Abstract
Although many details remain still elusive, it became increasingly evident in recent years that mechanosensing of microenvironmental biophysical cues and subsequent mechanotransduction are strongly involved in the regulation of neuronal cell development and functioning. This review gives an overview about the current understanding of brain and neuronal cell mechanobiology and how it impacts on neurogenesis, neuronal migration, differentiation, and maturation. We will focus particularly on the events in the cell/microenvironment interface and the decisive extracellular matrix (ECM) parameters (i.e. rigidity and nanometric spatial organisation of adhesion sites) that modulate integrin adhesion complex-based mechanosensing and mechanotransductive signalling. It will also be outlined how biomaterial approaches mimicking essential ECM features help to understand these processes and how they can be used to control and guide neuronal cell behaviour by providing appropriate biophysical cues. In addition, principal biophysical methods will be highlighted that have been crucial for the study of neuronal mechanobiology.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abrams GA, Goodman SL, Nealey PF, Franco M, Murphy CJ (2000) Nanoscale topography of the basement membrane underlying the corneal epithelium of the rhesus macaque. Cell Tissue Res 299:39–46
Alcaraz J, Otero J, Jorba I, Navajas D (2018) Bidirectional mechanobiology between cells and their local extracellular matrix probed by atomic force microscopy. Semin Cell Dev Biol, Application of Atomic Force Microscopy in cell biology 73:71–81. https://doi.org/10.1016/j.semcdb.2017.07.020
Amin L, Ercolini E, Ban J, Torre V (2013) Comparison of the force exerted by hippocampal and DRG growth cones. PLoS One 8:e73025. https://doi.org/10.1371/journal.pone.0073025
Anton ES, Kreidberg JA, Rakic P (1999) Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22:277–289
Antonovaite N, Beekmans SV, Hol EM, Wadman WJ, Iannuzzi D (2018) Regional variations in stiffness in live mouse brain tissue determined by depth-controlled indentation mapping. Sci Rep 8:12517. https://doi.org/10.1038/s41598-018-31035-y
Arnold M, Cavalcanti-Adam EA, Glass R, Blümmel J, Eck W, Kantlehner M, Kessler H, Spatz JP (2004) Activation of integrin function by nanopatterned adhesive interfaces. Chemphyschem 5:383–388. https://doi.org/10.1002/cphc.200301014
Athamneh AIM, Suter DM (2015) Quantifying mechanical force in axonal growth and guidance. Front Cell Neurosci 9. https://doi.org/10.3389/fncel.2015.00359
Baek J, Cho S-Y, Kang H, Ahn H, Jung W-B, Cho Y, Lee E, Cho S-W, Jung H-T, Im SG (2018) Distinct mechanosensing of human neural stem cells on extremely limited anisotropic cellular contact. ACS Appl Mater Interfaces. https://doi.org/10.1021/acsami.8b10171
Baek J, Jung W-B, Cho Y, Lee E, Yun G-T, Cho S-Y, Jung H-T, Im SG (2019) Facile fabrication of high-definition hierarchical wrinkle structures for investigating the geometry-sensitive fate commitment of human neural stem cells. ACS Appl Mater Interfaces 11:17247–17255. https://doi.org/10.1021/acsami.9b03479
Balgude AP, Yu X, Szymanski A, Bellamkonda RV (2001) Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures. Biomaterials 22:1077–1084
Banerjee A, Arha M, Choudhary S, Ashton RS, Bhatia SR, Schaffer DV, Kane RS (2009) The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells. Biomaterials 30:4695–4699. https://doi.org/10.1016/j.biomaterials.2009.05.050
Barnes JM, Przybyla L, Weaver VM (2017) Tissue mechanics regulate brain development, homeostasis and disease. J Cell Sci 130:71–82. https://doi.org/10.1242/jcs.191742
Barnes JM, Kaushik S, Bainer RO, Sa JK, Woods EC, Kai F, Przybyla L, Lee M, Lee HW, Tung JC, Maller O, Barrett AS, Lu KV, Lakins JN, Hansen KC, Obernier K, Alvarez-Buylla A, Bergers G, Phillips JJ, Nam D-H, Bertozzi CR, Weaver VM (2018) A tension-mediated glycocalyx–integrin feedback loop promotes mesenchymal-like glioblastoma. Nat Cell Biol 20:1203. https://doi.org/10.1038/s41556-018-0183-3
Barriga EH, Franze K, Charras G, Mayor R (2018) Tissue stiffening coordinates morphogenesis by triggering collective cell migration in vivo. Nature 554:523–527. https://doi.org/10.1038/nature25742
Bass MD, Roach KA, Morgan MR, Mostafavi-Pour Z, Schoen T, Muramatsu T, Mayer U, Ballestrem C, Spatz JP, Humphries MJ (2007) Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J Cell Biol 177:527–538. https://doi.org/10.1083/jcb.200610076
Béduer A, Vieu C, Arnauduc F, Sol J-C, Loubinoux I, Vaysse L (2012) Engineering of adult human neural stem cells differentiation through surface micropatterning. Biomaterials 33:504–514. https://doi.org/10.1016/j.biomaterials.2011.09.073
Betz T, Koch D, Lu Y-B, Franze K, Käs JA (2011) Growth cones as soft and weak force generators. Proc Natl Acad Sci 108:13420–13425. https://doi.org/10.1073/pnas.1106145108
Bikbaev A, Frischknecht R, Heine M (2015) Brain extracellular matrix retains connectivity in neuronal networks. Sci Rep 5:14527. https://doi.org/10.1038/srep14527
Bonneh-Barkay D, Wiley CA (2009) Brain extracellular matrix in neurodegeneration. Brain Pathol 19:573–585. https://doi.org/10.1111/j.1750-3639.2008.00195.x
Borghi F, Scaparra B, Paternoster C, Milani P, Podestà A (2018) Electrostatic double-layer interaction at the surface of rough cluster-assembled films: the case of nanostructured zirconia. Langmuir 34:10230–10242. https://doi.org/10.1021/acs.langmuir.8b01387
Bosch M, Castro J, Saneyoshi T, Matsuno H, Sur M, Hayashi Y (2014) Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron 82:444–459. https://doi.org/10.1016/j.neuron.2014.03.021
Bridgman PC, Dave S, Asnes CF, Tullio AN, Adelstein RS (2001) Myosin IIB is required for growth cone motility. J Neurosci 21:6159–6169. https://doi.org/10.1523/JNEUROSCI.21-16-06159.2001
Bugnicourt G, Brocard J, Nicolas A, Villard C (2014) Nanoscale surface topography reshapes neuronal growth in culture. Langmuir 30:4441–4449. https://doi.org/10.1021/la5001683
Campos LS, Leone DP, Relvas JB, Brakebusch C, Fässler R, Suter U, ffrench-Constant C (2004) Beta1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 131:3433–3444. https://doi.org/10.1242/dev.01199
Cao X, Pfaff SL, Gage FH (2008) YAP regulates neural progenitor cell number via the TEA domain transcription factor. Genes Dev 22:3320–3334. https://doi.org/10.1101/gad.1726608
Capitanio M, Pavone FS (2013) Interrogating biology with force: single molecule high-resolution measurements with optical tweezers. Biophys J 105:1293–1303. https://doi.org/10.1016/j.bpj.2013.08.007
Carisey A, Tsang R, Greiner AM, Nijenhuis N, Heath N, Nazgiewicz A, Kemkemer R, Derby B, Spatz J, Ballestrem C (2013) Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner. Curr Biol 23:271–281. https://doi.org/10.1016/j.cub.2013.01.009
Case LB, Waterman CM (2015) Integration of actin dynamics and cell adhesion by a three-dimensional, mechanosensitive molecular clutch. Nat Cell Biol 17:955–963. https://doi.org/10.1038/ncb3191
Case LB, Baird MA, Shtengel G, Campbell SL, Hess HF, Davidson MW, Waterman CM (2015) Molecular mechanism of vinculin activation and nanoscale spatial organization in focal adhesions. Nat Cell Biol 17:880–892. https://doi.org/10.1038/ncb3180
Cellot G, Toma FM, Varley ZK, Laishram J, Villari A, Quintana M, Cipollone S, Prato M, Ballerini L (2011) Carbon nanotube scaffolds tune synaptic strength in cultured neural circuits: novel frontiers in nanomaterial–tissue interactions. J Neurosci 31:12945–12953. https://doi.org/10.1523/JNEUROSCI.1332-11.2011
Chan CE, Odde DJ (2008) Traction dynamics of filopodia on compliant substrates. Science 322:1687–1691. https://doi.org/10.1126/science.1163595
Changede R, Sheetz M (2017) Integrin and cadherin clusters: a robust way to organize adhesions for cell mechanics. BioEssays 39. https://doi.org/10.1002/bies.201600123
Changede R, Xu X, Margadant F, Sheetz MP (2015) Nascent integrin adhesions form on all matrix rigidities after integrin activation. Dev Cell 35:614–621. https://doi.org/10.1016/j.devcel.2015.11.001
Changede R, Cai H, Wind SJ, Sheetz MP, (2019) Integrin nanoclusters can bridge thin matrix fibres to form cell-matrix adhesions. Nat Mater 1–10. https://doi.org/10.1038/s41563-019-0460-y
Chavis P, Westbrook G (2001) Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411:317–321. https://doi.org/10.1038/35077101
Chen L, Liao G, Waclaw RR, Burns KA, Linquist D, Campbell K, Zheng Y, Kuan C-Y (2007) Rac1 controls the formation of midline commissures and the competency of tangential migration in ventral telencephalic neurons. J Neurosci 27:3884–3893. https://doi.org/10.1523/JNEUROSCI.3509-06.2007
Chen L, Melendez J, Campbell K, Kuan C-Y, Zheng Y (2009) Rac1 deficiency in the forebrain results in neural progenitor reduction and microcephaly. Dev Biol 325:162–170. https://doi.org/10.1016/j.ydbio.2008.10.023
Chen W, Shao Y, Li X, Zhao G, Fu J (2014) Nanotopographical surfaces for stem cell fate control: engineering mechanobiology from the bottom. Nano Today 9:759–784. https://doi.org/10.1016/j.nantod.2014.12.002
Chen Y, Lee H, Tong H, Schwartz M, Zhu C (2017) Force regulated conformational change of integrin αVβ3. Matrix Biol 60–61:70–85. https://doi.org/10.1016/j.matbio.2016.07.002
Chen W, Han S, Qian W, Weng S, Yang H, Sun Y, Villa-Diaz LG, Krebsbach PH, Fu J (2018) Nanotopography regulates motor neuron differentiation of human pluripotent stem cells. Nanoscale 10:3556–3565. https://doi.org/10.1039/c7nr05430k
Cheng C-M, LeDuc PR, Lin Y-W (2011) Localized bimodal response of neurite extensions and structural proteins in dorsal-root ganglion neurons with controlled polydimethylsiloxane substrate stiffness. J Biomech 44:856–862. https://doi.org/10.1016/j.jbiomech.2010.12.006
Choi CK, Vicente-Manzanares M, Zareno J, Whitmore LA, Mogilner A, Horwitz AR (2008) Actin and alpha-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat Cell Biol 10:1039–1050. https://doi.org/10.1038/ncb1763
Christ AF, Franze K, Gautier H, Moshayedi P, Fawcett J, Franklin RJM, Karadottir RT, Guck J (2010) Mechanical difference between white and gray matter in the rat cerebellum measured by scanning force microscopy. J Biomech 43:2986–2992. https://doi.org/10.1016/j.jbiomech.2010.07.002
Ciobanasu C, Faivre B, Le Clainche C (2014) Actomyosin-dependent formation of the mechanosensitive talin-vinculin complex reinforces actin anchoring. Nat Commun 5:3095. https://doi.org/10.1038/ncomms4095
Cojoc D, Difato F, Ferrari E, Shahapure RB, Laishram J, Righi M, Fabrizio EMD, Torre V (2007) Properties of the force exerted by filopodia and lamellipodia and the involvement of cytoskeletal components. PLoS One 2:e1072. https://doi.org/10.1371/journal.pone.0001072
Da Silva JS, Medina M, Zuliani C, Di Nardo A, Witke W, Dotti CG (2003) RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability. J Cell Biol 162:1267–1279. https://doi.org/10.1083/jcb.200304021
Dai J, Sheetz MP (1995) Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers. Biophys J 68:988–996. https://doi.org/10.1016/S0006-3495(95)80274-2
De Vlaminck I, Dekker C (2012) Recent advances in magnetic tweezers. Annu Rev Biophys 41:453–472. https://doi.org/10.1146/annurev-biophys-122311-100544
del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP (2009) Stretching single talin rod molecules activates vinculin binding. Science 323:638–641. https://doi.org/10.1126/science.1162912
Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell WD, McKerracher L (2002) Rho signaling pathway targeted to promote spinal cord repair. J Neurosci 22:6570–6577
Dityatev A, Schachner M, Sonderegger P (2010a) The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nat Rev Neurosci 11:735–746. https://doi.org/10.1038/nrn2898
Dityatev A, Seidenbecher CI, Schachner M (2010b) Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci 33:503–512. https://doi.org/10.1016/j.tins.2010.08.003
Dufrêne YF, Evans E, Engel A, Helenius J, Gaub HE, Müller DJ (2011) Five challenges to bringing single-molecule force spectroscopy into living cells. Nat Methods 8:123–127. https://doi.org/10.1038/nmeth0211-123
Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES (2000) Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 27:33–44
Elkin BS, Azeloglu EU, Costa KD, Morrison B (2007) Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation. J Neurotrauma 24:812–822. https://doi.org/10.1089/neu.2006.0169
Elosegui-Artola A, Oria R, Chen Y, Kosmalska A, Pérez-González C, Castro N, Zhu C, Trepat X, Roca-Cusachs P (2016) Mechanical regulation of a molecular clutch defines force transmission and transduction in response to matrix rigidity. Nat Cell Biol 18:540–548. https://doi.org/10.1038/ncb3336
Fabbro A, Villari A, Laishram J, Scaini D, Toma FM, Turco A, Prato M, Ballerini L (2012) Spinal cord explants use carbon nanotube interfaces to enhance neurite outgrowth and to fortify synaptic inputs. ACS Nano 6:2041–2055. https://doi.org/10.1021/nn203519r
Falleroni F, Torre V, Cojoc D (2018) Cell mechanotransduction with piconewton forces applied by optical tweezers. Front Cell Neurosci 12:130. https://doi.org/10.3389/fncel.2018.00130
Ferrari A, Cecchini M, Serresi M, Faraci P, Pisignano D, Beltram F (2010) Neuronal polarity selection by topography-induced focal adhesion control. Biomaterials 31:4682–4694. https://doi.org/10.1016/j.biomaterials.2010.02.032
Ferrari A, Cecchini M, Dhawan A, Micera S, Tonazzini I, Stabile R, Pisignano D, Beltram F (2011) Nanotopographic control of neuronal polarity. Nano Lett 11:505–511. https://doi.org/10.1021/nl103349s
Ferraris GMS, Schulte C, Buttiglione V, De Lorenzi V, Piontini A, Galluzzi M, Podestà A, Madsen CD, Sidenius N (2014) The interaction between uPAR and vitronectin triggers ligand-independent adhesion signalling by integrins. EMBO J 33:2458–2472. https://doi.org/10.15252/embj.201387611
Fietz SA, Lachmann R, Brandl H, Kircher M, Samusik N, Schröder R, Lakshmanaperumal N, Henry I, Vogt J, Riehn A, Distler W, Nitsch R, Enard W, Pääbo S, Huttner WB (2012) Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal. Proc Natl Acad Sci 109:11836–11841. https://doi.org/10.1073/pnas.1209647109
Flanagan LA, Rebaza LM, Derzic S, Schwartz PH, Monuki ES (2006) Regulation of human neural precursor cells by laminin and integrins. J Neurosci Res 83:845–856. https://doi.org/10.1002/jnr.20778
Flynn KC (2013) The cytoskeleton and neurite initiation. Bioarchitecture 3:86–109
Fournier AE, Takizawa BT, Strittmatter SM (2003) Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 23:1416–1423. https://doi.org/10.1523/JNEUROSCI.23-04-01416.2003
Franze K, Janmey PA, Guck J (2013) Mechanics in neuronal development and repair. Annu Rev Biomed Eng 15:227–251. https://doi.org/10.1146/annurev-bioeng-071811-150045
Fuhs T, Reuter L, Vonderhaid I, Claudepierre T, Käs JA (2013) Inherently slow and weak forward forces of neuronal growth cones measured by a drift-stabilized atomic force microscope. Cytoskeleton 70:44–53. https://doi.org/10.1002/cm.21080
Gasiorowski JZ, Murphy CJ, Nealey PF (2013) Biophysical cues and cell behavior: the big impact of little things. Annu Rev Biomed Eng 15:155–176. https://doi.org/10.1146/annurev-bioeng-071811-150021
Gauthier NC, Roca-Cusachs P (2018) Mechanosensing at integrin-mediated cell–matrix adhesions: from molecular to integrated mechanisms. Curr Opin Cell Biol 50:20–26. https://doi.org/10.1016/j.ceb.2017.12.014
Gavara N (2017) A beginner’s guide to atomic force microscopy probing for cell mechanics. Microsc Res Tech 80:75–84. https://doi.org/10.1002/jemt.22776
Geissler M, Gottschling C, Aguado A, Rauch U, Wetzel CH, Hatt H, Faissner A (2013) Primary hippocampal neurons, which lack four crucial extracellular matrix molecules, display abnormalities of synaptic structure and function and severe deficits in perineuronal net formation. J Neurosci 33:7742–7755. https://doi.org/10.1523/JNEUROSCI.3275-12.2013
Georges PC, Miller WJ, Meaney DF, Sawyer ES, Janmey PA (2006) Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys J 90:3012–3018. https://doi.org/10.1529/biophysj.105.073114
Gertz CC, Leach MK, Birrell LK, Martin DC, Feldman EL, Corey JM (2010) Accelerated neuritogenesis and maturation of primary spinal motor neurons in response to nanofibers. Dev Neurobiol 70:589–603. https://doi.org/10.1002/dneu.20792
Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M, Yang MT, McLean MA, Sligar SG, Chen CS, Ha T, Schwartz MA (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466:263–266. https://doi.org/10.1038/nature09198
Green HJ, Brown NH (2019) Integrin intracellular machinery in action. Exp Cell Res 378:226–231. https://doi.org/10.1016/j.yexcr.2019.03.011
Grevesse T, Dabiri BE, Parker KK, Gabriele S (2015) Opposite rheological properties of neuronal microcompartments predict axonal vulnerability in brain injury. Sci Rep 5(9475). https://doi.org/10.1038/srep09475
Grzywa EL, Lee AC, Lee GU, Suter DM (2006) High-resolution analysis of neuronal growth cone morphology by comparative atomic force and optical microscopy. J Neurobiol 66:1529–1543. https://doi.org/10.1002/neu.20318
Gu H, Yu SP, Gutekunst C-A, Gross RE, Wei L (2013) Inhibition of the Rho signaling pathway improves neurite outgrowth and neuronal differentiation of mouse neural stem cells. Int J Physiol Pathophysiol Pharmacol 5:11–20
Haase K, Pelling AE (2015) Investigating cell mechanics with atomic force microscopy. J R Soc Interface 12. https://doi.org/10.1098/rsif.2014.0970
Hadden WJ, Young JL, Holle AW, McFetridge ML, Kim DY, Wijesinghe P, Taylor-Weiner H, Wen JH, Lee AR, Bieback K, Vo B-N, Sampson DD, Kennedy BF, Spatz JP, Engler AJ, Choi YS (2017) Stem cell migration and mechanotransduction on linear stiffness gradient hydrogels. Proc Natl Acad Sci 114:5647–5652. https://doi.org/10.1073/pnas.1618239114
Hällström W, Lexholm M, Suyatin DB, Hammarin G, Hessman D, Samuelson L, Montelius L, Kanje M, Prinz CN (2010) Fifteen-piconewton force detection from neural growth cones using nanowire arrays. Nano Lett 10:782–787. https://doi.org/10.1021/nl902675h
Haubst N, Georges-Labouesse E, Arcangelis AD, Mayer U, Götz M (2006) Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes. Development 133:3245–3254. https://doi.org/10.1242/dev.02486
Helenius J, Heisenberg C-P, Gaub HE, Muller DJ (2008) Single-cell force spectroscopy. J Cell Sci 121:1785–1791. https://doi.org/10.1242/jcs.030999
Hertz H (1882) Ueber die Berührung fester elastischer Körper. J Für Reine Angew Math (92):156–171
Hoffman-Kim D, Mitchel JA, Bellamkonda RV (2010) Topography, cell response, and nerve regeneration. Annu Rev Biomed Eng 12:203–231. https://doi.org/10.1146/annurev-bioeng-070909-105351
Hong SE, Shugart YY, Huang DT, Shahwan SA, Grant PE, Hourihane JO, Martin ND, Walsh CA (2000) Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 26:93–96. https://doi.org/10.1038/79246
Hopkins AM, Laporte LD, Tortelli F, Spedden E, Staii C, Atherton TJ, Hubbell JA, Kaplan DL (2013) Silk hydrogels as soft substrates for neural tissue engineering. Adv Funct Mater 23:5140–5149. https://doi.org/10.1002/adfm.201300435
Huang J, Grater SV, Corbellini F, Rinck S, Bock E, Kemkemer R, Kessler H, Ding J, Spatz JP (2009) Impact of order and disorder in RGD nanopatterns on cell adhesion. Nano Lett 9:1111–1116. https://doi.org/10.1021/nl803548b
Huang DL, Bax NA, Buckley CD, Weis WI, Dunn AR (2017) Vinculin forms a directionally asymmetric catch bond with F-actin. Science 357:703–706. https://doi.org/10.1126/science.aan2556
Humphries JD, Chastney MR, Askari JA, Humphries MJ (2019) Signal transduction via integrin adhesion complexes. Curr Opin Cell Biol 56:14–21. https://doi.org/10.1016/j.ceb.2018.08.004
Indrieri M, Podestà A, Bongiorno G, Marchesi D, Milani P (2011) Adhesive-free colloidal probes for nanoscale force measurements: production and characterization. Rev Sci Instrum 82:023708. https://doi.org/10.1063/1.3553499
Iskratsch T, Wolfenson H, Sheetz MP (2014) Appreciating force and shape—the rise of mechanotransduction in cell biology. Nat Rev Mol Cell Biol 15:825–833. https://doi.org/10.1038/nrm3903
Jiang G, Giannone G, Critchley DR, Fukumoto E, Sheetz MP (2003) Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424:334. https://doi.org/10.1038/nature01805
Jiang FX, Yurke B, Firestein BL, Langrana NA (2008) Neurite outgrowth on a DNA crosslinked hydrogel with tunable stiffnesses. Ann Biomed Eng 36:1565–1579. https://doi.org/10.1007/s10439-008-9530-z
Jiang J, Zhang Z, Yuan X, Poo M (2015) Spatiotemporal dynamics of traction forces show three contraction centers in migratory neurons. J Cell Biol 209:759–774. https://doi.org/10.1083/jcb.201410068
Jin Y, Lee JS, Kim J, Min S, Wi S, Yu JH, Chang G-E, Cho A-N, Choi Y, Ahn D-H, Cho S-R, Cheong E, Kim Y-G, Kim H-P, Kim Y, Kim DS, Kim HW, Quan Z, Kang H-C, Cho S-W (2018) Three-dimensional brain-like microenvironments facilitate the direct reprogramming of fibroblasts into therapeutic neurons. Nat Biomed Eng 2:522–539. https://doi.org/10.1038/s41551-018-0260-8
Johansson F, Carlberg P, Danielsen N, Montelius L, Kanje M (2006) Axonal outgrowth on nano-imprinted patterns. Biomaterials 27:1251–1258. https://doi.org/10.1016/j.biomaterials.2005.07.047
Jurchenko C, Salaita KS (2015) Lighting up the force: investigating mechanisms of mechanotransduction using fluorescent tension probes. Mol Cell Biol 35:2570–2582. https://doi.org/10.1128/MCB.00195-15
Kalappurakkal JM, Anilkumar AA, Patra C, van Zanten TS, Sheetz MP, Mayor S (2019) Integrin mechano-chemical signaling generates plasma membrane nanodomains that promote cell spreading. Cell 177:1738–1756.e23. https://doi.org/10.1016/j.cell.2019.04.037
Kang K, Choi S-E, Jang HS, Cho WK, Nam Y, Choi IS, Lee JS (2012) In vitro developmental acceleration of hippocampal neurons on nanostructures of self-assembled silica beads in filopodium-size ranges. Angew Chem Int Ed 51:2855–2858. https://doi.org/10.1002/anie.201106271
Kechagia JZ, Ivaska J, Roca-Cusachs P (2019) Integrins as biomechanical sensors of the microenvironment. Nat Rev Mol Cell Biol 1. https://doi.org/10.1038/s41580-019-0134-2
Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F (2007) Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells Dayt. Ohio 25:2146–2157. https://doi.org/10.1634/stemcells.2007-0082
Kerrisk ME, Greer CA, Koleske AJ (2013) Integrin α3 is required for late postnatal stability of dendrite arbors, dendritic spines and synapses, and mouse behavior. J Neurosci 33:6742–6752. https://doi.org/10.1523/JNEUROSCI.0528-13.2013
Kerstein PC, Nichol RH, Gomez TM (2015) Mechanochemical regulation of growth cone motility. Front Cell Neurosci 9:244. https://doi.org/10.3389/fncel.2015.00244
Keung AJ, de Juan-Pardo EM, Schaffer DV, Kumar S (2011) Rho GTPases mediate the mechanosensitive lineage commitment of neural stem cells. Stem Cells 29:1886–1897. https://doi.org/10.1002/stem.746
Keung AJ, Asuri P, Kumar S, Schaffer DV (2012) Soft microenvironments promote the early neurogenic differentiation but not self-renewal of human pluripotent stem cells. Integr Biol (Camb) 4:1049–1058. https://doi.org/10.1039/c2ib20083j
Keung AJ, Dong M, Schaffer DV, Kumar S (2013) Pan-neuronal maturation but not neuronal subtype differentiation of adult neural stem cells is mechanosensitive. Sci Rep 3:1817. https://doi.org/10.1038/srep01817
Kilinc D (2018) The emerging role of mechanics in synapse formation and plasticity. Front Cell Neurosci 12. https://doi.org/10.3389/fncel.2018.00483
Kilinc D, Blasiak A, O’Mahony JJ, Lee GU (2014) Low piconewton towing of CNS axons against diffusing and surface-bound repellents requires the inhibition of motor protein-associated pathways. Sci Rep 4:7128. https://doi.org/10.1038/srep07128
Kim Y, Kumar S (2014) CD44-mediated adhesion to hyaluronic acid contributes to mechanosensing and invasive motility. Mol Cancer Res 12:1416–1429. https://doi.org/10.1158/1541-7786.MCR-13-0629
Kim M-H, Park M, Kang K, Choi IS (2013) Neurons on nanometric topographies: insights into neuronal behaviors in vitro. Biomater Sci. 2:148–155. https://doi.org/10.1039/C3BM60255A
Knöll B, Nordheim A (2009) Functional versatility of transcription factors in the nervous system: the SRF paradigm. Trends Neurosci 32:432–442. https://doi.org/10.1016/j.tins.2009.05.004
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 102:452–460. https://doi.org/10.1016/j.bpj.2011.12.025
Kong F, García AJ, Mould AP, Humphries MJ, Zhu C (2009) Demonstration of catch bonds between an integrin and its ligand. J Cell Biol 185:1275–1284. https://doi.org/10.1083/jcb.200810002
Konno D, Yoshimura S, Hori K, Maruoka H, Sobue K (2005) Involvement of the phosphatidylinositol 3-kinase/rac1 and cdc42 pathways in radial migration of cortical neurons. J Biol Chem 280:5082–5088. https://doi.org/10.1074/jbc.M408251200
Koser DE, Moeendarbary E, Hanne J, Kuerten S, Franze K (2015) CNS cell distribution and axon orientation determine local spinal cord mechanical properties. Biophys J 108:2137–2147. https://doi.org/10.1016/j.bpj.2015.03.039
Koser DE, Thompson AJ, Foster SK, Dwivedy A, Pillai EK, Sheridan GK, Svoboda H, Viana M, Costa LD, Guck J, Holt CE, Franze K (2016) Mechanosensing is critical for axon growth in the developing brain. Nat Neurosci 19:1592–1598. https://doi.org/10.1038/nn.4394
Kostic A, Sap J, Sheetz MP (2007) RPTPα is required for rigidity-dependent inhibition of extension and differentiation of hippocampal neurons. J Cell Sci 120:3895–3904. https://doi.org/10.1242/jcs.009852
Krieg M, Fläschner G, Alsteens D, Gaub BM, Roos WH, Wuite GJL, Gaub HE, Gerber C, Dufrêne YF, Müller DJ (2019) Atomic force microscopy-based mechanobiology. Nat Rev Phys 1:41. https://doi.org/10.1038/s42254-018-0001-7
Lam D, Enright HA, Cadena J, Peters SKG, Sales AP, Osburn JJ, Soscia DA, Kulp KS, Wheeler EK, Fischer NO (2019) Tissue-specific extracellular matrix accelerates the formation of neural networks and communities in a neuron-glia co-culture on a multi-electrode array. Sci Rep 9:4159. https://doi.org/10.1038/s41598-019-40128-1
Last JA, Russell P, Nealey PF, Murphy CJ (2010) The applications of atomic force microscopy to vision science. Invest Ophthalmol Vis Sci 51:6083–6094. https://doi.org/10.1167/iovs.10-5470
Lathia JD, Patton B, Eckley DM, Magnus T, Mughal MR, Sasaki T, Caldwell MA, Rao MS, Mattson MP, ffrench-Constant C (2007) Patterns of laminins and integrins in the embryonic ventricular zone of the CNS. J Comp Neurol 505:630–643. https://doi.org/10.1002/cne.21520
Lau LW, Cua R, Keough MB, Haylock-Jacobs S, Yong VW (2013) Pathophysiology of the brain extracellular matrix: a new target for remyelination. Nat Rev Neurosci 14:722–729. https://doi.org/10.1038/nrn3550
Le S, Liu R, Lim CT, Yan J (2016) Uncovering mechanosensing mechanisms at the single protein level using magnetic tweezers. Methods 94:13–18. https://doi.org/10.1016/j.ymeth.2015.08.020
Leach JB, Brown XQ, Jacot JG, Dimilla PA, Wong JY (2007) Neurite outgrowth and branching of PC12 cells on very soft substrates sharply decreases below a threshold of substrate rigidity. J Neural Eng 4:26–34. https://doi.org/10.1088/1741-2560/4/2/003
Lee MR, Kwon KW, Jung H, Kim HN, Suh KY, Kim K, Kim K-S (2010) Direct differentiation of human embryonic stem cells into selective neurons on nanoscale ridge/groove pattern arrays. Biomaterials 31:4360–4366. https://doi.org/10.1016/j.biomaterials.2010.02.012
Leipzig ND, Shoichet MS (2009) The effect of substrate stiffness on adult neural stem cell behavior. Biomaterials 30:6867–6878. https://doi.org/10.1016/j.biomaterials.2009.09.002
Leterrier C, Dubey P, Roy S (2017) The nano-architecture of the axonal cytoskeleton. Nat Rev Neurosci 18:713–726. https://doi.org/10.1038/nrn.2017.129
Li J, Springer TA (2017) Integrin extension enables ultrasensitive regulation by cytoskeletal force. Proc Natl Acad Sci U S A 114:4685–4690. https://doi.org/10.1073/pnas.1704171114
Lilja J, Ivaska J (2018) Integrin activity in neuronal connectivity. J Cell Sci 131. https://doi.org/10.1242/jcs.212803
Lim SH, Liu XY, Song H, Yarema KJ, Mao H-Q (2010) The effect of nanofiber-guided cell alignment on the preferential differentiation of neural stem cells. Biomaterials 31:9031–9039. https://doi.org/10.1016/j.biomaterials.2010.08.021
Liu Y, Medda R, Liu Z, Galior K, Yehl K, Spatz JP, Cavalcanti-Adam EA, Salaita K (2014) Nanoparticle tension probes patterned at the nanoscale: impact of integrin clustering on force transmission. Nano Lett 14:5539–5546. https://doi.org/10.1021/nl501912g
Liu Y, Galior K, Ma VP-Y, Salaita K (2017) Molecular tension probes for imaging forces at the cell surface. Acc Chem Res 50:2915–2924. https://doi.org/10.1021/acs.accounts.7b00305
Long KR, Huttner WB (2019) How the extracellular matrix shapes neural development. Open Biol 9:180216. https://doi.org/10.1098/rsob.180216
Lowery LA, Van Vactor D (2009) The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol 10:332–343. https://doi.org/10.1038/nrm2679
Lu Y-B, Franze K, Seifert G, Steinhäuser C, Kirchhoff F, Wolburg H, Guck J, Janmey P, Wei E-Q, Käs J, Reichenbach A (2006) Viscoelastic properties of individual glial cells and neurons in the CNS. Proc Natl Acad Sci U S A 103:17759–17764. https://doi.org/10.1073/pnas.0606150103
Ma W, Tavakoli T, Derby E, Serebryakova Y, Rao MS, Mattson MP (2008) Cell-extracellular matrix interactions regulate neural differentiation of human embryonic stem cells. BMC Dev Biol 8:90. https://doi.org/10.1186/1471-213X-8-90
Maffioli E, Schulte C, Nonnis S, Grassi Scalvini F, Piazzoni C, Lenardi C, Negri A, Milani P, Tedeschi G (2017) Proteomic dissection of nanotopography-sensitive mechanotransductive signalling hubs that foster neuronal differentiation in PC12 cells. Front Cell Neurosci 11. https://doi.org/10.3389/fncel.2017.00417
Mammadov B, Sever M, Guler MO, Tekinay AB (2013) Neural differentiation on synthetic scaffold materials. Biomater Sci 1:1119–1137. https://doi.org/10.1039/C3BM60150A
Man AJ, Davis HE, Itoh A, Leach JK, Bannerman P (2011) Neurite outgrowth in fibrin gels is regulated by substrate stiffness. Tissue Eng Part A 17:2931–2942. https://doi.org/10.1089/ten.tea.2011.0030
McGeachie AB, Cingolani LA, Goda Y (2011) A stabilising influence: integrins in regulation of synaptic plasticity. Neurosci Res 70:24–29. https://doi.org/10.1016/j.neures.2011.02.006
Medberry CJ, Crapo PM, Siu BF, Carruthers CA, Wolf MT, Nagarkar SP, Agrawal V, Jones KE, Kelly J, Johnson SA, Velankar SS, Watkins SC, Modo M, Badylak SF (2013) Hydrogels derived from central nervous system extracellular matrix. Biomaterials 34:1033–1040. https://doi.org/10.1016/j.biomaterials.2012.10.062
Medeiros NA, Burnette DT, Forscher P (2006) Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat Cell Biol 8:215–226. https://doi.org/10.1038/ncb1367
Mercier F (2016) Fractones: extracellular matrix niche controlling stem cell fate and growth factor activity in the brain in health and disease. Cell Mol Life Sci 73:4661–4674. https://doi.org/10.1007/s00018-016-2314-y
Migliorini E, Grenci G, Ban J, Pozzato A, Tormen M, Lazzarino M, Torre V, Ruaro ME (2011) Acceleration of neuronal precursors differentiation induced by substrate nanotopography. Biotechnol Bioeng 108:2736–2746. https://doi.org/10.1002/bit.23232
Mitchison T, Kirschner M (1988) Cytoskeletal dynamics and nerve growth. Neuron 1:761–772
Miyata S, Kitagawa H (2017) Formation and remodeling of the brain extracellular matrix in neural plasticity: roles of chondroitin sulfate and hyaluronan. Biochim Biophys Acta Gen Subj 1861:2420–2434. https://doi.org/10.1016/j.bbagen.2017.06.010
Moffitt JR, Chemla YR, Smith SB, Bustamante C (2008) Recent advances in optical tweezers. Annu Rev Biochem 77:205–228. https://doi.org/10.1146/annurev.biochem.77.043007.090225
Mokalled MH, Johnson A, Kim Y, Oh J, Olson EN (2010) Myocardin-related transcription factors regulate the Cdk5/Pctaire1 kinase cascade to control neurite outgrowth, neuronal migration and brain development. Development 137:2365–2374. https://doi.org/10.1242/dev.047605
Moore SW, Biais N, Sheetz MP (2009) Traction on immobilized netrin-1 is sufficient to reorient axons. Science 325:166. https://doi.org/10.1126/science.1173851
Morgan MR, Hamidi H, Bass MD, Warwood S, Ballestrem C, Humphries MJ (2013) Syndecan-4 phosphorylation is a control point for integrin recycling. Dev Cell 24:472–485. https://doi.org/10.1016/j.devcel.2013.01.027
Mosley MC, Lim HJ, Chen J, Yang Y-H, Li S, Liu Y, Smith Callahan LA (2017) Neurite extension and neuronal differentiation of human induced pluripotent stem cell derived neural stem cells on polyethylene glycol hydrogels containing a continuous Young’s Modulus gradient. J Biomed Mater Res A 105:824–833. https://doi.org/10.1002/jbm.a.35955
Müller DJ, Helenius J, Alsteens D, Dufrêne YF (2009) Force probing surfaces of living cells to molecular resolution. Nat Chem Biol 5:383–390. https://doi.org/10.1038/nchembio.181
Musah S, Wrighton PJ, Zaltsman Y, Zhong X, Zorn S, Parlato MB, Hsiao C, Palecek SP, Chang Q, Murphy WL, Kiessling LL (2014) Substratum-induced differentiation of human pluripotent stem cells reveals the coactivator YAP is a potent regulator of neuronal specification. Proc Natl Acad Sci U S A 111:13805–13810. https://doi.org/10.1073/pnas.1415330111
Myers JP, Santiago-Medina M, Gomez TM (2011) Regulation of axonal outgrowth and pathfinding by integrin-ECM interactions. Dev Neurobiol 71:901–923. https://doi.org/10.1002/dneu.20931
Neuman KC, Nagy A (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat Methods 5:491–505. https://doi.org/10.1038/nmeth.1218
Nichol RH, Hagen KM, Lumbard DC, Dent EW, Gómez TM (2016) Guidance of axons by local coupling of retrograde flow to point contact adhesions. J Neurosci 36:2267–2282. https://doi.org/10.1523/JNEUROSCI.2645-15.2016
Norman LL, Aranda-Espinoza H (2010) Cortical neuron outgrowth is insensitive to substrate stiffness. Cell Mol Bioeng 3:398–414. https://doi.org/10.1007/s12195-010-0137-8
O’Toole M, Lamoureux P, Miller KE (2015) Measurement of subcellular force generation in neurons. Biophys J 108:1027–1037. https://doi.org/10.1016/j.bpj.2015.01.021
Oria R, Wiegand T, Escribano J, Elosegui-Artola A, Uriarte JJ, Moreno-Pulido C, Platzman I, Delcanale P, Albertazzi L, Navajas D, Trepat X, García-Aznar JM, Cavalcanti-Adam EA, Roca-Cusachs P (2017) Force loading explains spatial sensing of ligands by cells. Nature 552:219. https://doi.org/10.1038/nature24662
Orlando C, Ster J, Gerber U, Fawcett JW, Raineteau O (2012) Perisynaptic chondroitin sulfate proteoglycans restrict structural plasticity in an integrin-dependent manner. J Neurosci 32:18009–18017, 18017a. https://doi.org/10.1523/JNEUROSCI.2406-12.2012
Park YK, Goda Y (2016) Integrins in synapse regulation. Nat Rev Neurosci 17:745–756. https://doi.org/10.1038/nrn.2016.138
Park J, Kim D-H, Kim H-N, Wang CJ, Kwak MK, Hur E, Suh K-Y, An SS, Levchenko A (2016a) Directed migration of cancer cells guided by the graded texture of the underlying matrix. Nat Mater 15:792–801. https://doi.org/10.1038/nmat4586
Park M, Oh E, Seo J, Kim M-H, Cho H, Choi JY, Lee H, Choi IS (2016b) Control over neurite directionality and neurite elongation on anisotropic micropillar arrays. Small 12:1148–1152. https://doi.org/10.1002/smll.201501896
Parpura V, Haydon PG, Henderson E (1993) Three-dimensional imaging of living neurons and glia with the atomic force microscope. J Cell Sci 104(Pt 2):427–432
Paszek MJ, DuFort CC, Rossier O, Bainer R, Mouw JK, Godula K, Hudak JE, Lakins JN, Wijekoon AC, Cassereau L, Rubashkin MG, Magbanua MJ, Thorn KS, Davidson MW, Rugo HS, Park JW, Hammer DA, Giannone G, Bertozzi CR, Weaver VM (2014) The cancer glycocalyx mechanically primes integrin-mediated growth and survival. Nature 511:319–325. https://doi.org/10.1038/nature13535
Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248–1251. https://doi.org/10.1126/science.1072699
Puech P-H, Poole K, Knebel D, Muller DJ (2006) A new technical approach to quantify cell-cell adhesion forces by AFM. Ultramicroscopy 106:637–644. https://doi.org/10.1016/j.ultramic.2005.08.003
Puricelli L, Galluzzi M, Schulte C, Podestà A, Milani P (2015) Nanomechanical and topographical imaging of living cells by atomic force microscopy with colloidal probes. Rev Sci Instrum 86:033705. https://doi.org/10.1063/1.4915896
Rajnicek A, Britland S, McCaig C (1997) Contact guidance of CNS neurites on grooved quartz: influence of groove dimensions, neuronal age and cell type. J Cell Sci 110:2905–2913
Rico F, Roca-Cusachs P, Sunyer R, Farré R, Navajas D (2007) Cell dynamic adhesion and elastic properties probed with cylindrical atomic force microscopy cantilever tips. J Mol Recognit 20:459–466. https://doi.org/10.1002/jmr.829
Robles E, Woo S, Gomez TM (2005) Src-dependent tyrosine phosphorylation at the tips of growth cone filopodia promotes extension. J Neurosci 25:7669–7681. https://doi.org/10.1523/JNEUROSCI.2680-05.2005
Ruoslahti E (1996) Brain extracellular matrix. Glycobiology 6:489–492. https://doi.org/10.1093/glycob/6.5.489
Sack I, Streitberger K-J, Krefting D, Paul F, Braun J (2011) The influence of physiological aging and atrophy on brain viscoelastic properties in humans. PLoS One 6:e23451. https://doi.org/10.1371/journal.pone.0023451
Saha K, Keung AJ, Irwin EF, Li Y, Little L, Schaffer DV, Healy KE (2008) Substrate modulus directs neural stem cell behavior. Biophys J 95:4426–4438. https://doi.org/10.1529/biophysj.108.132217
Santiago-Medina M, Gregus KA, Gomez TM (2013) PAK-PIX interactions regulate adhesion dynamics and membrane protrusion to control neurite outgrowth. J Cell Sci 126:1122–1133. https://doi.org/10.1242/jcs.112607
Sarker M, Naghieh S, McInnes AD, Schreyer DJ, Chen X (2018) Strategic design and fabrication of nerve guidance conduits for peripheral nerve regeneration. Biotechnol J 13:1700635. https://doi.org/10.1002/biot.201700635
Schierbaum N, Rheinlaender J, Schäffer TE (2019) Combined atomic force microscopy (AFM) and traction force microscopy (TFM) reveals a correlation between viscoelastic material properties and contractile prestress of living cells. Soft Matter 15:1721–1729. https://doi.org/10.1039/C8SM01585F
Schillers H, Rianna C, Schäpe J, Luque T, Doschke H, Wälte M, Uriarte JJ, Campillo N, Michanetzis GPA, Bobrowska J, Dumitru A, Herruzo ET, Bovio S, Parot P, Galluzzi M, Podestà A, Puricelli L, Scheuring S, Missirlis Y, Garcia R, Odorico M, Teulon J-M, Lafont F, Lekka M, Rico F, Rigato A, Pellequer J-L, Oberleithner H, Navajas D, Radmacher M (2017) Standardized nanomechanical atomic force microscopy procedure (SNAP) for measuring soft and biological samples. Sci Rep 7:5117. https://doi.org/10.1038/s41598-017-05383-0
Schmid RS, Shelton S, Stanco A, Yokota Y, Kreidberg JA, Anton ES (2004) alpha3beta1 integrin modulates neuronal migration and placement during early stages of cerebral cortical development. Development 131:6023–6031. https://doi.org/10.1242/dev.01532
Schulte C, Racchetti G, D’Alessandro R, Meldolesi J (2010) A new form of neurite outgrowth sustained by the exocytosis of enlargeosomes expressed under the control of REST. Traffic Cph Den 11:1304–1314. https://doi.org/10.1111/j.1600-0854.2010.01095.x
Schulte C, Ferraris GMS, Oldani A, Galluzzi M, Podestà A, Puricelli L, de Lorenzi V, Lenardi C, Milani P, Sidenius N (2016a) Lamellipodial tension, not integrin/ligand binding, is the crucial factor to realise integrin activation and cell migration. Eur J Cell Biol 95:1–14. https://doi.org/10.1016/j.ejcb.2015.10.002
Schulte C, Ripamonti M, Maffioli E, Cappelluti MA, Nonnis S, Puricelli L, Lamanna J, Piazzoni C, Podestà A, Lenardi C, Tedeschi G, Malgaroli A, Milani P (2016b) Scale invariant disordered nanotopography promotes hippocampal neuron development and maturation with involvement of mechanotransductive pathways. Front Cell Neurosci 10:267. https://doi.org/10.3389/fncel.2016.00267
Schulte C, Rodighiero S, Cappelluti MA, Puricelli L, Maffioli E, Borghi F, Negri A, Sogne E, Galluzzi M, Piazzoni C, Tamplenizza M, Podestà A, Tedeschi G, Lenardi C, Milani P (2016c) Conversion of nanoscale topographical information of cluster-assembled zirconia surfaces into mechanotransductive events promotes neuronal differentiation. J Nanobiotechnology 14:18. https://doi.org/10.1186/s12951-016-0171-3
Schulte C, Podestà A, Lenardi C, Tedeschi G, Milani P (2017) Quantitative control of protein and cell interaction with nanostructured surfaces by cluster assembling. Acc Chem Res 50:231–239. https://doi.org/10.1021/acs.accounts.6b00433
Schulte C, Lamanna J, Moro AS, Piazzoni C, Borghi F, Chighizola M, Ortoleva S, Racchetti G, Lenardi C, Podestà A, Malgaroli A, Milani P (2018) Neuronal cells confinement by micropatterned cluster-assembled dots with mechanotransductive nanotopography. ACS Biomater Sci Eng. https://doi.org/10.1021/acsbiomaterials.8b00916
Schvartzman M, Palma M, Sable J, Abramson J, Hu X, Sheetz MP, Wind SJ (2011) Nanolithographic control of the spatial organization of cellular adhesion receptors at the single-molecule level. Nano Lett 11:1306–1312. https://doi.org/10.1021/nl104378f
Schwarz US, Soiné JRD (2015) Traction force microscopy on soft elastic substrates: a guide to recent computational advances. Biochim Biophys Acta 1853:3095–3104. https://doi.org/10.1016/j.bbamcr.2015.05.028
Seidlits SK, Khaing ZZ, Petersen RR, Nickels JD, Vanscoy JE, Shear JB, Schmidt CE (2010) The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. Biomaterials 31:3930–3940. https://doi.org/10.1016/j.biomaterials.2010.01.125
Sekine K, Kawauchi T, Kubo K-I, Honda T, Herz J, Hattori M, Kinashi T, Nakajima K (2012) Reelin controls neuronal positioning by promoting cell-matrix adhesion via inside-out activation of integrin α5β1. Neuron 76:353–369. https://doi.org/10.1016/j.neuron.2012.07.020
Shattil SJ, Kim C, Ginsberg MH (2010) The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol 11:288–300. https://doi.org/10.1038/nrm2871
Shen Q, Wang Y, Kokovay E, Lin G, Chuang S-M, Goderie SK, Roysam B, Temple S (2008) Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3:289–300. https://doi.org/10.1016/j.stem.2008.07.026
Sheng M, Kim E (2011) The postsynaptic organization of synapses. Cold Spring Harb Perspect Biol 3. https://doi.org/10.1101/cshperspect.a005678
Siedlik MJ, Varner VD, Nelson CM (2016) Pushing, pulling, and squeezing our way to understanding mechanotransduction. Methods 94:4–12. https://doi.org/10.1016/j.ymeth.2015.08.019
Sigal YM, Bae H, Bogart LJ, Hensch TK, Zhuang X (2019) Structural maturation of cortical peineuronal nets and their perforating synapses revealed by superresolution imaging. Proc Natl Acad Sci 116:7071–7076. https://doi.org/10.1073/pnas.1817222116
Simitzi C, Efstathopoulos P, Kourgiantaki A, Ranella A, Charalampopoulos I, Fotakis C, Athanassakis I, Stratakis E, Gravanis A (2015) Laser fabricated discontinuous anisotropic microconical substrates as a new model scaffold to control the directionality of neuronal network outgrowth. Biomaterials 67:115–128. https://doi.org/10.1016/j.biomaterials.2015.07.008
Simitzi C, Ranella A, Stratakis E (2017) Controlling the morphology and outgrowth of nerve and neuroglial cells: the effect of surface topography. Acta Biomater 51:21–52. https://doi.org/10.1016/j.actbio.2017.01.023
Smith Callahan LA, Xie S, Barker IA, Zheng J, Reneker DH, Dove AP, Becker ML (2013) Directed differentiation and neurite extension of mouse embryonic stem cell on aligned poly(lactide) nanofibers functionalized with YIGSR peptide. Biomaterials 34:9089–9095. https://doi.org/10.1016/j.biomaterials.2013.08.028
Sneddon IN (1965) The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. Int J Eng Sci 3:47–57. https://doi.org/10.1016/0020-7225(65)90019-4
Solecki DJ, Trivedi N, Govek E-E, Kerekes RA, Gleason SS, Hatten ME (2009) Myosin II motors and F-actin dynamics drive the coordinated movement of the centrosome and soma during CNS glial-guided neuronal migration. Neuron 63:63–80. https://doi.org/10.1016/j.neuron.2009.05.028
Sorg BA, Berretta S, Blacktop JM, Fawcett JW, Kitagawa H, Kwok JCF, Miquel M (2016) Casting a wide net: role of perineuronal nets in neural plasticity. J Neurosci 36:11459–11468. https://doi.org/10.1523/JNEUROSCI.2351-16.2016
Spedden E, White JD, Naumova EN, Kaplan DL, Staii C (2012) Elasticity maps of living neurons measured by combined fluorescence and atomic force microscopy. Biophys J 103:868–877. https://doi.org/10.1016/j.bpj.2012.08.005
Stabenfeldt SE, LaPlaca MC (2011) Variations in rigidity and ligand density influence neuronal response in methylcellulose-laminin hydrogels. Acta Biomater 7:4102–4108. https://doi.org/10.1016/j.actbio.2011.07.026
Strick T, Allemand J-F, Croquette V, Bensimon D (2000) Twisting and stretching single DNA molecules. Prog Biophys Mol Biol 74:115–140. https://doi.org/10.1016/S0079-6107(00)00018-3
Strohmeyer N, Bharadwaj M, Costell M, Fässler R, Müller DJ (2017) Fibronectin-bound α5β1 integrins sense load and signal to reinforce adhesion in less than a second. Nat Mater 16:1262–1270. https://doi.org/10.1038/nmat5023
Stukel JM, Willits RK (2015) Mechanotransduction of neural cells through cell–substrate interactions. Tissue Eng Part B Rev 22:173–182. https://doi.org/10.1089/ten.teb.2015.0380
Sun Y, Yong KMA, Villa-Diaz LG, Zhang X, Chen W, Philson R, Weng S, Xu H, Krebsbach PH, Fu J (2014) Hippo/YAP-mediated rigidity-dependent motor neuron differentiation of human pluripotent stem cells. Nat Mater 13:599–604. https://doi.org/10.1038/nmat3945
Sun Z, Costell M, Fässler R (2019) Integrin activation by talin, kindlin and mechanical forces. Nat Cell Biol 21:25. https://doi.org/10.1038/s41556-018-0234-9
Sundararaghavan HG, Monteiro GA, Firestein BL, Shreiber DI (2009) Neurite growth in 3D collagen gels with gradients of mechanical properties. Biotechnol Bioeng 102:632–643. https://doi.org/10.1002/bit.22074
Tajerian M, Hung V, Nguyen H, Lee G, Joubert L-M, Malkovskiy AV, Zou B, Xie S, Huang T-T, Clark JD (2018) The hippocampal extracellular matrix regulates pain and memory after injury. Mol Psychiatry 23:2302. https://doi.org/10.1038/s41380-018-0209-z
Tanner K (2018) Perspective: the role of mechanobiology in the etiology of brain metastasis. APL Bioeng 2:031801. https://doi.org/10.1063/1.5024394
Tate MC, García AJ, Keselowsky BG, Schumm MA, Archer DR, LaPlaca MC (2004) Specific beta1 integrins mediate adhesion, migration, and differentiation of neural progenitors derived from the embryonic striatum. Mol Cell Neurosci 27:22–31. https://doi.org/10.1016/j.mcn.2004.05.001
Taubenberger A, Cisneros DA, Friedrichs J, Puech P-H, Muller DJ, Franz CM (2007) Revealing early steps of α2β1 integrin-mediated adhesion to collagen type I by using single-cell force spectroscopy. Mol Biol Cell 18:1634–1644. https://doi.org/10.1091/mbc.E06-09-0777
Teixeira AI, Ilkhanizadeh S, Wigenius JA, Duckworth JK, Inganäs O, Hermanson O (2009) The promotion of neuronal maturation on soft substrates. Biomaterials 30:4567–4572. https://doi.org/10.1016/j.biomaterials.2009.05.013
Theodosiou M, Widmaier M, Böttcher RT, Rognoni E, Veelders M, Bharadwaj M, Lambacher A, Austen K, Müller DJ, Zent R, Fässler R (2016) Kindlin-2 cooperates with talin to activate integrins and induces cell spreading by directly binding paxillin. eLife 5:e10130. https://doi.org/10.7554/eLife.10130
Thompson AJ, Pillai EK, Dimov IB, Foster SK, Holt CE, Franze K (n.d.) Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain. eLife 8. https://doi.org/10.7554/eLife.39356
Tonazzini I, Meucci S, Faraci P, Beltram F, Cecchini M (2013) Neuronal differentiation on anisotropic substrates and the influence of nanotopographical noise on neurite contact guidance. Biomaterials 34:6027–6036. https://doi.org/10.1016/j.biomaterials.2013.04.039
Tonazzini I, Meucci S, Van Woerden GM, Elgersma Y, Cecchini M (2016) Impaired neurite contact guidance in ubiquitin ligase E3a (Ube3a)-deficient hippocampal neurons on nanostructured substrates. Adv Healthc Mater 5:850–862. https://doi.org/10.1002/adhm.201500815
Tyler WJ (2012) The mechanobiology of brain function. Nat Rev Neurosci 13:867–878. https://doi.org/10.1038/nrn3383
Uhler C, Shivashankar GV (2017) Chromosome intermingling: mechanical hotspots for genome regulation. Trends Cell Biol. https://doi.org/10.1016/j.tcb.2017.06.005
Vitriol EA, Zheng JQ (2012) Growth cone travel in space and time: the cellular ensemble of cytoskeleton, adhesion, and membrane. Neuron 73:1068–1081. https://doi.org/10.1016/j.neuron.2012.03.005
Wang X, Ha T (2013) Defining single molecular forces required to activate integrin and notch signaling. Science 340:991–994. https://doi.org/10.1126/science.1231041
Wang N, Butler JP, Ingber DE (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260:1124–1127. https://doi.org/10.1126/science.7684161
Wang HB, Mullins ME, Cregg JM, McCarthy CW, Gilbert RJ (2010) Varying the diameter of aligned electrospun fibers alters neurite outgrowth and Schwann cell migration. Acta Biomater 6:2970–2978. https://doi.org/10.1016/j.actbio.2010.02.020
Willits RK, Skornia SL (2004) Effect of collagen gel stiffness on neurite extension. J Biomater Sci Polym Ed 15:1521–1531
Winograd-Katz SE, Fässler R, Geiger B, Legate KR (2014) The integrin adhesome: from genes and proteins to human disease. Nat Rev Mol Cell Biol 15:273–288. https://doi.org/10.1038/nrm3769
Woo S, Gomez TM (2006) Rac1 and RhoA promote neurite outgrowth through formation and stabilization of growth cone point contacts. J Neurosci 26:1418–1428. https://doi.org/10.1523/JNEUROSCI.4209-05.2006
Xie J, Willerth SM, Li X, Macewan MR, Rader A, Sakiyama-Elbert SE, Xia Y (2009) The differentiation of embryonic stem cells seeded on electrospun nanofibers into neural lineages. Biomaterials 30:354–362. https://doi.org/10.1016/j.biomaterials.2008.09.046
Xiong Y, Lee AC, Suter DM, Lee GU (2009) Topography and nanomechanics of live neuronal growth cones analyzed by atomic force microscopy. Biophys J 96:5060–5072. https://doi.org/10.1016/j.bpj.2009.03.032
Xu Z, Chen Y, Chen Y (2019) Spatiotemporal regulation of Rho GTPases in neuronal migration. Cells 8:568. https://doi.org/10.3390/cells8060568
Yamaguchi Y, Katoh H, Yasui H, Mori K, Negishi M (2001) RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J Biol Chem 276:18977–18983. https://doi.org/10.1074/jbc.M100254200
Yang K, Jung K, Ko E, Kim J, Park KI, Kim J, Cho S-W (2013) Nanotopographical manipulation of focal adhesion formation for enhanced differentiation of human neural stem cells. ACS Appl Mater Interfaces 5:10529–10540. https://doi.org/10.1021/am402156f
Yang K, Jung H, Lee H-R, Lee JS, Kim SR, Song KY, Cheong E, Bang J, Im SG, Cho S-W (2014) Multiscale, hierarchically patterned topography for directing human neural stem cells into functional neurons. ACS Nano 8:7809–7822. https://doi.org/10.1021/nn501182f
Yang B, Lieu ZZ, Wolfenson H, Hameed FM, Bershadsky AD, Sheetz MP (2016) Mechanosensing controlled directly by tyrosine kinases. Nano Lett 16:5951–5961. https://doi.org/10.1021/acs.nanolett.6b02995
Yao M, Goult BT, Chen H, Cong P, Sheetz MP, Yan J (2014) Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation. Sci Rep 4:4610. https://doi.org/10.1038/srep04610
Young JL, Holle AW, Spatz JP (2016) Nanoscale and mechanical properties of the physiological cell–ECM microenvironment. Exp Cell Res 343:3–6. https://doi.org/10.1016/j.yexcr.2015.10.037
Zhang X, Jiang G, Cai Y, Monkley SJ, Critchley DR, Sheetz MP (2008) Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat Cell Biol 10:1062–1068. https://doi.org/10.1038/ncb1765
Zhang H, Deo M, Thompson RC, Uhler MD, Turner DL (2012) Negative regulation of Yap during neuronal differentiation. Dev Biol 361:103–115. https://doi.org/10.1016/j.ydbio.2011.10.017
Zhang D, Yang S, Toledo EM, Gyllborg D, Saltó C, Villaescusa JC, Arenas E (2017) Niche-derived laminin-511 promotes midbrain dopaminergic neuron survival and differentiation through YAP. Sci Signal 10:eaal4165. https://doi.org/10.1126/scisignal.aal4165
Zhu J, Zhu J, Springer TA (2013) Complete integrin headpiece opening in eight steps. J Cell Biol 201:1053–1068. https://doi.org/10.1083/jcb.201212037
Funding
This project has received funding from the European Union Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement no. 812772 (Phys2BioMed) and under the FET Open grant agreement no. 801126 (EDIT).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Chighizola, M., Dini, T., Lenardi, C. et al. Mechanotransduction in neuronal cell development and functioning. Biophys Rev 11, 701–720 (2019). https://doi.org/10.1007/s12551-019-00587-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12551-019-00587-2