Chondroitin sulfate proteoglycans regulate the growth, differentiation and migration of multipotent neural precursor cells through the integrin signaling pathway

Gu, Wen Li; Fu, Sai-Li; Wang, Yan Xia; Liu, Ying; Lü, He Zuo; Xu, Xiao–Ming; Lu, Pei-Hua

doi:10.1186/1471-2202-10-128

Cited by 71 publications

(75 citation statements)

References 56 publications

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“…This is consistent with reports that neuronal differentiation is inhibited when neurons are exposed to amyloid-β (40). It has been demonstrated that changes to CSPG structure through sulfation can alter its function and role in neural differentiation (18). We have recently shown that the secondary structure of polysaccharides can be dramatically altered through a simple oxidative modification of the backbone, and this is accompanied by changes to nanotopography and macromolecular organization (41).…”

Section: Regions Of Amyloid Plaque Buildup In Alzheimer's Present Incsupporting

confidence: 77%

“…Interestingly, the changes to the physical aspects of a neuronal environment can originate from changes to morphology of support cells such as astrocytes and also changes to ECM structure and properties. Cells and ECM polysaccharides play an important role in growth, differentiation, and migration of neural precursors, as well as in repair and plasticity in the central nervous system (17,18). However, in addition to a biological function, cells and macromolecules provide a physically defined environment (19,20), and we postulate a significant role for topography in neural development.…”

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confidence: 99%

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Stochastic nanoroughness modulates neuron–astrocyte interactions and function via mechanosensing cation channels

Blumenthal¹,

Hermanson

Heimrich

et al. 2014

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

136

135

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Extracellular soluble signals are known to play a critical role in maintaining neuronal function and homeostasis in the CNS. However, the CNS is also composed of extracellular matrix macromolecules and glia support cells, and the contribution of the physical attributes of these components in maintenance and regulation of neuronal function is not well understood. Because these components possess well-defined topography, we theorize a role for topography in neuronal development and we demonstrate that survival and function of hippocampal neurons and differentiation of telencephalic neural stem cells is modulated by nanoroughness. At roughnesses corresponding to that of healthy astrocytes, hippocampal neurons dissociated and survived independent from astrocytes and showed superior functional traits (increased polarity and calcium flux). Furthermore, telencephalic neural stem cells differentiated into neurons even under exogenous signals that favor astrocytic differentiation. The decoupling of neurons from astrocytes seemed to be triggered by changes to astrocyte apical-surface topography in response to nanoroughness. Blocking signaling through mechanosensing cation channels using GsMTx4 negated the ability of neurons to sense the nanoroughness and promoted decoupling of neurons from astrocytes, thus providing direct evidence for the role of nanotopography in neuron-astrocyte interactions. We extrapolate the role of topography to neurodegenerative conditions and show that regions of amyloid plaque buildup in brain tissue of Alzheimer's patients are accompanied by detrimental changes in tissue roughness. These findings suggest a role for astrocyte and ECM-induced topographical changes in neuronal pathologies and provide new insights for developing therapeutic targets and engineering of neural biomaterials. mechanotransduction | stretch-activated channels | FAM38A | Piezo-1 | polarization

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Section: Regions Of Amyloid Plaque Buildup In Alzheimer's Present Incsupporting

confidence: 77%

mentioning

confidence: 99%

Stochastic nanoroughness modulates neuron–astrocyte interactions and function via mechanosensing cation channels

Blumenthal¹,

Hermanson

Heimrich

et al. 2014

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

136

135

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“…Interestingly, TNC 2/2 mice show a reduction in expression of ASCL1 (Mash1) by retinal stem/progenitor cells (Besser et al, 2012), in contrast to our study where TNR deficiency resulted in increased ASCL1 expression in NSCs in the ganglionic eminence. Enzymatic degradation of chondroitin sulfate expressed by proteoglycans in the stem cell niche promotes differentiation and migration of neural progenitor cells (Gu et al, 2009), indicating an influence of these extracellular matrix molecules on neurogenesis. The importance of the extracellular matrix in regulating neurogenesis has been supported by studies on matrix metalloproteinases, which can regulate neurogenesis by proteolytic modulation of extracellular matrix molecules (Bovetti et al, 2007;Kang et al, 2008;Tonti et al, 2009;Zhang et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…In addition, a cognate receptor interacting with TNR in NSCs is b1 integrin, which is a prominent sensor of signaling from extracellular matrix components expressed by neural cells (Liao et al, 2008). b1 integrins are highly expressed in murine neurospheres (Gu et al, 2009), and more than 90% of human embryonic-stem-cellderived NSCs express b1 integrins (Ma et al, 2008). Blocking the functions of b1 integrin inhibits proliferation of NSCs (Ma et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

The extracellular matrix glycoprotein tenascin-R regulates neurogenesis during development and in the adult dentate gyrus of mice

Xiao

Jakovčevski

et al. 2013

Journal of Cell Science

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Abnormal generation of inhibitory neurons that synthesize c-aminobutyric acid (GABAergic) is characteristic of neuropsychological disorders. We provide evidence that the extracellular matrix molecule tenascin-R (TNR) -which is predominantly expressed by a subpopulation of interneuronsplays a role in the generation of GABAergic and granule neurons in the murine dentate gyrus by regulating fate determination of neural stem or progenitor cells (NSCs). During development, absence of TNR in constitutively TNR-deficient (TNR 2/2 ) mice results in increased numbers of dentate gyrus GABAergic neurons, decreased expression of its receptor b1 integrin, increased activation of p38 MAPK and increased expression of the GABAergic specification gene Ascl1. Postnatally, increased GABAergic input to adult hippocampal NSCs in TNR 2/2 mice is associated not only with increased numbers of GABAergic and, particularly, parvalbumin-immunoreactive neurons, as seen during development, but also with increased numbers of granule neurons, thus contributing to the increased differentiation of NSCs into granule cells. These findings indicate the importance of TNR in the regulation of hippocampal neurogenesis and suggest that TNR acts through distinct direct and indirect mechanisms during development and in the adult.

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“…Removal of CSs and DSs by ChaseABC treatment, which unselectively cleaves CSs and DSs from CSDSPGs, impaired neurosphere formation, decreased proliferation of NSCs in vitro and in the ventricular zone of E14.5 mouse forebrains (Sirko et al, 2007), and diminished in vitro proliferation of NSCs derived from the E16 rat forebrain (Gu et al, 2009). Although the influence of different CS and DS patterns on NSCs has been reported by studying isolated CSs and DSs, these investigations made use of either chemically synthesized CS and DS oligosaccharides or CSs and DSs extracted mostly from non-neural organs, as well as from different animal species with features possibly different from those derived from neural tissues (Gama et al, 2006;Ida et al, 2006;Sato et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

Dermatan sulfotransferase Chst14/D4st1, but not chondroitin sulfotransferase Chst11/C4st1, regulates proliferation and neurogenesis of neural progenitor cells

Bian

Akyüz

Bernreuther

et al. 2011

Journal of Cell Science

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SummaryChondroitin sulfates (CSs) and dermatan sulfates (DSs) are enriched in the microenvironment of neural stem cells (NSCs) during development and in the adult neurogenic niche, and have been implicated in mechanisms governing neural precursor migration, proliferation and differentiation. In contrast to previous studies, in which a chondroitinaseABC-dependent unselective deglycosylation of both CSs and DSs was performed, we used chondroitin 4-O-sulfotransferase-1 (Chst11/C4st1)-and dermatan 4-O-sulfotransferase-1 (Chst14/D4st1)-deficient NSCs specific for CSs and DSs, respectively, to investigate the involvement of specific sulfation profiles of CS and DS chains, and thus the potentially distinct roles of CSs and DSs in NSC biology. In comparison to wild-type controls, deficiency for Chst14 resulted in decreased neurogenesis and diminished proliferation of NSCs accompanied by increased expression of GLAST and decreased expression of Mash-1, and an upregulation of the expression of the receptors for fibroblast growth factor-2 (FGF-2) and epidermal growth factor (EGF). By contrast, deficiency in Chst11 did not influence NSC proliferation, migration or differentiation. These observations indicate for the first time that CSs and DSs play distinct roles in the self-renewal and differentiation of NSCs.

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Chondroitin sulfate proteoglycans regulate the growth, differentiation and migration of multipotent neural precursor cells through the integrin signaling pathway

Cited by 71 publications

References 56 publications

Stochastic nanoroughness modulates neuron–astrocyte interactions and function via mechanosensing cation channels

Stochastic nanoroughness modulates neuron–astrocyte interactions and function via mechanosensing cation channels

The extracellular matrix glycoprotein tenascin-R regulates neurogenesis during development and in the adult dentate gyrus of mice

Dermatan sulfotransferase Chst14/D4st1, but not chondroitin sulfotransferase Chst11/C4st1, regulates proliferation and neurogenesis of neural progenitor cells

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