The extracellular matrix glycoprotein tenascin-C promotes locomotor recovery after spinal cord injury in adult zebrafish

Yu, Young-Mi; Cristofanilli, Massimiliano; Valiveti, A.; Ma, Liping; Yoo, Myung Hoon; Morellini, Fabio; Schachner, Melitta

doi:10.1016/j.neuroscience.2011.03.043

Cited by 58 publications

(46 citation statements)

References 82 publications

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“…Thus, the strong injuryinduced increase of the expression of isoforms containing the TNfnBD or TNfnD6 domains may contribute to create an environment promoting axonal regrowth. This interpretation conforms with recent reports that Tnc retards retrograde degeneration in a spinal cord injury model, supposedly via the TNfnD-domain (Chen et al 2010;Yu et al 2011). On the other hand, Tnc deflects growth cones when presented as a sharp boundary next to conducive substrates such as laminins in a choice assay (Faissner and Kruse 1990;Götz et al 1996;Taylor et al 1993).…”

Section: Functional Implications Of Extracellular Matrix Up-regulatiosupporting

confidence: 93%

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

et al. 2012

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CNS lesions generally result in impaired function because regeneration of the adult CNS of mammals is poor. A variety of lesion models has been described that serve to further the understanding of the pathophysiology of the damaged tissue. A central cause of aborted regeneration is the glial scar that expresses a plethora of extracellular matrix molecules. Some of these are considered inhibitors of axon growth and regeneration. The laser lesion of the cortex offers the advantage that a circumscribed lesion of defined energy can be delivered to the cortex non-invasively through the intact dura mater and a thinly drilled wet translucent remnant of the skull. Previously, we have shown that distinct ECM is up-regulated in the penumbra of laser lesions in the rat visual cortex. We propose to transfer this model to the mouse, in view of the availability of a large number of genetical models in this small rodent. Here, we discuss this model and the lesion-related ECM that forms the focus of our analysis.

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Section: Functional Implications Of Extracellular Matrix Up-regulatiosupporting

confidence: 93%

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

et al. 2012

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“…19 When cultured neurons were treated with Pn2 after plating, the average length of the maximum neurite at 48 hours was significantly longer than that of neurons treated with bovine serum albumin (10 g/mL) or with Pn1 (10 g/mL; Figure 6C,D). These data indicate that Pn2 has the potential to promote neurite outgrowth.…”

Section: Pn2 Promoted Neuroprotection and Neurite Outgrowth In Culturmentioning

confidence: 89%

Role of Central Nervous System Periostin in Cerebral Ischemia

Shimamura

Taniyama

Katsuragi

et al. 2012

Stroke

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Background and Purpose-Although periostin, an extracellular matrix glycoprotein, plays pivotal roles in survival, migration, and regeneration in various cells, its expression and function in the brain are still unknown. Here, we investigated the expression and role of periostin in the ischemic brain. Methods-Expression of full-length periostin (periostin 1 [Pn1]) and its splicing variant lacking exon 17 (periostin 2 [Pn2]) was examined by real-time reverse transcription polymerase chain reaction (RT-PCR), Western blotting, and immunohistochemical staining in male C57BL6/J mice. The actions of periostin were examined in adult primary neuronal culture and in a transient middle cerebral artery occlusion (tMCAo) model. Results-Expression of Pn2, but not of Pn1, mRNA was markedly changed after tMCAo. Pn2 mRNA was decreased in the ischemic core at 3 hours after ischemia. At 24 hours, Pn2 mRNA was significantly increased in both the peri-ischemic and ischemic regions. Periostin was mainly observed in neurons in normal brain. However, neuronal expression of periostin was decreased temporarily in the ischemic region, but increased in astrocytes and around endothelial cells at 24 hours after tMCAo. Of importance, intracerebroventricular injection of Pn2 resulted in a significant reduction in infarct volume at 24 hours after tMCAo associated with phosphorylation of Akt. Also, the Pn2-treated mice survived longer until 1 week after tMCAo. Pn2 significantly inhibited neuronal death under hypoxia and stimulated neurite outgrowth. Conclusions-Here, we demonstrated that periostin was expressed in the brain, and exogenous Pn2 exhibited neuroprotective effects and accelerated neurite outgrowth. Additional studies on periostin may provide new insights into the treatment of ischemic stroke. (Stroke. 2012;43:1108-1114.)Key Words: periostin Ⅲ ischemia Ⅲ neuroprotection Ⅲ extracellular matrix Ⅲ neurite outgrowth P eriostin is a 93-kDa secreted N-glycoprotein that modulates cell-matrix interactions and cell functions in the extracellular matrix (ECM). 1 Although periostin was originally found in osteoblasts, 2 recent studies showed that periostin plays pivotal roles in cell survival under hypoxic conditions, 3 migration of cancer cells, 4 and proliferation of cardiomyocytes after acute myocardial infarction. 5 Interestingly, periostin has homology with fasciclin I, which is expressed in grasshoppers and Drosophila. Fasciclin I is a cell adhesion molecule expressed in the central nervous system (CNS) during embryonic CNS development in Drosophila. 6 Also, laser inactivation of fasciclin I disrupts axon adhesion of grasshopper pioneer neurons. 7 Thus, periostin might have pivotal roles in the CNS in mammals, although its expression and function have not been clarified in the adult CNS.One of the unique characteristics of periostin is its variable regions in the C-terminal regions, which contain exons 15 to 23 ( Figure 1A). The presence of splicing variants of periostin is becoming the center of the interest, given that various splicing...

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“…For example, Tenascin-C has been shown to be important for spinal cord regeneration in zebrafish, but possible interactions with Col XII are not known 5 . Furthermore, Col I and Fibronectin, which we find to be abundantly present in the lesion site, are also known ECM components that promote axons growth 45, 58, 59 .…”

Section: Discussionmentioning

confidence: 99%

Wnt signaling controls pro-regenerative Collagen XII in functional spinal cord regeneration in zebrafish

et al. 2017

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The inhibitory extracellular matrix in a spinal lesion site is a major impediment to axonal regeneration in mammals. In contrast, the extracellular matrix in zebrafish allows substantial axon re-growth, leading to recovery of movement. However, little is known about regulation and composition of the growth-promoting extracellular matrix. Here we demonstrate that activity of the Wnt/β-catenin pathway in fibroblast-like cells in the lesion site is pivotal for axon re-growth and functional recovery. Wnt/β-catenin signaling induces expression of col12a1a/b and deposition of Collagen XII, which is necessary for axons to actively navigate the non-neural lesion site environment. Overexpression of col12a1a rescues the effects of Wnt/β-catenin pathway inhibition and is sufficient to accelerate regeneration. We demonstrate that in a vertebrate of high regenerative capacity, Wnt/β-catenin signaling controls the composition of the lesion site extracellular matrix and we identify Collagen XII as a promoter of axonal regeneration. These findings imply that the Wnt/β-catenin pathway and Collagen XII may be targets for extracellular matrix manipulations in non-regenerating species.

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The extracellular matrix glycoprotein tenascin-C promotes locomotor recovery after spinal cord injury in adult zebrafish

Cited by 58 publications

References 82 publications

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

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

Role of Central Nervous System Periostin in Cerebral Ischemia

Wnt signaling controls pro-regenerative Collagen XII in functional spinal cord regeneration in zebrafish

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