Insulin-Like Growth Factor-1 Regulates Neurite Outgrowth and Neuronal Migration From Organotypic Cultured Dorsal Root Ganglion

Xiang, Yuzhi; Ding, Ning; Xing, Ziying; Zhang, Weiwei; Liu, Huaxiang; Li, Zhenzhong

doi:10.3109/00207454.2010.535935

Cited by 23 publications

(15 citation statements)

References 30 publications

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“…Furthermore, our studies demonstrated that IGF‐I plays a critical role in regulating the exit of neuroblasts from the subventricular zone (SVZ) and the incorporation of new neurons into the adult olfactory bulb (OB), in part through the activation of the PI3K/AKT pathway . However, IGF‐I effects on hippocampal cell migration/positioning were not reported .…”

Section: Introductionmentioning

confidence: 95%

Brain Insulin-Like Growth Factor-I Directs the Transition from Stem Cells to Mature Neurons During Postnatal/Adult Hippocampal Neurogenesis

Nieto‐Estévez

Oueslati‐Morales

et al. 2016

Stem Cells

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The specific actions of insulin-like growth factor-I (IGF-I) and the role of brain-derived IGF-I during hippocampal neurogenesis have not been fully defined. To address the influence of IGF-I on the stages of hippocampal neurogenesis, we studied a postnatal/adult global Igf-I knockout (KO) mice (Igf-I 2/2) and a nervous system Igf-I conditional KO (Igf-I D/D ). In both KO mice we found an accumulation of Tbr2 1 -intermediate neuronal progenitors, some of which were displaced in the outer granule cell layer (GCL) and the molecular layer (ML) of the dentate gyrus (DG). Similarly, more ectopic Ki671 -cycling cells were detected. Thus, the GCL was disorganized with significant numbers of Prox1 1 -granule neurons outside this layer and altered morphology of radial glial cells (RGCs). Dividing progenitors were also generated in greater numbers in clonal hippocampal stem cell (HPSC) cultures from the KO mice. Indeed, higher levels of Hes5 and Ngn2, transcription factors that maintain the stem and progenitor cell state, were expressed in both HPSCs and the GCL-ML from the Igf-I D/D mice. To determine the impact of Igf-I deletion on neuronal generation in vivo, progenitors in Igf-I 2/2 and Igf-I 1/1 mice were labeled with a GFPexpressing vector. This revealed that in the Igf-I 2/2 mice more GFP 1 -immature neurons were formed and they had less complex dendritic trees. These findings indicate that local IGF-I plays critical roles during postnatal/adult hippocampal neurogenesis, regulating the transition from HPSCs and progenitors to mature granule neurons in a cell stage-dependent manner. STEM CELLS 2016;34:2194-2209 SIGNIFICANCE STATEMENTThere is evidence that systemic insulin-like growth factor-I (IGF-I) promotes neuronal maintenance in the postnatal/adult hippocampus. Other studies have suggested the implication of locally-produced IGF-I in the modulation of adult hippocampal neurogenesis in vivo but this concept was not demonstrated. We present novel findings showing that brain IGF-I directs the generation of granule neurons from neural stem cells in the postnatal/adult mouse hippocampus. We also show that the regulation of gene expression and cycling cell number by IGF-I may be part of the mechanisms involved in these actions.

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Section: Introductionmentioning

confidence: 95%

Brain Insulin-Like Growth Factor-I Directs the Transition from Stem Cells to Mature Neurons During Postnatal/Adult Hippocampal Neurogenesis

Nieto‐Estévez

Oueslati‐Morales

et al. 2016

Stem Cells

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“…IGF-1 and BDNF have been implicated to play important role in the nervous system and neurogenesis, under both healthy and inflammatory conditions, by regulating cell growth, differentiation, migration, survival and neurite outgrowth [56]–[58]. For example, IGF-1 was shown to regulate neurite outgrowth and cell migration from rat dorsal root ganglion explants in a dose-dependent manner (0–20 nM) [59]. Similarly, BDNF was found to significantly enhance cortical neurite outgrowth in a dose-dependent (0–100 pg/mL) manner when cultured in the presence of immature astrocytes, suggesting potential applications in axonal regrowth strategies after spinal cord injury [60].…”

Section: Resultsmentioning

confidence: 99%

Synergistic Effects of 3D ECM and Chemogradients on Neurite Outgrowth and Guidance: A Simple Modeling and Microfluidic Framework

Zervantonakis

Kothapalli

2014

PLoS ONE

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During nervous system development, numerous cues within the extracellular matrix microenvironment (ECM) guide the growing neurites along specific pathways to reach their intended targets. Neurite motility is controlled by extracellular signal sensing through the growth cone at the neurite tip, including chemoattractive and repulsive cues. However, it is difficult to regenerate and restore neurite tracts, lost or degraded due to an injury or disease, in the adult central nervous system. Thus, it is important to evaluate the dynamic interplay between ECM and the concentration gradients of these cues, which would elicit robust neuritogenesis. Such information is critical in understanding the processes involved in developmental biology, and in developing high-fidelity neurite regenerative strategies post-injury, and in drug discovery and targeted therapeutics for neurodegenerative conditions. Here, we quantitatively investigated this relationship using a combination of mathematical modeling and in vitro experiments, and determined the synergistic role of guidance cues and ECM on neurite outgrowth and turning. Using a biomimetic microfluidic system, we have shown that cortical neurite outgrowth and turning under chemogradients (IGF-1 or BDNF) within 3D scaffolds is highly regulated by the source concentration of the guidance cue and the physical characteristics of the scaffold. A mechanistic-driven partial differential equation model of neurite outgrowth has been proposed, which could also be used prospectively as a predictive tool. The parameters for the chemotaxis term in the model are determined from the experimental data using our microfluidic assay. Resulting model simulations demonstrate how neurite outgrowth was critically influenced by the experimental variables, which was further supported by experimental data on cell-surface-receptor expressions. The model results are in excellent agreement with the experimental findings. This integrated approach represents a framework for further elucidation of biological mechanisms underlying neuronal responses of specialized cell types, during various stages of development, and under healthy or diseased conditions.

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“…The number of nerve fiber bundles extended from the DRG explants was counted as previously described (Xiang et al, 2011). Briefly, nerve fiber bundles extended from the DRG explants as far as 200 µm from the edge of a quarter of each DRG explant were counted in each sample.…”

Section: Determination Of Neurite Outgrowth From Drg Explantsmentioning

confidence: 99%

Carbon Disulfide Inhibits Neurite Outgrowth and Neuronal Migration of Dorsal Root Ganglion In Vitro

Ding

Xiang

Jiang

et al. 2011

International Journal of Neuroscience

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Carbon disulfide (CS₂) is a neurotoxic industrial solvent and widely used in the vulcanization of rubber, rayon, cellophane, and adhesives. Although the neurotoxicity of CS₂ has been recognized for over a century, the precise mechanism of neurotoxic action of CS₂ remains unknown. In the present study, a embryonic rat dorsal root ganglia (DRG) explants culture model was established. Using the organotypic DRG cultures, the direct neurotoxic effects of CS₂ on outgrowth of neurites and migration of neurons from DRG explants were investigated. The organotypic DRG cultures were exposed to different concentrations of CS₂ (0.01 mmol/L, 0.1 mmol/L, 1 mmol/L). The number of nerve fiber bundles extended from DRG explants decreased significantly in the presence of CS₂ (0.01 mmol/L, 15.00 ± 2.61, p < .05; 0.1 mmol/L, 11.17 ± 1.47, p < .001; 1 mmol/L, 8.00 ± 1.41, p < .001) as compared with that in the absence of CS₂ (17.83 ± 2.48). The number of neurons migrated from DRG explants decreased significantly in the presence of CS₂ (0.01 mmol/L, 79.50 ± 9.40, p < .01; 0.1 mmol/L, 62.50 ± 14.15, p < .001; 1 mmol/L, 34.67 ± 7.58, p < .001) as compared with that in the absence of CS₂ (99.33 ± 15.16). And also, the decreases in the number of nerve fiber bundles and migrated DRG neurons were in a dose-dependent manner of CS₂. These data implicated that CS₂ could inhibit neurite outgrowth and neuronal migration from DRG explants in vitro.

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Insulin-Like Growth Factor-1 Regulates Neurite Outgrowth and Neuronal Migration From Organotypic Cultured Dorsal Root Ganglion

Cited by 23 publications

References 30 publications

Brain Insulin-Like Growth Factor-I Directs the Transition from Stem Cells to Mature Neurons During Postnatal/Adult Hippocampal Neurogenesis

Brain Insulin-Like Growth Factor-I Directs the Transition from Stem Cells to Mature Neurons During Postnatal/Adult Hippocampal Neurogenesis

Synergistic Effects of 3D ECM and Chemogradients on Neurite Outgrowth and Guidance: A Simple Modeling and Microfluidic Framework

Carbon Disulfide Inhibits Neurite Outgrowth and Neuronal Migration of Dorsal Root Ganglion In Vitro

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