Regenerative capacity of neural tissue scales with changes in tissue mechanics post injury

Alejandro Carnicer-Lombarte; Damiano G. Barone; Filip Wronowski; George G. Malliaras; James W. Fawcett; Kristian Franze

doi:10.1016/j.biomaterials.2023.122393

Regenerative capacity of neural tissue scales with changes in tissue mechanics post injury

Alejandro Carnicer-Lombarte^*
, Damiano G. Barone
, Filip Wronowski
, George G. Malliaras
, James W. Fawcett
, Kristian Franze^*

^*Corresponding author for this work

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

15 Citations (Scopus)

Abstract

Spinal cord injuries have devastating consequences for humans, as mammalian neurons of the central nervous system (CNS) cannot regenerate. In the peripheral nervous system (PNS), however, neurons may regenerate to restore lost function following injury. While mammalian CNS tissue softens after injury, how PNS tissue mechanics changes in response to mechanical trauma is currently poorly understood. Here we characterised mechanical rat nerve tissue properties before and after in vivo crush and transection injuries using atomic force microscopy-based indentation measurements. Unlike CNS tissue, PNS tissue significantly stiffened after both types of tissue damage. This nerve tissue stiffening strongly correlated with an increase in collagen I levels. Schwann cells, which crucially support PNS regeneration, became more motile and proliferative on stiffer substrates in vitro, suggesting that changes in tissue stiffness may play a key role in facilitating or impeding nervous system regeneration. © 2023 The Authors.

Original language	English
Article number	122393
Number of pages	12
Journal	Biomaterials
Volume	303
Online published	9 Nov 2023
DOIs	https://doi.org/10.1016/j.biomaterials.2023.122393
Publication status	Published - Dec 2023
Externally published	Yes

Funding

This work was supported by the UK Medical Research Council (MRC) and the Sackler Foundation (doctoral training grant RG70550 to AC), the UK Wellcome Trust (Translational Medicine and Therapeutics PhD Programme Fellowship 109511/Z/15/Z to DGB), the European Research Council (Consolidator Award 772426 to KF), the UK Biotechnology and Biological Sciences Research Council (Research Grant BB/N006402/1 to KF), the UK Medical Research Council (Career Development Award G1100312/1 to KF), and the Alexander von Humboldt-Foundation (Alexander von Humboldt-Professorship to KF).

Research Keywords

Crush injury
Nerve compartments
Nerve injury
Nerve stiffness
Schwann cells
Tissue mechanics

Publisher's Copyright Statement

This full text is made available under CC-BY 4.0. https://creativecommons.org/licenses/by/4.0/

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title = "Regenerative capacity of neural tissue scales with changes in tissue mechanics post injury",

abstract = "Spinal cord injuries have devastating consequences for humans, as mammalian neurons of the central nervous system (CNS) cannot regenerate. In the peripheral nervous system (PNS), however, neurons may regenerate to restore lost function following injury. While mammalian CNS tissue softens after injury, how PNS tissue mechanics changes in response to mechanical trauma is currently poorly understood. Here we characterised mechanical rat nerve tissue properties before and after in vivo crush and transection injuries using atomic force microscopy-based indentation measurements. Unlike CNS tissue, PNS tissue significantly stiffened after both types of tissue damage. This nerve tissue stiffening strongly correlated with an increase in collagen I levels. Schwann cells, which crucially support PNS regeneration, became more motile and proliferative on stiffer substrates in vitro, suggesting that changes in tissue stiffness may play a key role in facilitating or impeding nervous system regeneration. {\textcopyright} 2023 The Authors.",

keywords = "Crush injury, Nerve compartments, Nerve injury, Nerve stiffness, Schwann cells, Tissue mechanics",

author = "Alejandro Carnicer-Lombarte and Barone, \{Damiano G.\} and Filip Wronowski and Malliaras, \{George G.\} and Fawcett, \{James W.\} and Kristian Franze",

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T1 - Regenerative capacity of neural tissue scales with changes in tissue mechanics post injury

AU - Carnicer-Lombarte, Alejandro

AU - Barone, Damiano G.

AU - Wronowski, Filip

AU - Malliaras, George G.

AU - Fawcett, James W.

AU - Franze, Kristian

PY - 2023/12

Y1 - 2023/12

N2 - Spinal cord injuries have devastating consequences for humans, as mammalian neurons of the central nervous system (CNS) cannot regenerate. In the peripheral nervous system (PNS), however, neurons may regenerate to restore lost function following injury. While mammalian CNS tissue softens after injury, how PNS tissue mechanics changes in response to mechanical trauma is currently poorly understood. Here we characterised mechanical rat nerve tissue properties before and after in vivo crush and transection injuries using atomic force microscopy-based indentation measurements. Unlike CNS tissue, PNS tissue significantly stiffened after both types of tissue damage. This nerve tissue stiffening strongly correlated with an increase in collagen I levels. Schwann cells, which crucially support PNS regeneration, became more motile and proliferative on stiffer substrates in vitro, suggesting that changes in tissue stiffness may play a key role in facilitating or impeding nervous system regeneration. © 2023 The Authors.

AB - Spinal cord injuries have devastating consequences for humans, as mammalian neurons of the central nervous system (CNS) cannot regenerate. In the peripheral nervous system (PNS), however, neurons may regenerate to restore lost function following injury. While mammalian CNS tissue softens after injury, how PNS tissue mechanics changes in response to mechanical trauma is currently poorly understood. Here we characterised mechanical rat nerve tissue properties before and after in vivo crush and transection injuries using atomic force microscopy-based indentation measurements. Unlike CNS tissue, PNS tissue significantly stiffened after both types of tissue damage. This nerve tissue stiffening strongly correlated with an increase in collagen I levels. Schwann cells, which crucially support PNS regeneration, became more motile and proliferative on stiffer substrates in vitro, suggesting that changes in tissue stiffness may play a key role in facilitating or impeding nervous system regeneration. © 2023 The Authors.

KW - Crush injury

KW - Nerve compartments

KW - Nerve injury

KW - Nerve stiffness

KW - Schwann cells

KW - Tissue mechanics

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U2 - 10.1016/j.biomaterials.2023.122393

DO - 10.1016/j.biomaterials.2023.122393

M3 - RGC 21 - Publication in refereed journal

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SN - 0142-9612

VL - 303

JO - Biomaterials

JF - Biomaterials

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ER -

Regenerative capacity of neural tissue scales with changes in tissue mechanics post injury

Abstract

Funding

Research Keywords

Publisher's Copyright Statement

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