Schwann cell durotaxis can be guided by physiologically relevant stiffness gradients |
Evans, Elisabeth B.
(Department of Molecular Pharmacology, Physiology, Brown University)
Brady, Samantha W. (Department of Molecular Pharmacology, Physiology, Brown University) Tripathi, Anubhav (Department of Molecular Pharmacology, Physiology, Brown University) Hoffman-Kim, Diane (Department of Molecular Pharmacology, Physiology, Brown University) |
1 | Wong JY, Velasco A, Rajagopalan P, Pham Q. Directed Movement of Vascular Smooth Muscle Cells on Gradient-Compliant Hydrogels . 2003. https://doi.org/10.1021/LA026403P. DOI |
2 | Tse JR, Engler AJ, Tse JR, Engler AJ. Preparation of Hydrogel Substrates with Tunable Mechanical Properties. In: Curr Protoc Cell Biol. Hoboken: Wiley; 2010. p. 10-161101616. https://doi.org/10.1002/0471143030. cb1016s47. http://doi.wiley.com/10.1002/0471143030.cb1016s47. DOI |
3 | Takigawa T, Morino Y, Urayama K, Masuda T. Osmotic Poisson's Ratio and Equilibrium Stress of Poly(acrylamide) Gels. Polymer J. 1996;28(11): 1012-3. https://doi.org/10.1295/polymj.28.1012. DOI |
4 | Nectow AR, Marra KG, Kaplan DL. Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng Part B Rev. 2012;18(1): 40-50. https://doi.org/10.1089/ten.TEB.2011.0240. DOI |
5 | Urbanski MM, Kingsbury L, Moussouros D, Kassim I, Mehjabeen S, Paknejad N, Melendez-Vasquez CV. Myelinating glia differentiation is regulated by extracellular matrix elasticity. Sci Rep. 2016;6:33751. https://doi.org/10.1038/srep33751. DOI |
6 | Franze K, Janmey PA, Guck J. Mechanics in Neuronal Development and Repair. Annu Rev Biomed Eng. 15(1):227-51. https://doi.org/10.1146/annurev-bioeng-071811-150045. |
7 | Wang HB, Dembo M, Hanks SK, Wang Y. Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc Natl Acad Sci U S A. 2001;98(20):11295-300. https://doi.org/10.1073/pnas.201201198. DOI |
8 | Wakatsuki S, Araki T, Sehara-Fujisawa A. Neuregulin-1/glial growth factor stimulates Schwann cell migration by inducing integrin-ErbB2- focal adhesion kinase complex formation. Genes Cells Devoted Mol Cellular Mech. 2014;19(1):66-77. https://doi.org/10.1111/gtc.12108. DOI |
9 | Chen LM, Bailey D, Fernandez-Valle C. Association of beta 1 integrin with focal adhesion kinase and paxillin in differentiating Schwann cells. J Neurosci Official J Soc Neurosci. 2000;20(10):3776-84. DOI |
10 | Lo CM, Wang HB, Dembo M, Wang Y-L. Cell movement is guided by the rigidity of the substrate. Biophys J. 2000;79(1):144-52. https://doi.org/10.1016/S0006-3495(00)76279-5. DOI |
11 | Isenberg BC, Dimilla PA, Walker M, Kim S, Wong JY. Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength. Biophys J. 2009;97(5):1313-22. https://doi.org/10.1016/j.bpj.2009.06.021. DOI |
12 | Farrell BE, Daniele RP, Lauffenburger DA. Quantitative relationships between single-cell and cell-population model parameters for chemosensory migration responses of alveolar macrophages to C5a. Cell Motil Cytoskeleton. 1990;16(4):279-93. https://doi.org/10.1002/cm.970160407. DOI |
13 | Georges PC, Miller WJ, Meaney DF, Sawyer ES, Janmey PA. Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys J. 2006;90(8):3012-8. https://doi.org/10.1529/BIOPHYSJ.105.073114. DOI |
14 | Bhana B, Iyer RK, Chen WLK, Zhao R, Sider KL, Likhitpanichkul M, Simmons CA, Radisic M. Influence of substrate stiffness on the phenotype of heart cells. Biotechnol Bioeng. 2010;105(6):. https://doi.org/10.1002/bit.22647. |
15 | Fallenstein GT, Hulce VD, Melvin JW. Dynamic mechanical properties of human brain tissue. J Biomech. 1969;2(3):217-26. https://doi.org/10.1016/0021-9290(69)90079-7. DOI |
16 | Solon J, Levental I, Sengupta K, Georges PC, Janmey PA. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J. 2007;93(12):4453-61. https://doi.org/10.1529/BIOPHYSJ.106.101386. DOI |
17 | Moshayedi P, da F Costa L, Christ A, Lacour SP, Fawcett J, Guck J, Franze K. Mechanosensitivity of astrocytes on optimized polyacrylamide gels analyzed by quantitative morphometry. J Phys Condens Matter. 2010;22(19):194114. https://doi.org/10.1088/0953-8984/22/19/194114. DOI |
18 | Cordelieres FP, Schindelin J. Manual Tracking Image J Plugin. Version 2.1.1. URL: https://imagej.net/Manual%20Tracking. |
19 | Islam A, Younesi M, Mbimba T, Akkus O. Collagen substrate stiffness anisotropy affects cellular elongation, nuclear shape, and stem cell fate toward anisotropic tissue lineage. Adv Healthcare Mater. 2016;5(17):2237-47. https://doi.org/10.1002/adhm.201600284. DOI |
20 | Grevesse T, Versaevel M, Circelli G, Desprez S, Gabriele S. A simple route to functionalize polyacrylamide hydrogels for the independent tuning of mechanotransduction cues. Lab Chip. 2013;13(5):777. https://doi.org/10.1039/c2lc41168g. DOI |
21 | Maniotis AJ, Chen CS, Ingber DE. Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci U S A. 1997;94(3): 849-54. DOI |
22 | Lovett DB, Shekhar N, Nickerson JA, Roux KJ, Lele TP. Modulation of Nuclear Shape by Substrate Rigidity. Cel Mol Bioeng. 2013;6(2):230-8. https://doi.org/10.1007/s12195-013-0270-2. DOI |
23 | Jessen KR, Mirsky R. The repair Schwann cell and its function in regenerating nerves. J Physiol. 2016;594(13):3521-1. https://doi.org/10.1113/JP270874. DOI |
24 | Stoll G, Muller HW. Nerve injury, axonal degeneration and neural regeneration: basic insights. Brain Pathol (Zurich, Switzerland). 1999;9(2):313-25. |
25 | Previtera ML, Langhammer CG, Langrana NA, Firestein BL. Regulation of dendrite arborization by substrate stiffness is mediated by glutamate receptors. Ann Biomed Eng. 2010;38(12):3733-43. https://doi.org/10.1007/s10439-010-0112-5. DOI |
26 | Flanagan LA, Ju YE, Marg B, Osterfield M, Janmey PA. Neurite branching on deformable substrates. Neuroreport. 2002;13(18):2411-5. https://doi.org/10.1097/01.wnr.0000048003.96487.97. DOI |
27 | Cheung Y, Azeloglu E, Shiovitz D, Costa K, Seliktar D, Sia S. Microscale control of stiffness in a cell-adhesive substrate using microfluidics-based lithography. Angewandte Chemie Int Edition. 2009;48(39):7188-92. https://doi.org/10.1002/anie.200900807. DOI |
28 | Gomez-Sanchez JA, Pilch KS, van der Lans M, Fazal SV, Benito C, Wagstaff LJ, Mirsky R, Jessen KR. After Nerve Injury, Lineage Tracing Shows That Myelin and Remak Schwann Cells Elongate Extensively and Branch to Form Repair Schwann Cells, Which Shorten Radically on Remyelination. J Neurosci Official J Soc Neurosci. 2017;37(37):9086-99. https://doi.org/10.1523/JNEUROSCI.1453-17.2017. DOI |
29 | Parrinello S, Napoli I, Ribeiro S, Digby PW, Fedorova M, Parkinson DB, Doddrell RDS, Nakayama M, Adams RH, Lloyd AC. EphB signaling directs peripheral nerve regeneration through sox2-dependent Schwann cell sorting. Cell. 2010;143(1):145-55. https://doi.org/10.1016/j.cell.2010.08.039. DOI |
30 | Zaari N, Rajagopalan P, Kim SK, Engler AJ, Wong JY. Photopolymerization in microfluidic gradient generators: microscale control of substrate compliance to manipulate cell response. Adv Mater. 2004;16(23-24): 2133-7. https://doi.org/10.1002/adma.200400883. DOI |
31 | Hartman CD, Isenberg BC, Chua SG, Wong JY. Vascular smooth muscle cell durotaxis depends on extracellular matrix composition. https://doi.org/10.1073/pnas.1611324113. DOI |
32 | Kidoaki S, Sakashita H. Rectified cell migration on saw-like micro-elastically patterned hydrogels with asymmetric gradient ratchet teeth. PloS ONE. 2013;8(10):78067. https://doi.org/10.1371/journal.pone.0078067. DOI |
33 | Kloxin AM, Benton JA, Anseth KS. In situ elasticity modulation with dynamic substrates to direct cell phenotype. Biomaterials. 2010;31(1):1-8. https://doi.org/10.1016/j.biomaterials.2009.09.025. DOI |
34 | Bollmann L, Koser DE, Shahapure R, Gautier HOB, Holzapfel GA, Scarcelli G, Gather MC, Ulbricht E, Franze K. Microglia mechanics: immune activation alters traction forces and durotaxis. Front Cell Neurosci. 2015;9:363. https://doi.org/10.3389/fncel.2015.00363. |
35 | Marklein RA, Burdick JA. Spatially controlled hydrogel mechanics to modulate stem cell interactions. Soft Matter. 2010;6(1):136-43. https://doi.org/10.1039/B916933D. DOI |
36 | Williams LR, Longo FM, Powell HC, Lundborg G, Varon S. Spatial-temporal progress of peripheral nerve regeneration within a silicone chamber: parameters for a bioassay. J Comp Neurol. 1983;218(4): 460-70. https://doi.org/10.1002/cne.902180409. DOI |
37 | van Oosten ASG, Vahabi M, Licup AJ, Sharma A, Galie PA, MacKintosh FC, Janmey PA. Uncoupling shear and uniaxial elastic moduli of semiflexible biopolymer networks: compression-softening and stretch-stiffening. Sci Rep. 2016;6:19270. https://doi.org/10.1038/srep19270. DOI |
38 | Vladkova TG. Surface engineered polymeric biomaterials with improved biocontact properties. Int J Polymer Sci. 2010:1-22. https://doi.org/10.1155/2010/296094. |
39 | Rosen P, Misfeldt DS. Cell density determines epithelial migration in culture. Proc Natl Acad Sci U S A. 1980;77(8):4760-3. DOI |
40 | Sazonova OV, Lee KL, Isenberg BC, Rich CB, Nugent MA, Wong JY. Cell-cell interactions mediate the response of vascular smooth muscle cells to substrate stiffness. Biophys J. 2011;101(3):622-30. https://doi.org/10.1016/j.bpj.2011.06.051. DOI |
41 | Kuo C.-H. R, Xian J, Brenton JD, Franze K, Sivaniah E. Complex Stiffness Gradient Substrates for Studying Mechanotactic Cell Migration. Adv Mater. 2012;24(45):6059-64. https://doi.org/10.1002/adma.201202520. DOI |
42 | Vincent LG, Choi YS, Alonso-Latorre B, del Alamo JC, Engler AJ. Mesenchymal stem cell durotaxis depends on substrate stiffness gradient strength. Biotechnol J. 2013;8(4):472-84. https://doi.org/10.1002/biot.201200205. DOI |
43 | Hadden WJ, Young JL, Holle AW, McFetridge ML, Kim DY, Wijesinghe P, Taylor-Weiner H, Wen JH, Lee AR, Bieback K, Vo BN, Sampson DD, Kennedy BF, Spatz JP, Engler AJ, Choi YS. Stem cell migration and mechanotransduction on linear stiffness gradient hydrogels. Proc Natl Acad Sci U S A. 2017;114(22):5647-52. https://doi.org/10.1073/pnas.1618239114. DOI |
44 | Pelham RJ, Wang YL. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci U S A. 1997;94(25):13661-5. DOI |
45 | Oakes PW, Patel DC, Morin NA, Zitterbart DP, Fabry B, Reichner JS, Tang JX. Neutrophil morphology and migration are affected by substrate elasticity. Blood. 2009;114(7):1387-95. https://doi.org/10.1182/blood-2008-11-191445. DOI |
46 | Balgude AP, Yu X, Szymanski A, Bellamkonda RV. Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures. Biomaterials. 2001;22(10):1077-84. https://doi.org/10.1016/S0142-9612(00)00350-1. DOI |
47 | Previtera ML, Langhammer CG, Firestein BL. Effects of substrate stiffness and cell density on primary hippocampal cultures. J Biosci Bioeng. 2010;110(4):459-70. https://doi.org/10.1016/j.jbiosc.2010.04.004. DOI |
48 | Rosso G, Liashkovich I, Young P, Rohr D, Shahin V. Schwann cells and neurite outgrowth from embryonic dorsal root ganglions are highly mechanosensitive. Nanomed Nanotechnol Biol Med. 2017;13(2):493-501. https://doi.org/10.1016/J.NANO.2016.06.011. DOI |
49 | Lopez-Fagundo C, Bar-Kochba E, Livi LL, Hoffman-Kim D, Franck C. Three-dimensional traction forces of Schwann cells on compliant substrates. J R Soc Interface. 2014;11(97):20140247. https://doi.org/10.1098/rsif.2014.0247. DOI |
50 | Chernousov MA, Yu WM, Chen ZL, Carey DJ, Strickland S. Regulation of Schwann cell function by the extracellular matrix. Glia. 2008;56(14): 1498-507. https://doi.org/10.1002/glia.20740. DOI |
51 | Hoffman-Kim D, Mitchel JA, Bellamkonda RV. Topography, cell response, and nerve regeneration. Annu Rev Biomed Eng. 2010;12:203-31. https://doi.org/10.1146/annurev-bioeng-070909-105351. DOI |
52 | Peyton SR, Putnam AJ. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J Cellular Physiol. 2005;204(1): 198-209. https://doi.org/10.1002/jcp.20274. DOI |
53 | Raucher D, Sheetz MP. Cell spreading and lamellipodial extension rate is regulated by membrane tension. J Cell Biol. 2000;148(1):127-36. https://doi.org/10.1083/JCB.148.1.127. DOI |
54 | Chen G, Zhang Z, Wei Z, Cheng Q, Li X, Li W, Duan S, Gu X. Lysosomal exocytosis in Schwann cells contributes to axon remyelination. Glia. 2012;60(2):295-305. https://doi.org/10.1002/glia.21263. DOI |
55 | Tse JR, Engler AJ. Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate. PloS ONE. 2011;6(1):15978. https://doi.org/10.1371/journal.pone.0015978. DOI |
56 | Belkas JS, Shoichet MS, Midha R. Peripheral nerve regeneration through guidance tubes. Neurol Res. 2004;26(2):151-60. https://doi.org/10.1179/016164104225013798. DOI |
57 | Engler A, Bacakova L, Newman C, Hategan A, Griffin M, Discher D. Substrate Compliance versus Ligand Density in Cell on Gel Responses. Biophys J. 2004;86(1):617-28. https://doi.org/10.1016/S0006-3495(04)74140-5. DOI |
58 | Kouyoumdjian JA. Peripheral nerve injuries: a retrospective survey of 456 cases. Muscle Nerve. 2006;34(6):785-8. https://doi.org/10.1002/mus.20624. DOI |