Abstract
The presence of bones around the central nervous system (CNS) provides it with highly effective physiologically crucial mechanical protection. The peripheral nervous system (PNS), in contrast, lacks this barrier. Consequently, the long held belief is that the PNS is mechanically vulnerable. On the other hand, the PNS is exposed to a variety of physiological mechanical stresses during regular daily activities. This fact prompts us to question the dogma of PNS mechanical vulnerability. As a matter of fact, impaired mechanics of PNS nerves is associated with neuropathies with the liability to mechanical stresses paralleled by significant impairment of PNS physiological functions. Our recent biomechanical integrity investigations on nerve fibers from wild-type and neuropathic mice lend strong support in favor of natural mechanical protection of the PNS and demonstrate a key role of Schwann cells (SCs) therein. Moreover, recent works point out that SCs can sense mechanical properties of their microenvironment and the evidence is growing that SCs mechanosensitivity is important for PNS development and myelination. Hence, SCs exhibit mechanical strength necessary for PNS mechanoprotection as well as mechanosensitivity necessary for PNS development and myelination. This mini review reflects on the intriguing dual ability of SCs and implications for PNS physiology and pathophysiology.
Highlights
The general assumption that the peripheral nervous system (PNS) is prone to mechanical injuries is based on the absence of a formidable physical barrier in the PNS that presents the skull and bony vertebrae in the central nervous system (CNS)
Unlike oligodendrocytes and their associated axons in the CNS, Schwann cells (SCs) and axons in the PNS are enveloped in a basal lamina, a specialized form of extracellular matrices (ECMs) (Colognato et al, 2005)
A change of the basal lamina structural arrangement from a networked to a parallel orientation pattern, as observed in neuropathic Pmp22−/− mice, is associated with a loss of the biomechanical integrity of nerve fibers; Pmp22−/− mice are among the animal models to study the relationship between peripheral myelin protein 22 (PMP22) and the pathogenesis of hereditary PNS neuropathies (Adlkofer et al, 1995)
Summary
The general assumption that the peripheral nervous system (PNS) is prone to mechanical injuries is based on the absence of a formidable physical barrier in the PNS that presents the skull and bony vertebrae in the central nervous system (CNS). The presence of a myelin sheath around nerve fibers is one of the critical factors ensuring a high conduction velocity. Fascicles in turn are joined together with a blood supply and fatty tissue within yet another layer known as the epineurium Unlike oligodendrocytes and their associated axons in the CNS, Schwann cells (SCs) and axons in the PNS are enveloped in a basal lamina, a specialized form of ECM (Colognato et al, 2005). The role of the basal lamina in providing mechanical strength to PNS nerves has recently been demonstrated (Rosso et al, 2014) and will be discussed in the present review. Mechanosensitivity strongly impacts SCs shape, migration, adhesion and mechanics (Rosso et al, 2017) and is assumed to play key roles in PNS development, maintenance, myelination and regeneration as discussed here. Unlike the CNS which certainly received some attention so far, the importance of mechanosensitivity for the PNS is just beginning to be recognized (Koch et al, 2012; Athamneh et al, 2015; Poitelon et al, 2016; Urbanski et al, 2016; Rosso et al, 2017)
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