Physical understanding of axonal growth patterns on grooved substrates: groove ridge crossing versus longitudinal alignment

Bio-Design and Manufacturing - Tập 3 - Trang 348-360 - 2020
Deming Zhang1,2, Hairui Suo3, Jin Qian4, Jun Yin1,2, Jianzhong Fu1,2, Yong Huang5
1The State Key Laboratory of Fluid Power and Mechatronic Systems, School of Mechanical Engineering, Zhejiang University, Hangzhou, China
2Key Laboratory of 3D Printing Process and Equipment of Zhejiang Province, School of Mechanical Engineering, Zhejiang University, Hangzhou, China
3School of Automation, Hangzhou Dianzi University, Hangzhou, China
4Key Laboratory of Soft Machines and Smart Devices of Zhejiang Province, Department of Engineering Mechanics, Zhejiang University, Hangzhou, China
5Department of Mechanical and Aerospace Engineering, University of Florida, Gainesville, USA

Tóm tắt

Surface topographies such as micrometric edges and grooves have been widely used to improve neuron outgrowth. However, finding the mechanism of neuron–surface interactions on grooved substrates remains a challenge. In this work, PC12 cells and chick forebrain neurons (CFNs) were cultured on grooved and smooth polyacrylonitrile substrates. It was found that CFNs showed a tendency of growing across groove ridges; while PC12 cells were only observed to grow in the longitudinal direction of grooves. To further investigate these observations, a 3D physical model of axonal outgrowth was developed. In this model, axon shafts are simulated as elastic 3D beams, accounting for the axon outgrowth as well as the focal contacts between axons and substrates. Moreover, the bending direction of axon tips during groove ridge crossing is governed by the energy minimization principle. Our physical model predicts that axonal groove ridge crossing is contributed by the bending compliance of axons, caused by lower Young’s modulus and smaller diameters. This work will aid the understanding of the mechanisms involved in axonal alignment and elongation of neurons guided by grooved substrates, and the obtained insights can be used to enhance the design of instructive scaffolds for nerve tissue engineering and regeneration applications.

Tài liệu tham khảo

Palispis WA, Gupta R (2017) Surgical repair in humans after traumatic nerve injury provides limited functional neural regeneration in adults. Exp Neurol 290:106–114 Narayan SK, Arumugam M, Chittoria R (2019) Outcome of human peripheral nerve repair interventions using conduits: a systematic review. J Neurol Sci 396:18–24 Singh A, Shiekh PA, Das M, Seppala J, Kumar A (2019) Aligned chitosan-gelatin cryogel-filled polyurethane nerve guidance channel for neural tissue engineering: fabrication, characterization, and in vitro evaluation. Biomacromolecules 20:662–673 Yin J, Wang ZH, Chai WX, Dai GL, Suo HR, Zhang N, Wen XJ, Huang Y (2017) Fabrication of inner grooved hollow fiber membranes using microstructured spinneret for nerve regeneration. J Manufact Sci Eng Trans Asme 139:111007 Zhou C, Liu B, Huang Y, Zeng X, You HJ, Li J, Zhang YG (2017) The effect of four types of artificial nerve graft structures on the repair of 10-mm rat sciatic nerve gap. J Biomed Mater Res Part A 105:3077–3085 Singh A, Asikainen S, Teotia AK, Shiekh PA, Huotilainen E, Qayoom I, Partanen J, Seppala J, Kumar A (2018) Biomimetic photocurable three-dimensional printed nerve guidance channels with aligned cryomatrix lumen for peripheral nerve regeneration. ACS Appl Mater Interfaces 10:43327–43342 Suo HR, Wang ZH, Dai GL, Fu JZ, Yin J, Chang LQ (2018) Polyacrylonitrile nerve conduits with inner longitudinal grooved textures to enhance neuron directional outgrowth. J Microelectromech Syst 27:457–463 Isaacs J, Browne T (2014) Overcoming short gaps in peripheral nerve repair: conduits and human acellular nerve allograft. Hand 9:131–137 Hopkins TM, Little KJ, Vennemeyer JJ, Triozzi JL, Turgeon MK, Heilman AM, Minteer D, Marra K, Hom DB, Pixley SK (2017) Short and long gap peripheral nerve repair with magnesium metal filaments. J Biomed Mater Res Part A 105:3148–3158 Zhang Q, Li YL, Sun H, Zeng L, Li X, Yuan B, Ning CY, Dong H, Chen XF (2015) hMSCs bridging across micro-patterned grooves. RSC Adv 5:47975–47982 Zhang DT, Wu S, Feng JY, Duan YY, Xing DM, Gao CY (2018) Micropatterned biodegradable polyesters clicked with CQAASIKVAV promote cell alignment, directional migration, and neurite outgrowth. Acta Biomater 74:143–155 Park S, Choi KS, Kim D, Kim W, Lee D, Kim HN, Hyun H, Lim KT, Kim JW, Kim YR, Kim J (2018) Controlled extracellular topographical and chemical cues for acceleration of neuronal development. J Ind Eng Chem 61:65–70 Krishnamoorthy S, Zhang ZY, Xu CX (2020) Guided cell migration on a graded micropillar substrate. Bio-Des Manuf 3:60–70 Wang B, Shi J, Wei J, Wang L, Tu XL, Tang YD, Chen Y (2017) Fabrication of elastomer pillar arrays with height gradient for cell culture studies. Microelectron Eng 175:50–55 Wei J, Pozzi D, Severino FPU, Torre V, Chen Y (2017) Fabrication of PLGA nanofibers on PDMS micropillars for neuron culture studies. Microelectron Eng 175:67–72 Toma M, Belu A, Mayer D, Offenhäusser A (2017) Flexible gold nanocone array surfaces as a tool for regulating neuronal behavior. Small 13(24):1700629 Yao L, de Ruiter GCW, Wang HA, Knight AM, Spinner RJ, Yaszemski MJ, Windebank AJ, Pandit A (2010) Controlling dispersion of axonal regeneration using a multichannel collagen nerve conduit. Biomaterials 31:5789–5797 Bagher Z, Azami M, Ebrahimi-Barough S, Mirzadeh H, Solouk A, Soleimani M, Ai J, Nourani MR, Joghataei MT (2016) Differentiation of Wharton’s Jelly-derived mesenchymal stem cells into motor neuron-like cells on three-dimensional collagen-grafted nanofibers. Mol Neurobiol 53:2397–2408 Li CW, Davis B, Shea J, Sant H, Gale BK, Agarwal J (2018) Optimization of micropatterned poly(lactic-co-glycolic acid) films for enhancing dorsal root ganglion cell orientation and extension. Neural Regener Res 13:105–111 Dalby MJ, Riehle MO, Yarwood SJ, Wilkinson CDW, Curtis ASG (2003) Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography. Exp Cell Res 284:274–282 Hsu SH, Lu PS, Ni HC, Su CH (2007) Fabrication and evaluation of microgrooved polymers as peripheral nerve conduits. Biomed Microdevice 9:665–674 Goldner JS, Bruder JM, Li G, Gazzola D, Hoffman-Kim D (2006) Neurite bridging across micropatterned grooves. Biomaterials 27:460–472 George JH, Nagel D, Waller S, Hill E, Parri HR, Coleman MD, Cui ZF, Ye H (2018) A closer look at neuron interaction with track-etched microporous membranes. Sci Rep 8:1–11 Teo BKK, Ankam S, Chan LY, Yim EKF (2010) Nanotopography/mechanical induction of stem-cell differentiation. Nuclear Mech Genome Regul 98:241–294 Nguyen AT, Sathe SR, Yim EKF (2016) From nano to micro: topographical scale and its impact on cell adhesion, morphology and contact guidance. J Phys Condens Matter 28:183001 Simitzi C, Karali K, Ranella A, Stratakis E (2018) Controlling the outgrowth and functions of neural stem cells: the effect of surface topography. Chem Phys Chem 19:1143–1163 Chua JS, Chng CP, Moe AAK, Tann JY, Goh ELK, Chiam KH, Yim EKF (2014) Extending neurites sense the depth of the underlying topography during neuronal differentiation and contact guidance. Biomaterials 35:7750–7761 Roach P, Parker T, Gadegaard N, Alexander MR (2010) Surface strategies for control of neuronal cell adhesion: a review. Surf Sci Rep 65:145–173 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 Togari A, Dickens G, Kuzuya H, Guroff G (1985) The effect of fibroblast growth-factor on Pc12 cells. J Neurosci 5:307–316 Li RX, Kong Y, Ladisch S (1998) Nerve growth factor-induced neurite formation in PC12 cells is independent of endogenous cellular gangliosides. Glycobiology 8:597–603 Vaudry D, Stork PJS, Lazarovici P, Eiden LE (2002) Signaling pathways for PC12 cell differentiation: making the right connections. Science 296:1648–1649 Kuang SK, Yang X, Wang Z, Huang T, Kindy M, Xi T, Gao BZ (2016) How microelectrode array-based chick forebrain neuron biosensors respond to glutamate NMDA receptor antagonist AP5 and GABAA receptor antagonist musimol. Sens Bio-Sens Res 10:9–14 Fjelldal MF, Freyd T, Evenseth LM, Sylte I, Ring A, Paulsen RE (2019) Exploring the overlapping binding sites of ifenprodil and EVT-101 in GluN2B-containing NMDA receptors using novel chicken embryo forebrain cultures and molecular modeling. Pharmacol Res Perspect 7:e00480 Foley JD, Grunwald EW, Nealey PF, Murphy CJ (2005) Cooperative modulation of neuritogenesis by PC12 cells by topography and nerve growth factor. Biomaterials 26:3639–3644 Tian LL, Prabhakaran MP, Hu J, Chen ML, Besenbacher F, Ramakrishna S (2016) Synergistic effect of topography, surface chemistry and conductivity of the electrospun nanofibrous scaffold on cellular response of PC12 cells. Colloids Surf B 145:420–429 Erdman NR (2016) Creation of a pioneer-neuron axonal pathfinding model for future use in developmental neurotoxicity testing applications, Ph.D. Thesis, Clemson University, United State Pettmann B, Louis JC, Sensenbrenner M (1979) Morphological and biochemical maturation of neurones cultured in the absence of glial cells. Nature 281:378–380 Arfsten J, Bradtmoller C, Kampen I, Kwade A (2008) Compressive testing of single yeast cells in liquid environment using a nanoindentation system. J Mater Res 23:3153–3160 Ahmad MR, Nakajima M, Kojima S, Homma M, Fukuda T (2010) Nanoindentation methods to measure viscoelastic properties of single cells using sharp, flat, and buckling tips inside esem. IEEE Trans Nanobiosci 9:12–23 Kuznetsova TG, Starodubtseva MN, Yegorenkov NI, Chizhik SA, Zhdanov RI (2007) Atomic force microscopy probing of cell elasticity. Micron 38:824–833 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 Qian J, Wang J, Gao H (2008) Lifetime and strength of adhesive molecular bond clusters between elastic media. Langmuir 24:1262–1270 Zhang WL, Lin Y, Qian J, Chen WQ, Gao H (2013) Tuning molecular adhesion via material anisotropy. Adv Func Mater 23:4729–4738 Aeschlimann M (2000) Biophysical models of axonal pathfinding, Ph.D. Thesis, University of Lausanne, Switzerland Yin J, Coutris N, Huang Y (2011) Investigation of inner surface groove formation under radially inward pressure during immersion precipitation-based hollow fiber membrane fabrication. J Manufact Sci Eng Trans Asme 133:587–626 Gong Z (2017) Physical understanding of cells and cell-ECM interactions, Ph.D. Thesis, University of Hong Kong, Hong Kong SAR 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 107:665–674 Kobayashi N, Mundel P (1997) A role of microtubules during the formation of cell processes in neuronal and nonneuronal cells. Cell Tissue Res 291:163–174 Kiddie G, McLean D, Van Ooyen A, Graham B (2005) Biologically plausible models of neurite outgrowth. Prog Brain Res 147:67–80 Yin J, Coutris N, Huang Y (2012) Numerical study of axonal outgrowth in grooved nerve conduits. J Neural Eng 9:056001 Raffa V, Falcone F, De Vincentiis S, Falconieri A, Calatayud MP, Goya GF, Cuschieri A (2018) Piconewton mechanical forces promote neurite growth. Biophys J 115:2026–2033 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 Szymanski JM, Zhang KR, Feinberg AW (2017) Measuring the Poisson’s ratio of fibronectin using engineered nanofibers. Sci Rep 7:1–9 Ouyang H, Nauman E, Shi RY (2013) Contribution of cytoskeletal elements to the axonal mechanical properties. J Biol Eng 7:21 Fass JN, Odde DJ (2003) Tensile force-dependent neurite elicitation via anti-beta 1 integrin antibody-coated magnetic beads. Biophys J 85:623–636 Riggio C, Calatayud MP, Giannaccini M, Sanz B, Torres TE, Fernandez-Pacheco R, Ripoli A, Ibarra MR, Dente L, Cuschieri A, Goya GF, Raffa V (2014) The orientation of the neuronal growth process can be directed via magnetic nanoparticles under an applied magnetic field. Nanomed Nanotechnol Biol Med 10:1549–1558 O’Toole M, Lamoureux P, Miller KE (2008) A Physical model of axonal elongation: force, viscosity, and adhesions govern the mode of outgrowth. Biophys J 94:2610–2620 Hoffman-Kim D, Mitchel JA, Bellamkonda RV (2010) Topography, Cell response, and nerve regeneration. Annu Rev Biomed Eng 12:203–231 Omotade OF, Pollitt SL, Zheng JQ (2017) Actin-based growth cone motility and guidance. Mol Cell Neurosci 84:4–10 Lowery LA, Van Vactor D (2009) The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol 10:332–343 Abe K, Katsuno H, Toriyama M, Baba K, Mori T, Hakoshima T, Kanemura Y, Watanabe R, Inagaki N (2018) Grip and slip of L1-CAM on adhesive substrates direct growth cone haptotaxis. Proc Natl Acad Sci USA 115:2764–2769 Li NZ, Folch A (2005) Integration of topographical and biochemical cues by axons during growth on microfabricated 3-D substrates. Exp Cell Res 311:307–316 Goriely A, Budday S, Kuhl E (2015) Neuromechanics: from Neurons to Brain. Adv Appl Mech 48:79–139 Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G, Sabanay I, Mahalu D, Safran S, Bershadsky A, Addadi L, Geiger B (2001) Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol 3:466–472 Sarangi BR, Gupta M, Doss BL, Tissot N, Lam F, Mege RM, Borghi N, Ladoux B (2017) Coordination between intra- and extracellular forces regulates focal adhesion dynamics. Nano Lett 17:399–406 Goodno BJ, Gere JM (2018) Mechanics of materials, 9th edn. Cengage Learning, Boston Beer FP, Johnston ER Jr, DeWolf JT, Mazurek DF (2017) Statics and mechanics of materials, 2nd edn. McGraw-Hill Education, New York Gao HJ, Qian J, Chen B (2011) Probing mechanical principles of focal contacts in cell-matrix adhesion with a coupled stochastic-elastic modelling framework. J R Soc Interface 8:1217–1232