Role of Peripheral Nerve Extracellular Matrix in Schwann Cell Function and in Neurite Regeneration

Bunge, Mary Bartlett; Bunge, Richard P.; Kleitman, Naomi; Dean, Andy C.

doi:10.1159/000111911

Cited by 116 publications

(72 citation statements)

References 35 publications

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“…2 and 3). Collagen is an important ECM component, constituting approximately 49% of total protein of peripheral nerve (Bunge et al, 1989). The principal role of collagen is to provide structural as well as mechanical support to the nerve.…”

Section: Resultsmentioning

confidence: 99%

Decellularisation and histological characterisation of porcine peripheral nerves

Žilić

Wilshaw

Haycock

2016

Biotech & Bioengineering

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Peripheral nerve injuries affect a large proportion of the global population, often causing significant morbidity and loss of function. Current treatment strategies include the use of implantable nerve guide conduits (NGC's) to direct regenerating axons between the proximal and distal ends of the nerve gap. However, NGC's are limited in their effectiveness at promoting regeneration Current NGCs are not suitable as substrates for supporting either neuronal or Schwann cell growth, as they lack an architecture similar to that of the native extracellular matrix (ECM) of the nerve. The aim of this study was to create an acellular porcine peripheral nerve using a novel decellularisation protocol, in order to eliminate the immunogenic cellular components of the tissue, while preserving the three‐dimensional histoarchitecture and ECM components. Porcine peripheral nerve (sciatic branches were decellularised using a low concentration (0.1%; w/v) sodium dodecyl sulphate in conjunction with hypotonic buffers and protease inhibitors, and then sterilised using 0.1% (v/v) peracetic acid. Quantitative and qualitative analysis revealed a ≥95% (w/w) reduction in DNA content as well as preservation of the nerve fascicles and connective tissue. Acellular nerves were shown to have retained key ECM components such as collagen, laminin and fibronectin. Slow strain rate to failure testing demonstrated the biomechanical properties of acellular nerves to be comparable to fresh controls. In conclusion, we report the production of a biocompatible, biomechanically functional acellular scaffold, which may have use in peripheral nerve repair. Biotechnol. Bioeng. 2016;113: 2041–2053. © 2016 The Authors. Biotechnology and Bioengineering published by Wiley Periodicals, Inc.

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Section: Resultsmentioning

confidence: 99%

Decellularisation and histological characterisation of porcine peripheral nerves

Žilić

Wilshaw

Haycock

2016

Biotech & Bioengineering

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“…Among the matrix components, laminin has an important role as it promotes neurite outgrowth and extension of several nerve cell types (Sanes, 1989). Laminin is produced by Schwann cells and astrocytes (Liesi et al, 1983;Bunge et al, 1989) and is a basal membrane component in the peripheral nerves (Bunge et al, 1989) and in selected regions of the central nervous system (Liesi, 1985). Nerve cells recognize laminin via cell-surface receptors of the integrin family (Reichardt et al, 1989).…”

Section: Introductionmentioning

confidence: 99%

Up-regulation of the integrin alpha 1/beta 1 in human neuroblastoma cells differentiated by retinoic acid: correlation with increased neurite outgrowth response to laminin.

et al. 1991

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Retinoic acid (RA) is known to induce differentiation of neuroblastoma cells in vitro. Here we show that treatment of two human neuroblastoma cell lines, SY5Y and IMR32, with RA resulted in a fivefold increase of the integrin alpha 1/beta 1 expression. The effect was selective because expression of the alpha 3/beta 1 integrin, also present in these cells, was not increased. The up-regulation of the alpha 1/beta 1 differentiated SY5Y cells correlated with increased neurite response to laminin. In fact, RA-treated SY5Y cells elongated neurites on laminin-coated substratum more efficiently compared with untreated cells or cells treated with nerve growth factor, insulin, or phorbol 12-myristate 13-acetate. These three agents induced partial morphological differentiation but did not increase alpha 1 integrin expression. Neurite extension in RA-treated cells was more efficient on laminin than on fibronectin or collagen type I and was inhibited with beta 1 integrin antibodies on all three substrates. Affinity chromatography experiments showed that alpha 1/beta 1 is the major laminin receptor in both untreated and RA-treated SY5Y cells. These data show that RA, a naturally occurring morphogen implicated in embryonic development, can selectively regulate the expression of integrin complexes in neuronal cells and suggest an important role of the alpha 1/beta 1 laminin receptor in the morphological differentiation of nerve cells.

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Section: Polymersmentioning

confidence: 99%

“…Basement membrane is a specific type of ECM secreted by support cells and composed of >20 different molecules [75] . They are of specific interest for axon regeneration due to their crucial role in regeneration in the damaged peripheral nerve [76] .Although it is typically difficult to isolate and manipulate these fragile substrates without causing damage, recent advances have made successful isolation of various basement membranes possible [75] . Several combination ECM materials isolated from mammalian sources are commercially available [52,77] , while others are in various stages of development and characterization [19,[78][79][80] .…”

mentioning

confidence: 99%

Biomaterials for spinal cord repair

Haggerty

Oudega

2013

Neurosci. Bull.

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Spinal cord injury (SCi) results in permanent loss of function leading to often devastating personal, economic and social problems. A contributing factor to the permanence of SCi is that damaged axons do not regenerate, which prevents the re-establishment of axonal circuits involved in function. Many groups are working to develop treatments that address the lack of axon regeneration after SCi. The emergence of biomaterials for regeneration and increased collaboration between engineers, basic and translational scientists, and clinicians hold promise for the development of effective therapies for SCi. A plethora of biomaterials is available and has been tested in various models of SCi. Considering the clinical relevance of contusion injuries, we primarily focus on polymers that meet the specific criteria for addressing this type of injury. Biomaterials may provide structural support and/or serve as a delivery vehicle for factors to arrest growth inhibition and promote axonal growth. Designing materials to address the specific needs of the damaged central nervous system is crucial and possible with current technology. Here, we review the most prominent materials, their optimal characteristics, and their potential roles in repairing and regenerating damaged axons following SCi.Keywords: spinal cord injury; axon regeneration; biodegradable materials; extracellular matrix proteins; functional recovery; growth factor; guidance; injury and repair; spinal motor neuron IntroductionSpinal cord injury (SCi) causes loss of neurons and axons resulting in motor and sensory function impairments. There are thousands of new cases of SCi in the world annually [1,2] occurring often in young adults. The lack of endogenous repair and the significant costs to the individual, family and society [1] are important motivations behind the continuing efforts to develop effective therapies. Promoting axonal regeneration is considered a potential repair strategy because it could lead to recovery of axonal circuits involved in motor and/or sensory function [3] .The central nervous system (CNS) neurons are intrinsically capable of some regeneration of damaged axons [4] but their attempts after SCi are frustrated by structural and chemical obstructions in the damaged nervous tissue [5] . Spinal cord repair approaches typically lead to small functional gains. one feature that most of these approaches have in common is a poor axonal regeneration response, suggesting that promoting axonal regeneration, including synapse formation, is essential to achieve substantial functional repair after SCi. if so, it is rational to anticipate that effective spinal cord therapies will need to include interventions addressing the axon growth-inhibition that leads to the poor axonal growth responses. As introduced above, axonal regeneration is considered an important repair mechanism for the injured spinal cord. Therefore, this review focuses on materials that have shown most promise to elicit an axonal regeneration response to foster functional restoration after ...

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Role of Peripheral Nerve Extracellular Matrix in Schwann Cell Function and in Neurite Regeneration

Cited by 116 publications

References 35 publications

Decellularisation and histological characterisation of porcine peripheral nerves

Decellularisation and histological characterisation of porcine peripheral nerves

Up-regulation of the integrin alpha 1/beta 1 in human neuroblastoma cells differentiated by retinoic acid: correlation with increased neurite outgrowth response to laminin.

Biomaterials for spinal cord repair

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