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A novel perspective on neuron study: damaging and promoting effects in different neurons induced by mechanical stress

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Abstract

A growing volume of experimental evidence demonstrates that mechanical stress plays a significant role in growth, proliferation, apoptosis, gene expression, electrophysiological properties and many other aspects of neurons. In this review, first, the mechanical microenvironment and properties of neurons under in vivo conditions are introduced and analyzed. Second, research works in recent decades on the effects of different mechanical forces, especially compression and tension, on various neurons, including dorsal root ganglion neurons, retinal ganglion cells, cerebral cortex neurons, hippocampus neurons, neural stem cells, and other neurons, are summarized. Previous research results demonstrate that mechanical stress can not only injure neurons by damaging their morphology, impacting their electrophysiological characteristics and gene expression, but also promote neuron self-repair. Finally, some future perspectives in neuron research are discussed.

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References

  • Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, Begley DJ (2010) Structure and function of the blood–brain barrier. Neurobiol Dis 37(1):13–25

    Article  Google Scholar 

  • Ahmed WW, Saif TA (2014) Active transport of vesicles in neurons is modulated by mechanical tension. Sci Rep. doi:10.1038/srep04481

  • Ahmed SM, Rzigalinski BA, Willoughby KA, Sitterding HA, Ellis EF (2000) Stretch-induced injury alters mitochondrial membrane potential and cellular ATP in cultured astrocytes and neurons. J Neurochem 74(5):1951–1960

    Article  Google Scholar 

  • Ahmed F, Chaudhary P, Sharma SC (2001) Effects of increased intraocular pressure on rat retinal ganglion cells. Int J Dev Neurosci 19(2):209–218

    Article  Google Scholar 

  • Aihara M, Chen Y-N, Uchida S, Nakayama M, Araie M (2014) Hyperbaric pressure and increased susceptibility to glutamate toxicity in retinal ganglion cells in vitro. Mol Vis 20:606–615

    Google Scholar 

  • Anava S, Greenbaum A, Ben Jacob E, Hanein Y, Ayali A (2009) The regulative role of neurite mechanical tension in network development. Biophys J 96(4):1661–1670

    Article  Google Scholar 

  • Arimura N et al (2005) Phosphorylation by Rho kinase regulates CRMP-2 activity in growth cones. Mol Cell Biol 25(22):9973–9984

    Article  Google Scholar 

  • Arundine M, Aarts M, Lau A, Tymianski M (2004) Vulnerability of central neurons to secondary insults after in vitro mechanical stretch. J Neurosci 24(37):8106–8123

    Article  Google Scholar 

  • Bareyre FM (2008a) Neuronal repair and replacement in spinal cord injury. J Neurol Sci 265(1):63–72

    Article  Google Scholar 

  • Bareyre FM (2008b) Neuronal repair and replacement in spinal cord injury. J Neurol Sci 265(1–2):63–72

    Article  Google Scholar 

  • Bormann P, Zumsteg VM, Roth LWA, Reinhard E (1998) Target contact regulates GAP-43 and alpha-tubulin mRNA levels in regenerating retinal ganglion cells. J Neurosci Res 52(4):405–419

    Article  Google Scholar 

  • Bray D (1979) Mechanical tension produced by nerve-cells in tissue-culture. J Cell Sci 37(JUN):391–410

    Google Scholar 

  • Bray D (1984) Axonal growth in response to experimentally applied mechanical tension. Dev Biol 102(2):379–389

    Article  Google Scholar 

  • Bridges D, Thompson SWN, Rice ASC (2001) Mechanism in neuropathic pain. Br J Anaesth 87(1):12–26

    Article  Google Scholar 

  • Cater HL, Gitterman D, Davis SM, Benham CD, Morrison B III, Sundstrom LE (2007) Stretch-induced injury in organotypic hippocampal slice cultures reproduces in vivo post-traumatic neurodegeneration: role of glutamate receptors and voltage-dependent calcium channels. J Neurochem 101(2):434–447

    Article  Google Scholar 

  • Chang Y-J, Tsai C-J, Tseng F-G, Chen T-J, Wang T-W (2013) Micropatterned stretching system for the investigation of mechanical tension on neural stem cells behavior. Nanomed Nanotechnol Biol Med 9(3):345–355

    Article  Google Scholar 

  • Chen L-J, Wang Y-J, Chen J-R, Tseng G-F (2015) NMDA receptor triggered molecular cascade underlies compression-induced rapid dendritic spine plasticity in cortical neurons. Exp Neurol 266:86–98

    Article  Google Scholar 

  • Colicos MA, Dixon CE, Dash PK (1996) Delayed, selective neuronal death following experimental cortical impact injury in rats: possible role in memory deficits. Brain Res 739(1–2):111–119

    Article  Google Scholar 

  • Dennerll TJ, Joshi HC, Steel VL, Buxbaum RE, Heidemann SR (1988) Tension and compression in the cytoskeleton of PC-12 neurites II -quantitative measurements. J Cell Biol 107(2):665–674

    Article  Google Scholar 

  • Dennerll TJ, Lamoureux P, Buxbaum RE, Heidemann SR (1989) The cytomechanics of axonal elongation and retraction. J Cell Biol 109(6):3073–3083

  • Esfandiari L, Paff M, Tang WC (2012) Initial studies of mechanical compression on neurogenesis with neonatal neural stem cells. Nanomed Nanotechnol Biol Med 8(4):415–418

    Article  Google Scholar 

  • Fan N, Donnelly DF, LaMotte RH (2011a) Chronic compression of mouse dorsal root ganglion alters voltage-gated sodium and potassium currents in medium-sized dorsal root ganglion neurons. J Neurophysiol 106(6):3067–3072

    Article  Google Scholar 

  • Fan N, Sikand P, Donnelly DF, Ma C, LaMotte RH (2011b) Increased Na+ and K+ currents in small mouse dorsal root ganglion neurons after ganglion compression. J Neurophysiol 106(1):211–218

    Article  Google Scholar 

  • Ge S, C-h Y, K-s H, G-l M, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54(4):559–566

    Article  Google Scholar 

  • Geddes DM, Cargill RS, LaPlaca MC (2003a) Mechanical stretch to neurons results in a strain rate and magnitude-dependent increase in plasma membrane permeability. J Neurotrauma 20(10):1039–1049

    Article  Google Scholar 

  • Geddes DM, LaPlaca MC, Cargill RS (2003b) Susceptibility of hippocampal neurons to mechanically induced injury. Exp Neurol 184(1):420–427

    Article  Google Scholar 

  • Hanein Y, Tadmor O, Anava S, Ayali A (2011) Neuronal soma migration is determined by neurite tension. Neuroscience 172:572–579

    Article  Google Scholar 

  • Heidemann SR, Buxbaum RE (1990) Tension as a regulator and integrator of axonal growth. Cell Motil Cytoskelet 17(1):6–10

    Article  Google Scholar 

  • Heidemann SR, Buxbaum RE (1994) Mechanical tension as a regulator of axonal development. Neurotoxicology 15(1):95–107

    Google Scholar 

  • Jeon KJ et al (2014) Combined effects of flow-induced shear stress and micropatterned surface morphology on neuronal differentiation of human mesenchymal stem cells. J Biosci Bioeng 117(2):242–247

    Article  Google Scholar 

  • Ji JZ et al (2005) Effects of elevated intraocular pressure on mouse retinal ganglion cells. Vision Res 45(2):169–179

    Article  Google Scholar 

  • Kandel ER, Schwartz JH, Jessell TM (2000) Principles of neural science, vol 4. McGraw-Hill, New York

    Google Scholar 

  • Kim IA et al (2006) Effects of mechanical stimuli and microfiber-based substrate on neurite outgrowth and guidance. J Biosci Bioeng 101(2):120–126

    Article  Google Scholar 

  • Koch D, Rosoff WJ, Jiang J, Geller HM, Urbach JS (2012) Strength in the periphery: growth cone biomechanics and substrate rigidity response in peripheral and central nervous system neurons. Biophys J 102(3):452–460

    Article  Google Scholar 

  • Lamoureux P, Buxbaum RE, Heidemann SR (1989) Direct evidence that growth cones pull. Nature 340(6229):159–162

    Article  Google Scholar 

  • Lamoureux P, Zheng J, Buxbaum RE, Heidemann SR (1992) A cytomechanical investigation of neurite growth on different culture surfaces. J Cell Biol 118(3):655–661

    Article  Google Scholar 

  • Lamoureux P, Ruthel G, Buxbaum RE, Heidemann SR (2002) Mechanical tension can specify axonal fate in hippocampal neurons. J Cell Biol 159(3):499–508

    Article  Google Scholar 

  • LaPlaca MC, Prado GR (2010) Neural mechanobiology and neuronal vulnerability to traumatic loading. J Biomech 43(1):71–78

    Article  Google Scholar 

  • Lee JK, Lu S, Madhukar A (2010) Real-time dynamics of Ca2+, Caspase-3/7, and morphological changes in retinal ganglion cell apoptosis under elevated pressure. PLoS One. doi:10.1371/journal.pone.0013437

  • Li X, Chu J, Wang A, Zhu Y, Chu WK, Yang L, Li S (2011) Uniaxial mechanical strain modulates the differentiation of neural crest stem cells into smooth muscle lineage on micropatterned surfaces. PLoS One. doi:10.1371/journal.pone.0026029

  • Li X, Chu JS, Yang L, Li S (2012) Anisotropic effects of mechanical strain on neural crest stem cells. Ann Biomed Eng 40(3):598–605

    Article  MathSciNet  Google Scholar 

  • Lin G, Wu VI, Hainley RE, Flanagan LA, Monuki ES, Tang WC (2004) Development of a MEMS microsystem to study the effect of mechanical tension on cerebral cortex neurogenesis. In: Conference proceedings: annual international conference of the IEEE engineering in medicine and biology society IEEE engineering in medicine and biology society annual conference, vol 4, pp 2607–2610

  • Lindqvist N, Liu Q, Zajadacz J, Franze K, Reichenbach A (2010) Retinal glial (muller) cells: sensing and responding to tissue stretch. Invest Ophthalmol Vis Sci 51(3):1683–1690

    Article  Google Scholar 

  • Lusardi TA, Smith DH, Wolf JA, Meaney DF (2003) The separate roles of calcium and mechanical forces in mediating cell death in mechanically injured neurons. Biorheology 40(1–3):401–409

    Google Scholar 

  • Ma C, LaMotte RH (2007) Multiple sites for generation of ectopic spontaneous activity in neurons of the chronically compressed dorsal root ganglion. J Neurosci 27(51):14059–14068

    Article  Google Scholar 

  • Maxwell WL, Islam MN, Graham DI, Gennarelli TA (1994) A qualitative and quantitative-analysis of the response of the retinal ganglion-cell soma after stretch injury to the adult guinea-pig optic-nerve. J Neurocytol 23(6):379–392

    Article  Google Scholar 

  • Meseke M, Foerster E (2013) A 3D-matrigel/microbead assay for the visualization of mechanical tractive forces at the neurite-substrate interface of cultured neurons. J Biomed Mater Res Part A 101(6):1726–1733

    Article  Google Scholar 

  • Mueller BK, Mack H, Teusch N (2005) Rho kinase, a promising drug target for neurological disorders. Nat Rev Drug Discov 4(5):387–398

    Article  Google Scholar 

  • Nakadate H, Aomura S, Zhang Y, Kakuta A, Fujiwara S (2010) Strain magnitude and strain rate influence stretch-induced injury of pc12 cells. In: Lim CT, Goh JCH (eds) IFMBE Proceedings of the 6th world congress of biomechanics, vol 31, pp 1091–1094

  • Paez-Gonzalez P et al (2011) Ank3-dependent SVZ niche assembly is required for the continued production of new neurons. Neuron 71(1):61–75

    Article  Google Scholar 

  • Pathak MM et al (2014) Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells. Proc Natl Acad Sci 111(45):16148–16153

    Article  Google Scholar 

  • Pfister BJ, Iwata A, Meaney DF, Smith DH (2004) Extreme stretch growth of integrated axons. J Neurosci 24(36):7978–7983

  • Pittenger C, Kandel ER (2003) In search of general mechanisms for long-lasting plasticity: aplysia and the hippocampus. Philos Trans R Soc Lond Ser B Biol Sci 358(1432):757–763

    Article  Google Scholar 

  • Quan X, Guo K, Wang Y, Huang L, Chen B, Ye Z, Luo Z (2014) Mechanical compression insults induce nanoscale changes of membrane-skeleton arrangement which could cause apoptosis and necrosis in dorsal root ganglion neurons. Biosci Biotechnol Biochem 78(10):1631–1639

    Article  Google Scholar 

  • Rangappa N, Romero A, Nelson KD, Eberhart RC, Smith GM (2000) Laminin-coated poly(L-lactide) filaments induce robust neurite growth while providing directional orientation. J Biomed Mater Res 51(4):625–634

    Article  Google Scholar 

  • Rousseau V, Sabel BA (2001) Restoration of vision IV: role of compensatory soma swelling of surviving retinal ganglion cells in recovery of vision after optic nerve crush. Restor Neurol Neurosci 18(4):177–189

    Google Scholar 

  • Rydevik BL (1992) The effects of compression on the physiology of nerve roots. J Manip Physiol Ther 15(1):62–66

    Google Scholar 

  • Shi RY, Asano T, Vining NC, Blight AR (2000) Control of membrane sealing in injured mammalian spinal cord axons. J Neurophysiol 84(4):1763–1769

    Google Scholar 

  • Shiraishi T, Suzuki K, Morishita S, Kanno H, Asme (2010) Control of apoptosis and differentiation of cultured neural stem cells by mechanical vibration. Imece2009: proceedings of the ASME international mechanical engineering congress and exposition, vol 2

  • Sigal IA, Ethier CR (2009) Biomechanics of the optic nerve head. Exp Eye Res 88(4):799–807

    Article  Google Scholar 

  • Smith DH (2009) Stretch growth of integrated axon tracts: extremes and exploitations. Prog Neurobiol 89(3):231–239

    Article  Google Scholar 

  • Steketee MB et al (2014) Regulation of Intrinsic axon growth ability at retinal ganglion cell growth cones. Invest Ophthalmol Vis Sci 55(7):4369–4377

    Article  Google Scholar 

  • Suter DM, Miller KE (2011) The emerging role of forces in axonal elongation. Prog Neurobiol 94(2):91–101

    Article  Google Scholar 

  • Suzuki K, Morishita S, Shiraishi T, Kanno H, Asme (2009) Effects of mechanical vibration on proliferation and differentiation of neural stem cells. In: Proceedings of the ASME international mechanical engineering congress and exposition 2008, vol 2

  • Tan ZY, Donnelly DF, LaMotte RH (2006) Effects of a chronic compression of the dorsal root ganglion on voltage-gated Na+ and K+ currents in cutaneous afferent neurons. J Neurophysiol 95(2):1115–1123

    Article  Google Scholar 

  • Taylor Z, Miller K (2004) Reassessment of brain elasticity for analysis of biomechanisms of hydrocephalus. J Biomech 37(8):1263–1269

    Article  Google Scholar 

  • Teruel MN, Meyer T (1997) Electroporation-induced formation of individual calcium entry sites in the cell body and processes of adherent cells. Biophys J 73(4):1785–1796

    Article  Google Scholar 

  • Topp KS, Boyd BS (2006) Structure and biomechanics of peripheral nerves: nerve responses to physical stresses and implications for physical therapist practice. Phys Ther 86(1):92–109

    Google Scholar 

  • Urcola JH, Hernandez M, Vecino E (2006) Three experimental glaucoma models in rats: comparison of the effects of intraocular pressure elevation on retinal ganglion cell size and death. Exp Eye Res 83(2):429–437

    Article  Google Scholar 

  • VanEssen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385(6614):313–318

    Article  Google Scholar 

  • Wang H et al (2005) Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol 25(9):1817–1823

    Article  Google Scholar 

  • Winn HR (2004) Youmans neurological surgery. WB Saunders, New York

    Google Scholar 

  • Xia J, Lim JC, Lu W, Beckel JM, Macarak EJ, Laties AM, Mitchell CH (2012) Neurons respond directly to mechanical deformation with pannexin-mediated ATP release and autostimulation of P2X7 receptors. J Physiol Lond 590(10):2285–2304

    Article  Google Scholar 

  • Ye Z, Wang Y, Quan X, Li J, Hu X, Huang J, Luo Z (2012) Effects of mechanical force on cytoskeleton structure and calpain-induced apoptosis in rat dorsal root ganglion neurons in vitro. PLoS One. doi:10.1371/journal.pone.0052183

  • Zhang Y, Wang Y-H, Ge H-Y, Arendt-Nielsen L, Wang R, Yue S-W (2008) A transient receptor potential vanilloid 4 contributes to mechanical allodynia following chronic compression of dorsal root ganglion in rats. Neurosci Lett 432(3):222–227

    Article  Google Scholar 

  • Zhang Y, Huai J, Wang Y, Wang Y, Yue S (2011) Increased gene and protein expressions of the transient receptor potential vanilloid receptor 4 following sustained pure mechanical pressure on rat dorsal root ganglion neurons. Neural Regen Res 6(35):2739–2745

    Google Scholar 

  • Zheng J, Lamoureux P, Santiago V, Dennerll T, Buxbaum RE, Heidemann SR (1991) Tensile regulation of axonal elongation and initiation. J Neurosci 11(4):1117–1125

    Google Scholar 

  • Zheng J, Buxbaum RE, Heidemann SR (1993) Investigation of microtubule assembly and organization accompanying tension-induced neurite initiation. J Cell Sci 104:1239–1250

    Google Scholar 

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Acknowledgments

This research was supported by the National Key Basic Research Project (Project “973”) (2014CB541600) and the Fundamental Research Funds for the Central Universities (2015CDJZR) and funded by 2014 Chongqing University Postgraduates’ Innovation Project (Project Number:CYS14004).

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Correspondence to Yazhou Wang.

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Wang, Y., Wang, W., Li, Z. et al. A novel perspective on neuron study: damaging and promoting effects in different neurons induced by mechanical stress. Biomech Model Mechanobiol 15, 1019–1027 (2016). https://doi.org/10.1007/s10237-015-0743-4

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  • DOI: https://doi.org/10.1007/s10237-015-0743-4

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