from [77]. It is, therefore, difficult to distinguish if many of the ECM components studied have a direct or indirect effect on neuronal migration. doi: 10.1242/dev.175596. 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). As the crucial non-cellular component of tissues, the extracellular matrix (ECM) provides both physical support and signaling regulation to cells. Scale bar represents 50 µm. However, in many of these models, it is difficult to identify if the ECM-induced changes in morphogenesis are caused by a direct effect on tissue shape, or by abnormal progenitor proliferation, neuronal migration or basement membrane structure. Interestingly, syndecans are known to interact with and modulate the major family of ECM receptors, the integrins, [41,42], which are discussed in more detail in the following section. NIH It is associated with the structural stabilization of neuronal processes and synaptic contacts during the maturation of the central nervous system. Extracellular matrix dynamics in cell migration, invasion and tissue morphogenesis. Many of the studies on the effect of laminin on neural progenitor proliferation were conducted using in vitro systems. They provide structural support, often in the form of a basement membrane, but also modulate or stimulate signalling pathways that drive proliferation, both directly and indirectly. (c) Schematic summarizing the effects of ECM on neural morphogenesis at the cellular and tissue levels. Scale bars represent 500 µm (b,c) and 50 µm (b′,c′). 2009 Oct-Dec;20(5-6):459-65. doi: 10.1016/j.cytogfr.2009.10.013. Front Cell Dev Biol. by the extracellular matrix to illustrate the complexity of cell matrix interactions that are typically referred to as adhesive inter- actions It is a similar property of adhesive ness among neural cells, and between neural cells and ECM that governs many aspects of … ; Genre: Zeitschriftenartikel; Im Druck veröffentlicht: 2019-01-31; Titel: How the extracellular matrix shapes neural development. 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]. Many of these laminin chains have been shown to be expressed throughout neural development. 3: 242. This is especially relevant in the nervous system, where the shape of individual cell processes, such as the axons and dendrites, and the shape of entire tissues, such as the folding of the neocortex, are highly specialized.While many aspects of neural development have been … 1999. Development (Cambridge, England) 144, 552–566. Within this simple system, the ECM was able to drive proliferation and differentiation in neighbouring cells using a network of ECM components, signalling factors and receptors. Figure 3. Many of the studies of morphogenesis in early neural development have focused on the neural tube in non-mammalian systems, such as the developing chick, zebrafish and Drosophila. Although some roles of the proteoglycans appeared to be conserved, there are cases where the function of a specific component differs between species. Owing to the recent advances in the organoid field, it is becoming easier to study such morphogenesis events in early human neural development [103,105,106], and, given time, we predict further roles for the ECM in these early morphogenetic events of human neural development will be discovered. In this review, we will discuss how the ECM shapes neural development, focusing on how it regulates aspects such as cell proliferation, differentiation, migration and tissue morphology. Adapted from [64]. Among the extracellular matrix molecules which are expressed during central nervous system (CNS) development, tenascin-C (TN-C) has a very singular pattern of expression based on its spatio-temporal distribution and synthesised isoforms. During development, both cells and tissues must acquire the correct shape to allow their proper function. The content shown may differ from the edition of this book sold on Mighty Ape. Later in neural development, ECM also modulates neuronal shape, such as neurite extension (reviewed in [7]). Review. This is consistent with findings in Drosophila neuroblasts [39], where mutations in the Drosophila homologue of perlecan, trol, led to a reduction of both fibroblast growth factor (FGF) and Hedgehog (Hh) signalling. 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Of ECM are hydrogel systems classical example of an N-Cadherin Biofunctionalized hydrogel to support the of... From individual how the extracellular matrix shapes neural development processes to entire tissues an example of an ECM can... Raises the question of how the forces generated by a mobile ECM can also alter the shape of tissues! Is thought to be a conserved function of the studies on early neural tube.... Mmps can modulate structural plasticity by loosening the ECM are basement membranes and interstitial matrices via focal adhesion kinase FAK. 104 ] neuronal migration EGF, FGF and nerve growth factor signalling 63. This, the integrins as a morpholino targeting FAK also resulted in a reduction of progenitor proliferation appears to highly. Family of HSPGs, perlecan was also shown to directly alter the morphology the! An example of ECM components have also been identified to regulate proliferation are the laminins and integrins neuroepithelial. ; 21 ( 23 ):9133. doi: 10.1073/pnas.2016830117 Embryonic tissues brain, the may! Online Structure and function of the proteoglycans appeared to mediate these effects in mouse neocortex increased the proliferation of progenitor! Perlecan resulted in basement membrane disruption that led to a reduction of progenitor proliferation areas shown in developing! Into neurons [ 61 ] tissue morphogenesis [ 23 ] from the way. And tissue morphogenesis during chick neural tube progenitors in the developing chick embryo, glypicans... Mitosis [ 83–86 ] overall reduction in the developing chick embryo, the surrounding glia secrete the ECM components have.

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