Generic placeholder image

Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

Review Article

Effects of Electrical Stimulation on Stem Cells

Author(s): Wang Heng*, Mit Bhavsar, Zhihua Han and John H. Barker

Volume 15, Issue 5, 2020

Page: [441 - 448] Pages: 8

DOI: 10.2174/1574888X15666200129154747

Price: $65

Abstract

Recent interest in developing new regenerative medicine- and tissue engineering-based treatments has motivated researchers to develop strategies for manipulating stem cells to optimize outcomes in these potentially, game-changing treatments. Cells communicate with each other, and with their surrounding tissues and organs via electrochemical signals. These signals originate from ions passing back and forth through cell membranes and play a key role in regulating cell function during embryonic development, healing, and regeneration. To study the effects of electrical signals on cell function, investigators have exposed cells to exogenous electrical stimulation and have been able to increase, decrease and entirely block cell proliferation, differentiation, migration, alignment, and adherence to scaffold materials. In this review, we discuss research focused on the use of electrical stimulation to manipulate stem cell function with a focus on its incorporation in tissue engineering-based treatments.

Keywords: Electrical stimulation (EStim), stem cells, tissue engineering (TE), bioelectricity, cell proliferation, cell function.

[1]
Goradel NH, Hour FG, Negahdari B, et al. Stem cell therapy: a new therapeutic option for cardiovascular diseases. J Cell Biochem 2018; 119(1): 95-104.
[http://dx.doi.org/10.1002/jcb.26169] [PMID: 28543595]
[2]
Sun C, Serra C, Lee G, Wagner KR. Stem cell-based therapies for Duchenne muscular dystrophy. Exp Neurol 2020; 323113086
[http://dx.doi.org/10.1016/j.expneurol.2019.113086] [PMID: 31639376]
[3]
Kim H, Hyun MR, Kim SW. The effect of adipose-derived stem cells on wound healing: comparison of methods of ap-plication. Stem Cells Int 2019; 20192745640
[http://dx.doi.org/10.1155/2019/2745640] [PMID: 31636674]
[4]
Trubiani O, Marconi GD, Pierdomenico SD, Piattelli A, Dio-mede F, Pizzicannella J. Human oral stem cells, biomaterials and extracellular vesicles: a promising tool in bone tissue re-pair. Int J Mol Sci 2019; 20(20)e4978
[http://dx.doi.org/10.3390/ijms20204987] [PMID: 31600911]
[5]
Sharma S, Gupta DK. Tissue engineering and stem cell therapy in pediatric urology. J Indian Assoc Pediatr Surg 2019; 24(4): 237-46.
[http://dx.doi.org/10.4103/jiaps.JIAPS_77_18] [PMID: 31571753]
[6]
Barbry P, Cavard A, Chanson M, Jaffe AB, Plasschaert LW. Regeneration of airway epithelial cells to study rare cell states in cystic fibrosis J Cyst Fibros 2019. S1569-1993(19)30894-X
[7]
Elkhenany H, El-Badri N, Dhar M. Green propolis extract promotes in vitro proliferation, differentiation, and migration of bone marrow stromal cells. Biomed Pharmacother 2019; 115108861
[http://dx.doi.org/10.1016/j.biopha.2019.108861] [PMID: 31005795]
[8]
Ohlstein B, Kai T, Decotto E, Spradling A. The stem cell niche: theme and variations. Curr Opin Cell Biol 2004; 16(6): 693-9.
[http://dx.doi.org/10.1016/j.ceb.2004.09.003] [PMID: 15530783]
[9]
Han CY, Liu J, Wan F, et al. Effects of Tianqijiangtang capsule on survival, self-renewal and differentiation of hippocampal neural stem cells of embryonic rats cultured in high glucose medium. Am J Transl Res 2019; 11(9): 5560-72.
[PMID: 31632529]
[10]
Zhang T, Liu C, Chi L. Suppression of miR-10a-5p in bone marrow mesenchymal stem cells enhances the therapeutic effect on spinal cord injury via BDNF. Neurosci Lett 2020; 714134562
[http://dx.doi.org/10.1016/j.neulet.2019.134562] [PMID: 31626878]
[11]
Bertucci TB, Dai G. Biomaterial engineering for controlling pluripotent stem cell fate. Stem Cells Int 2018; 20189068203
[http://dx.doi.org/10.1155/2018/9068203] [PMID: 30627175]
[12]
Richards D, Swift J, Wong LS, Richardson SM. Photorespon-sive hydrogels with photoswitchable stiffness: emerging plat-forms to study temporal aspects of mesenchymal stem cell re-sponses to extracellular stiffness regulation. Adv Exp Med Biol 2019; 1144: 53-69.
[http://dx.doi.org/10.1007/5584_2018_293] [PMID: 30456642]
[13]
Tse JR, Engler AJ. Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate. PLoS One 2011; 6(1)e15978
[http://dx.doi.org/10.1371/journal.pone.0015978] [PMID: 21246050]
[14]
Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126(4): 677-89.
[http://dx.doi.org/10.1016/j.cell.2006.06.044] [PMID: 16923388]
[15]
Park JS, Chu JS, Tsou AD, et al. The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-β. Biomaterials 2011; 32(16): 3921-30.
[http://dx.doi.org/10.1016/j.biomaterials.2011.02.019] [PMID: 21397942]
[16]
Sharma RI, Snedeker JG. Paracrine interactions between mesenchymal stem cells affect substrate driven differentiation toward tendon and bone phenotypes. PLoS One 2012; 7(2)e31504
[http://dx.doi.org/10.1371/journal.pone.0031504] [PMID: 22355373]
[17]
Ward DF Jr, Salasznyk RM, Klees RF, et al. Mechanical strain enhances extracellular matrix-induced gene focusing and promotes osteogenic differentiation of human mesenchymal stem cells through an extracellular-related kinase-dependent pathway. Stem Cells Dev 2007; 16(3): 467-80.
[http://dx.doi.org/10.1089/scd.2007.0034] [PMID: 17610377]
[18]
Young DA, Choi YS, Engler AJ, Christman KL. Stimulation of adipogenesis of adult adipose-derived stem cells using substrates that mimic the stiffness of adipose tissue. Biomaterials 2013; 34(34): 8581-8.
[http://dx.doi.org/10.1016/j.biomaterials.2013.07.103] [PMID: 23953825]
[19]
Takahashi J, Palmer TD, Gage FH. Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J Neurobiol 1999; 38(1): 65-81.
[http://dx.doi.org/10.1002/(SICI)1097-4695(199901)38:1<65:AID-NEU5>3.0.CO;2-Q] [PMID: 10027563]
[20]
Saha K, Keung AJ, Irwin EF, et al. Substrate modulus directs neural stem cell behavior. Biophys J 2008; 95(9): 4426-38.
[http://dx.doi.org/10.1529/biophysj.108.132217] [PMID: 18658232]
[21]
Pelham RJ Jr, Wang Yl. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 1997; 94(25): 13661-5.
[http://dx.doi.org/10.1073/pnas.94.25.13661] [PMID: 9391082]
[22]
Kamimura M, Sugawara M, Yamamoto S, Yamaguchi K, Nakanishi J. Dynamic control of cell adhesion on a stiffness-tunable substrate for analyzing the mechanobiology of collective cell migration. Biomater Sci 2016; 4(6): 933-7.
[http://dx.doi.org/10.1039/C6BM00100A] [PMID: 27048916]
[23]
Canver AC, Ngo O, Urbano RL, Clyne AM. Endothelial directed collective migration depends on substrate stiffness via localized myosin contractility and cell-matrix interactions. J Biomech 2016; 49(8): 1369-80.
[http://dx.doi.org/10.1016/j.jbiomech.2015.12.037] [PMID: 26792289]
[24]
Shukla VC, Higuita-Castro N, Nana-Sinkam P, Ghadiali SN. Substrate stiffness modulates lung cancer cell migration but not epithelial to mesenchymal transition. J Biomed Mater Res A 2016; 104(5): 1182-93.
[http://dx.doi.org/10.1002/jbm.a.35655] [PMID: 26779779]
[25]
Moazzem Hossain M, Wang X, Bergan RC, Jin JP. Diminished expression of h2-calponin in prostate cancer cells promotes cell proliferation, migration and the dependence of cell adhesion on substrate stiffness. FEBS Open Bio 2014; 4: 627-36.
[http://dx.doi.org/10.1016/j.fob.2014.06.003] [PMID: 25161871]
[26]
Elsaadany M, Winters K, Adams S, Stasuk A, Ayan H, Yildirim-Ayan E. Equiaxial strain modulates adipose-derived stem Cell differentiation within 3D biphasic scaffolds towards an-nulus fibrosus. Sci Rep 2017; 7(1): 12868.
[http://dx.doi.org/10.1038/s41598-017-13240-3] [PMID: 28993681]
[27]
Mao AS, Shin JW, Mooney DJ. Effects of substrate stiffness and cell-cell contact on mesenchymal stem cell differentiation. Biomaterials 2016; 98: 184-91.
[http://dx.doi.org/10.1016/j.biomaterials.2016.05.004] [PMID: 27203745]
[28]
Zhang N, Kohn DH. Using polymeric materials to control stem cell behavior for tissue regeneration. Birth Defects Res C Embryo Today 2012; 96(1): 63-81.
[http://dx.doi.org/10.1002/bdrc.21003] [PMID: 22457178]
[29]
Adorno-Cruz V, Liu H. Regulation and functions of integrin α2 in cell adhesion and disease. Genes Dis 2018; 6(1): 16-24.
[http://dx.doi.org/10.1016/j.gendis.2018.12.003] [PMID: 30906828]
[30]
Kalappurakkal JM, Anilkumar AA, Patra C, van Zanten TS, Sheetz MP, Mayor S. Integrin mechano-chemical signaling generates plasma membrane nanodomains that promote cell spreading. Cell 2019; 177(7): 1738-1756.e23.
[http://dx.doi.org/10.1016/j.cell.2019.04.037] [PMID: 31104842]
[31]
Cooper J, Giancotti FG. Integrin signaling in cancer: mecha-notransduction, stemness, epithelial plasticity, and therapeutic resistance. Cancer Cell 2019; 35(3): 347-67.
[http://dx.doi.org/10.1016/j.ccell.2019.01.007] [PMID: 30889378]
[32]
Xie H, Cao T, Franco-Obregón A, Rosa V. Graphene-induced osteogenic differentiation is mediated by the integrin/FAK ax-is. Int J Mol Sci 2019; 20(3)e574
[http://dx.doi.org/10.3390/ijms20030574] [PMID: 30699966]
[33]
Moreno-Vicente R, Pavón DM, Martín-Padura I, et al. Caveo-lin-1 modulates mechanotransduction responses to substrate stiffness through actin-dependent control of YAP. Cell Rep 2018; 25(6): 1622-1635.e6.
[http://dx.doi.org/10.1016/j.celrep.2018.10.024] [PMID: 30404014]
[34]
Dohi T, Padmanabhan J, Akaishi S, et al. The interplay of mechanical stress, strain, and stiffness at the keloid periphery correlates with increased caveolin-1/ROCK signaling and scar progression. Plast Reconstr Surg 2019; 144(1): 58e-67e.
[http://dx.doi.org/10.1097/PRS.0000000000005717] [PMID: 31246819]
[35]
Duchemin AL, Vignes H, Vermot J. Mechanically activated piezo channels modulate outflow tract valve development through the Yap1 and Klf2-Notch signaling axis eLife 2019; 8e44706
[http://dx.doi.org/10.7554/eLife.44706] [PMID: 31524599]
[36]
Deng J, Petersen BE, Steindler DA, Jorgensen ML, Laywell ED. Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 2006; 24(4): 1054-64.
[http://dx.doi.org/10.1634/stemcells.2005-0370] [PMID: 16322639]
[37]
Hofstetter CP, Schwarz EJ, Hess D, et al. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci USA 2002; 99(4): 2199-204.
[http://dx.doi.org/10.1073/pnas.042678299] [PMID: 11854516]
[38]
McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004; 6(4): 483-95.
[http://dx.doi.org/10.1016/S1534-5807(04)00075-9] [PMID: 15068789]
[39]
Jin L, Zhao W, Ren B, et al. Osteochondral tissue regenerated via a strategy by stacking pre-differentiated BMSC sheet on fibrous mesh in a gradient. Biomed Mater 2019; 14(6)065017
[http://dx.doi.org/10.1088/1748-605X/ab49e2] [PMID: 31574486]
[40]
Li WY, Zhu GY, Yue WJ, Sun GD, Zhu XF, Wang Y. KLF7 overexpression in bone marrow stromal stem cells graft transplantation promotes sciatic nerve regeneration. J Neural Eng 2019; 16(5)056011
[http://dx.doi.org/10.1088/1741-2552/ab3188] [PMID: 31296795]
[41]
Her GJ, Wu HC, Chen MH, Chen MY, Chang SC, Wang TW. Control of three-dimensional substrate stiffness to manipulate mesenchymal stem cell fate toward neuronal or glial lineages. Acta Biomater 2013; 9(2): 5170-80.
[http://dx.doi.org/10.1016/j.actbio.2012.10.012] [PMID: 23079022]
[42]
Oh SH, An DB, Kim TH, Lee JH. Wide-range stiffness gradient PVA/HA hydrogel to investigate stem cell differentiation behavior. Acta Biomater 2016; 35: 23-31.
[http://dx.doi.org/10.1016/j.actbio.2016.02.016] [PMID: 26883774]
[43]
Si Z, Wang X, Sun C, et al. Adipose-derived stem cells: Sources, potency, and implications for regenerative therapies. Biomed Pharmacother 2019; 114108765
[http://dx.doi.org/10.1016/j.biopha.2019.108765] [PMID: 30921703]
[44]
Choi YS, Vincent LG, Lee AR, Dobke MK, Engler AJ. Mechanical derivation of functional myotubes from adipose-derived stem cells. Biomaterials 2012; 33(8): 2482-91.
[http://dx.doi.org/10.1016/j.biomaterials.2011.12.004] [PMID: 22197570]
[45]
Xie J, Zhang D, Zhou C, Yuan Q, Ye L, Zhou X. Substrate elasticity regulates adipose-derived stromal cell differentiation towards osteogenesis and adipogenesis through β-catenin transduction. Acta Biomater 2018; 79: 83-95.
[http://dx.doi.org/10.1016/j.actbio.2018.08.018] [PMID: 30134207]
[46]
Major LG, Choi YS. Developing a high-throughput platform to direct adipogenic and osteogenic differentiation in adipose-derived stem cells. J Tissue Eng Regen Med 2018; 12(10): 2021-8.
[http://dx.doi.org/10.1002/term.2736] [PMID: 30053766]
[47]
Winer JP, Janmey PA, McCormick ME, Funaki M. Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng Part A 2009; 15(1): 147-54.
[http://dx.doi.org/10.1089/ten.tea.2007.0388] [PMID: 18673086]
[48]
Fernández D, Guerra M, Lisoni JG, et al. Fibrous materials made of poly(epsilon-caprolactone)/poly(ethylene oxide)-b-poly(epsilon-caprolactone) blends support neural stem cells differentiation. Polymers (Basel) 2019; 11(10): 1621.
[http://dx.doi.org/10.3390/polym11101621] [PMID: 31597231]
[49]
Nakajima M, Ishimuro T, Kato K, et al. Combinatorial protein display for the cell-based screening of biomaterials that direct neural stem cell differentiation. Biomaterials 2007; 28(6): 1048-60.
[http://dx.doi.org/10.1016/j.biomaterials.2006.10.004] [PMID: 17081602]
[50]
Cukierman E, Pankov R, Stevens DR, Yamada KM. Taking cell-matrix adhesions to the third dimension. Science 2001; 294(5547): 1708-12.
[http://dx.doi.org/10.1126/science.1064829] [PMID: 11721053]
[51]
Dusseiller MR, Smith ML, Vogel V, Textor M. Microfabricat-ed three-dimensional environments for single cell studies. Biointerphases 2006; 1(1): 1.
[http://dx.doi.org/10.1116/1.2190698] [PMID: 20408608]
[52]
Ochsner M, Textor M, Vogel V, Smith ML. Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape. PLoS One 2010; 5(3)e9445
[http://dx.doi.org/10.1371/journal.pone.0009445] [PMID: 20351781]
[53]
Zaman MH, Trapani LM, Sieminski AL, et al. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci USA 2006; 103(29): 10889-94.
[http://dx.doi.org/10.1073/pnas.0604460103] [PMID: 16832052]
[54]
Loessner D, Meinert C, Kaemmerer E, et al. Functionalization, preparation and use of cell-laden gelatin methacryloyl-based hydrogels as modular tissue culture platforms. Nat Protoc 2016; 11(4): 727-46.
[http://dx.doi.org/10.1038/nprot.2016.037] [PMID: 26985572]
[55]
Huebsch N, Arany PR, Mao AS, et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 2010; 9(6): 518-26.
[http://dx.doi.org/10.1038/nmat2732] [PMID: 20418863]
[56]
Žigon-Branc S, Markovic M, Van Hoorick J, et al. Impact of hydrogel stiffness on differentiation of human adipose-derived stem cell microspheroids. Tissue Eng Part A 2019; 25(19-20): 1369-80.
[http://dx.doi.org/10.1089/ten.tea.2018.0237] [PMID: 30632465]
[57]
Moffat KL, Sun WH, Pena PE, et al. Characterization of the structure-function relationship at the ligament-to-bone interface. Proc Natl Acad Sci USA 2008; 105(23): 7947-52.
[http://dx.doi.org/10.1073/pnas.0712150105] [PMID: 18541916]
[58]
Byron A. Analyzing the anatomy of integrin adhesions. Sci Signal 2011; 4(170): jc3.
[http://dx.doi.org/10.1126/scisignal.2001896] [PMID: 21521876]
[59]
Enemchukwu NO, Cruz-Acuña R, Bongiorno T, et al. Synthetic matrices reveal contributions of ECM biophysical and biochemical properties to epithelial morphogenesis. J Cell Biol 2016; 212(1): 113-24.
[http://dx.doi.org/10.1083/jcb.201506055] [PMID: 26711502]
[60]
Rape AD, Zibinsky M, Murthy N, Kumar S. A synthetic hydrogel for the high-throughput study of cell-ECM interactions. Nat Commun 2015; 6: 8129.
[http://dx.doi.org/10.1038/ncomms9129] [PMID: 26350361]
[61]
Steinmetz NJ, Aisenbrey EA, Westbrook KK, Qi HJ, Bryant SJ. Mechanical loading regulates human MSC differentiation in a multi-layer hydrogel for osteochondral tissue engineering. Acta Biomater 2015; 21: 142-53.
[http://dx.doi.org/10.1016/j.actbio.2015.04.015] [PMID: 25900444]
[62]
Nemir S, Hayenga HN, West JL. PEGDA hydrogels with patterned elasticity: Novel tools for the study of cell response to substrate rigidity. Biotechnol Bioeng 2010; 105(3): 636-44.
[http://dx.doi.org/10.1002/bit.22574] [PMID: 19816965]
[63]
Nemir S, West JL. Synthetic materials in the study of cell response to substrate rigidity. Ann Biomed Eng 2010; 38(1): 2-20.
[http://dx.doi.org/10.1007/s10439-009-9811-1] [PMID: 19816774]
[64]
Baker BM, Chen CS. Deconstructing the third dimension: how 3D culture microenvironments alter cellular cues. J Cell Sci 2012; 125(Pt 13): 3015-24.
[http://dx.doi.org/10.1242/jcs.079509] [PMID: 22797912]
[65]
Sabir MI, Xu XX, Li L. A review on biodegradable polymeric materials for bone tissue engineering applications. J Mater Sci 2009; 44(21): 5713-24.
[http://dx.doi.org/10.1007/s10853-009-3770-7]
[66]
Wozniak MA, Chen CS. Mechanotransduction in development: a growing role for contractility. Nat Rev Mol Cell Biol 2009; 10(1): 34-43.
[http://dx.doi.org/10.1038/nrm2592] [PMID: 19197330]
[67]
Ge S, Zhao N, Wang L, Liu H, Yang P. Effects of hydroxyapatite nanostructure on channel surface of porcine acellular dermal matrix scaffold on cell viability and osteogenic differentiation of human periodontal ligament stem cells. Int J Nanomedicine 2013; 8: 1887-95.
[http://dx.doi.org/10.2147/IJN.S44695] [PMID: 23690686]
[68]
Chaudhuri O, Gu L, Klumpers D, et al. Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat Mater 2016; 15(3): 326-34.
[http://dx.doi.org/10.1038/nmat4489] [PMID: 26618884]
[69]
Song Y, Ju Y, Morita Y, Xu B, Song G. Surface functionalization of nanoporous alumina with bone morphogenetic protein 2 for inducing osteogenic differentiation of mesenchymal stem cells. Mater Sci Eng C 2014; 37: 120-6.
[http://dx.doi.org/10.1016/j.msec.2014.01.004] [PMID: 24582231]
[70]
Badami AS, Kreke MR, Thompson MS, Riffle JS, Goldstein AS. Effect of fiber diameter on spreading, proliferation, and differentiation of osteoblastic cells on electrospun poly(lactic acid) substrates. Biomaterials 2006; 27(4): 596-606.
[http://dx.doi.org/10.1016/j.biomaterials.2005.05.084] [PMID: 16023716]
[71]
Boote C, Elsheikh A, Kassem W, et al. The influence of lamellar orientation on corneal material behavior: biomechanical and structural changes in an avian corneal disorder. Invest Ophthalmol Vis Sci 2011; 52(3): 1243-51.
[http://dx.doi.org/10.1167/iovs.10-5962] [PMID: 21051696]
[72]
Wang J, Chen H, Cao P, et al. Inflammatory cytokines induce caveolin-1/β-catenin signalling in rat nucleus pulposus cell apoptosis through the p38 MAPK pathway. Cell Prolif 2016; 49(3): 362-72.
[http://dx.doi.org/10.1111/cpr.12254] [PMID: 27125453]
[73]
Ren K, Tang J, Jiang X, et al. Periodic mechanical stress stimulates cav-1-dependent IGF-1R mitogenic signals in rat chondrocytes through ERK1/2. Cell Physiol Biochem 2018; 48(4): 1652-63.
[http://dx.doi.org/10.1159/000492288] [PMID: 30078012]
[74]
Yeh YC, Ling JY, Chen WC, Lin HH, Tang MJ. Mechanotransduction of matrix stiffness in regulation of focal adhesion size and number: reciprocal regulation of caveolin-1 and β1 integrin. Sci Rep 2017; 7(1): 15008.
[http://dx.doi.org/10.1038/s41598-017-14932-6] [PMID: 29118431]
[75]
Sohn J, Brick RM, Tuan RS. From embryonic development to human diseases: The functional role of caveolae/caveolin. Birth Defects Res C Embryo Today 2016; 108(1): 45-64.
[http://dx.doi.org/10.1002/bdrc.21121] [PMID: 26991990]
[76]
Lamaze C, Tardif N, Dewulf M, Vassilopoulos S, Blouin CM. The caveolae dress code: structure and signaling. Curr Opin Cell Biol 2017; 47: 117-25.
[http://dx.doi.org/10.1016/j.ceb.2017.02.014] [PMID: 28641181]
[77]
Du J, Chen X, Liang X, et al. Integrin activation and internalization on soft ECM as a mechanism of induction of stem cell differentiation by ECM elasticity. Proc Natl Acad Sci USA 2011; 108(23): 9466-71.
[http://dx.doi.org/10.1073/pnas.1106467108] [PMID: 21593411]
[78]
Volkers L, Mechioukhi Y, Coste B. Piezo channels: from structure to function. Pflugers Arch 2015; 467(1): 95-9.
[http://dx.doi.org/10.1007/s00424-014-1578-z] [PMID: 25037583]
[79]
Zhong M, Komarova Y, Rehman J, Malik AB. Mechanosensing Piezo channels in tissue homeostasis including their role in lungs. Pulm Circ 2018; 8(2)2045894018767393
[http://dx.doi.org/10.1177/2045894018767393] [PMID: 29521167]
[80]
Coste B, Mathur J, Schmidt M, et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 2010; 330(6000): 55-60.
[http://dx.doi.org/10.1126/science.1193270] [PMID: 20813920]
[81]
Pathak MM, Nourse JL, Tran T, et al. Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells. Proc Natl Acad Sci USA 2014; 111(45): 16148-53.
[http://dx.doi.org/10.1073/pnas.1409802111] [PMID: 25349416]
[82]
He L, Si G, Huang J, Samuel ADT, Perrimon N. Mechanical regulation of stem-cell differentiation by the stretch-activated Piezo channel. Nature 2018; 555(7694): 103-6.
[http://dx.doi.org/10.1038/nature25744] [PMID: 29414942]
[83]
Sugimoto A, Miyazaki A, Kawarabayashi K, et al. Piezo type mechanosensitive ion channel component 1 functions as a regulator of the cell fate determination of mesenchymal stem cells. Sci Rep 2017; 7(1): 17696.
[http://dx.doi.org/10.1038/s41598-017-18089-0] [PMID: 29255201]
[84]
Hu JK, Du W, Shelton SJ, Oldham MC, DiPersio CM, Klein OD. An FAK-YAP-mTOR signaling axis regulates stem cell-based tissue renewal in mice. Cell Stem Cell 2017; 21(1): 91-106.e6.
[http://dx.doi.org/10.1016/j.stem.2017.03.023] [PMID: 28457749]
[85]
Taniguchi K, Wu LW, Grivennikov SI, et al. A gp130-Src-YAP module links inflammation to epithelial regeneration. Nature 2015; 519(7541): 57-62.
[http://dx.doi.org/10.1038/nature14228] [PMID: 25731159]
[86]
Panciera T, Azzolin L, Cordenonsi M, Piccolo S. Mechanobiology of YAP and TAZ in physiology and disease. Nat Rev Mol Cell Biol 2017; 18(12): 758-70.
[http://dx.doi.org/10.1038/nrm.2017.87] [PMID: 28951564]
[87]
Dupont S, Morsut L, Aragona M, et al. Role of YAP/TAZ in mechanotransduction. Nature 2011; 474(7350): 179-83.
[http://dx.doi.org/10.1038/nature10137] [PMID: 21654799]
[88]
Musah S, Wrighton PJ, Zaltsman Y, et al. Substratum-induced differentiation of human pluripotent stem cells reveals the coactivator YAP is a potent regulator of neuronal specification. Proc Natl Acad Sci USA 2014; 111(38): 13805-10.
[http://dx.doi.org/10.1073/pnas.1415330111] [PMID: 25201954]
[89]
Tang Y, Rowe RG, Botvinick EL, et al. MT1-MMP-dependent control of skeletal stem cell commitment via a β1-integrin/YAP/TAZ signaling axis. Dev Cell 2013; 25(4): 402-16.
[http://dx.doi.org/10.1016/j.devcel.2013.04.011] [PMID: 23685250]
[90]
Pethő Z, Najder K, Bulk E, Schwab A. Mechanosensitive ion channels push cancer progression. Cell Calcium 2019; 80: 79-90.
[http://dx.doi.org/10.1016/j.ceca.2019.03.007] [PMID: 30991298]
[91]
Barnes SC, Lawless BM, Shepherd DET, Espino DM, Bicknell GR, Bryan RT. Viscoelastic properties of human bladder tumours. J Mech Behav Biomed Mater 2016; 61: 250-7.
[http://dx.doi.org/10.1016/j.jmbbm.2016.03.012] [PMID: 27082128]
[92]
Liu Z, Bilston L. On the viscoelastic character of liver tissue: experiments and modelling of the linear behaviour. Biorheology 2000; 37(3): 191-201.
[PMID: 11026939]
[93]
Sack I, Beierbach B, Hamhaber U, Klatt D, Braun J. Non-invasive measurement of brain viscoelasticity using magnetic resonance elastography. NMR Biomed 2008; 21(3): 265-71.
[http://dx.doi.org/10.1002/nbm.1189] [PMID: 17614101]
[94]
Chaudhuri O, Gu L, Darnell M, et al. Substrate stress relaxation regulates cell spreading. Nat Commun 2015; 6: 6364.
[http://dx.doi.org/10.1038/ncomms7365] [PMID: 25695512]
[95]
Lee HP, Gu L, Mooney DJ, Levenston ME, Chaudhuri O. Mechanical confinement regulates cartilage matrix formation by chondrocytes. Nat Mater 2017; 16(12): 1243-51.
[http://dx.doi.org/10.1038/nmat4993] [PMID: 28967913]
[96]
Nicodemus GD, Skaalure SC, Bryant SJ. Gel structure has an impact on pericellular and extracellular matrix deposition, which subsequently alters metabolic activities in chondrocyte-laden PEG hydrogels. Acta Biomater 2011; 7(2): 492-504.
[http://dx.doi.org/10.1016/j.actbio.2010.08.021] [PMID: 20804868]
[97]
Schuh E, Hofmann S, Stok KS, Notbohm H, Müller R, Rotter N. The influence of matrix elasticity on chondrocyte behavior in 3D. J Tissue Eng Regen Med 2012; 6(10): e31-42.
[http://dx.doi.org/10.1002/term.501] [PMID: 22034455]
[98]
Tamate R, Ueki T, Kitazawa Y, Kuzunuki M, Watanabe M, Akimoto AM, et al. Photo-dimerization induced dynamic vis-coelastic changes in ABA triblock copolymer-based hydrogels for 3D cell culture. Chem Mater 2016; 28(17): 6401-8.
[http://dx.doi.org/10.1021/acs.chemmater.6b02839]
[99]
Lou J, Stowers R, Nam S, Xia Y, Chaudhuri O. Stress relaxing hyaluronic acid-collagen hydrogels promote cell spreading, fiber remodeling, and focal adhesion formation in 3D cell culture. Biomaterials 2018; 154: 213-22.
[http://dx.doi.org/10.1016/j.biomaterials.2017.11.004] [PMID: 29132046]
[100]
Charrier EE, Pogoda K, Wells RG, Janmey PA. Control of cell morphology and differentiation by substrates with independently tunable elasticity and viscous dissipation. Nat Commun 2018; 9(1): 449.
[http://dx.doi.org/10.1038/s41467-018-02906-9] [PMID: 29386514]
[101]
Czeisler C, Short A, Nelson T, et al. Surface topography during neural stem cell differentiation regulates cell migration and cell morphology. J Comp Neurol 2016; 524(17): 3485-502.
[http://dx.doi.org/10.1002/cne.24078] [PMID: 27418162]
[102]
Song W, Lu H, Kawazoe N, Chen G. Adipogenic differentiation of individual mesenchymal stem cell on different geometric micropatterns. Langmuir 2011; 27(10): 6155-62.
[http://dx.doi.org/10.1021/la200487w] [PMID: 21486006]
[103]
Biggs MJP, Richards RG, Dalby MJ. Nanotopographical modification: a regulator of cellular function through focal adhesions. Nanomedicine (Lond) 2010; 6(5): 619-33.
[http://dx.doi.org/10.1016/j.nano.2010.01.009] [PMID: 20138244]
[104]
Pemberton GD, Childs P, Reid S, et al. Nanoscale stimulation of osteoblastogenesis from mesenchymal stem cells: nanotopography and nanokicking. Nanomedicine (Lond) 2015; 10(4): 547-60.
[http://dx.doi.org/10.2217/nnm.14.134] [PMID: 25723089]
[105]
Ye K, Wang X, Cao L, et al. Matrix stiffness and nanoscale spatial organization of cell-adhesive ligands direct stem cell fate. Nano Lett 2015; 15(7): 4720-9.
[http://dx.doi.org/10.1021/acs.nanolett.5b01619] [PMID: 26027605]
[106]
Chang B, Ma C, Liu X. Nanofibers regulate single bone mar-row stem cell osteogenesis via FAK/RhoA/YAP1 pathway. ACS Appl Mater Interfaces 2018; 10(39): 33022-31.
[http://dx.doi.org/10.1021/acsami.8b11449] [PMID: 30188689]
[107]
Liu C, Zhu C, Li J, et al. The effect of the fibre orientation of electrospun scaffolds on the matrix production of rabbit annulus fibrosus-derived stem cells. Bone Res 2015; 3: 15012.
[http://dx.doi.org/10.1038/boneres.2015.12] [PMID: 26273539]
[108]
Chu G, Yuan Z, Zhu C, et al. Substrate stiffness- and topography-dependent differentiation of annulus fibrosus-derived stem cells is regulated by Yes-associated protein. Acta Biomater 2019; 92: 254-64.
[http://dx.doi.org/10.1016/j.actbio.2019.05.013] [PMID: 31078765]
[109]
Ma C, Kuzma ML, Bai X, Yang J. Biomaterial-based metabolic regulation in regenerative engineering. Adv Sci (Weinh) 2019; 6(19)1900819
[http://dx.doi.org/10.1002/advs.201900819] [PMID: 31592416]
[110]
Rasi Ghaemi S, Delalat B, Cavallaro A, Mierczynska-Vasilev A, Vasilev K, Voelcker NH. Differentiation of rat mesenchy-mal stem cells toward osteogenic lineage on extracellular ma-trix protein gradients. Adv Healthc Mater 2019; 8(17)e1900595
[http://dx.doi.org/10.1002/adhm.201900595] [PMID: 31328896]
[111]
Guo J, Li C, Ling S, Huang W, Chen Y, Kaplan DL. Multiscale design and synthesis of biomimetic gradient protein/biosilica composites for interfacial tissue engineering. Biomaterials 2017; 145: 44-55.
[http://dx.doi.org/10.1016/j.biomaterials.2017.08.025] [PMID: 28843732]
[112]
Madhurakkat Perikamana SK, Lee J, Ahmad T, et al. Harnessing biochemical and structural cues for tenogenic differentiation of adipose derived stem cells (ADSCs) and development of an in vitro tissue interface mimicking tendon-bone insertion graft. Biomaterials 2018; 165: 79-93.
[http://dx.doi.org/10.1016/j.biomaterials.2018.02.046] [PMID: 29522987]
[113]
Wang X, Wenk E, Zhang X, Meinel L, Vunjak-Novakovic G, Kaplan DL. Growth factor gradients via microsphere delivery in biopolymer scaffolds for osteochondral tissue engineering. J Control Release 2009; 134(2): 81-90.
[http://dx.doi.org/10.1016/j.jconrel.2008.10.021] [PMID: 19071168]
[114]
Li X, Xie J, Lipner J, Yuan X, Thomopoulos S, Xia Y. Nanofiber scaffolds with gradations in mineral content for mimicking the tendon-to-bone insertion site. Nano Lett 2009; 9(7): 2763-8.
[http://dx.doi.org/10.1021/nl901582f] [PMID: 19537737]
[115]
Fu J, Wang YK, Yang MT, et al. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat Methods 2010; 7(9): 733-6.
[http://dx.doi.org/10.1038/nmeth.1487] [PMID: 20676108]
[116]
Song Y, Tang Y, Song J, et al. Cyclic mechanical stretch enhances BMP9-induced osteogenic differentiation of mesenchymal stem cells. Int Orthop 2018; 42(4): 947-55.
[http://dx.doi.org/10.1007/s00264-018-3796-z] [PMID: 29429074]
[117]
Song G, Ju Y, Shen X, Luo Q, Shi Y, Qin J. Mechanical stretch promotes proliferation of rat bone marrow mesenchymal stem cells. Colloids Surf B Biointerfaces 2007; 58(2): 271-7.
[http://dx.doi.org/10.1016/j.colsurfb.2007.04.001] [PMID: 17499488]
[118]
Wu Y, Zhang P, Dai Q, et al. Effect of mechanical stretch on the proliferation and differentiation of BMSCs from ovariectomized rats. Mol Cell Biochem 2013; 382(1-2): 273-82.
[http://dx.doi.org/10.1007/s11010-013-1744-1] [PMID: 23842623]
[119]
Zhong W, Tian K, Zheng X, et al. Mesenchymal stem cell and chondrocyte fates in a multishear microdevice are regulated by Yes-associated protein. Stem Cells Dev 2013; 22(14): 2083-93.
[http://dx.doi.org/10.1089/scd.2012.0685] [PMID: 23442010]
[120]
Hosseini MS, Tafazzoli-Shadpour M, Haghighipour N, Aghdami N, Goodarzi A. The synergistic effects of shear stress and cyclic hydrostatic pressure modulate chondrogenic induction of human mesenchymal stem cells. Int J Artif Organs 2015; 38(10): 557-64.
[http://dx.doi.org/10.5301/ijao.5000433] [PMID: 26541277]
[121]
Bao X, Li Z, Liu H, et al. Stimulation of chondrocytes and chondroinduced mesenchymal stem cells by osteoinduced mesenchymal stem cells under a fluid flow stimulus on an integrated microfluidic device. Mol Med Rep 2018; 17(2): 2277-88.
[PMID: 29207069]
[122]
Choi JR, Yong KW, Choi JY. Effects of mechanical loading on human mesenchymal stem cells for cartilage tissue engineering. J Cell Physiol 2018; 233(3): 1913-28.
[http://dx.doi.org/10.1002/jcp.26018] [PMID: 28542924]
[123]
Panadero JA, Lanceros-Mendez S, Ribelles JL. Differentiation of mesenchymal stem cells for cartilage tissue engineering: Individual and synergetic effects of three-dimensional environment and mechanical loading. Acta Biomater 2016; 33: 1-12.
[http://dx.doi.org/10.1016/j.actbio.2016.01.037] [PMID: 26826532]
[124]
Szychlinska MA, Stoddart MJ, D’Amora U, Ambrosio L, Alini M, Musumeci G. Mesenchymal stem cell-based cartilage re-generation approach and cell senescence: can we manipulate cell aging and function? Tissue Eng Part B Rev 2017; 23(6): 529-39.
[http://dx.doi.org/10.1089/ten.teb.2017.0083] [PMID: 28514935]
[125]
Fahy N, Alini M, Stoddart MJ. Mechanical stimulation of mesenchymal stem cells: Implications for cartilage tissue engineering. J Orthop Res 2018; 36(1): 52-63.
[PMID: 28763118]
[126]
Wu S, Wang Y, Streubel PN, Duan B. Living nanofiber yarn-based woven biotextiles for tendon tissue engineering using cell tri-culture and mechanical stimulation. Acta Biomater 2017; 62: 102-15.
[http://dx.doi.org/10.1016/j.actbio.2017.08.043] [PMID: 28864251]
[127]
Wang JH, Yang G, Li Z, Shen W. Fibroblast responses to cyclic mechanical stretching depend on cell orientation to the stretching direction. J Biomech 2004; 37(4): 573-6.
[http://dx.doi.org/10.1016/j.jbiomech.2003.09.011] [PMID: 14996570]
[128]
West JR, Juncosa N, Galloway MT, Boivin GP, Butler DL. Characterization of in vivo Achilles tendon forces in rabbits during treadmill locomotion at varying speeds and inclinations. J Biomech 2004; 37(11): 1647-53.
[http://dx.doi.org/10.1016/j.jbiomech.2004.02.019] [PMID: 15388306]
[129]
Juncosa N, West JR, Galloway MT, Boivin GP, Butler DL. In vivo forces used to develop design parameters for tissue engineered implants for rabbit patellar tendon repair. J Biomech 2003; 36(4): 483-8.
[http://dx.doi.org/10.1016/S0021-9290(02)00459-1] [PMID: 12600338]
[130]
Butler DL, Goldstein SA, Guilak F. Functional tissue engineering: the role of biomechanics. J Biomech Eng 2000; 122(6): 570-5.
[http://dx.doi.org/10.1115/1.1318906] [PMID: 11192376]
[131]
Li C, Pan J, Ye L, et al. Autophagy regulates the therapeutic potential of adipose-derived stem cells in LPS-induced pulmonary microvascular barrier damage. Cell Death Dis 2019; 10(11): 804.
[http://dx.doi.org/10.1038/s41419-019-2037-8] [PMID: 31645547]
[132]
Marsh SE, Blurton-Jones M. Neural stem cell therapy for neurodegenerative disorders: The role of neurotrophic support. Neurochem Int 2017; 106: 94-100.
[http://dx.doi.org/10.1016/j.neuint.2017.02.006] [PMID: 28219641]
[133]
Gandhimathi C, Quek YJ, Ezhilarasu H, Ramakrishna S, Bay BH, Srinivasan DK. Osteogenic differentiation of mesenchy-mal stem cells with silica-coated gold nanoparticles for bone tissue engineering. Int J Mol Sci 2019; 20(20)e5135
[http://dx.doi.org/10.3390/ijms20205135] [PMID: 31623264]
[134]
Qasim M, Chae DS, Lee NY. Bioengineering strategies for bone and cartilage tissue regeneration using growth factors and stem cells. J Biomed Mater Res A 2020; 108(3): 394-411.
[http://dx.doi.org/10.1002/jbm.a.36817] [PMID: 31618509]
[135]
Müller P, Lemcke H, David R. Stem cell therapy in heart dis-eases - cell types, mechanisms and improvement strategies. Cell Physiol Biochem 2018; 48(6): 2607-55.
[http://dx.doi.org/10.1159/000492704] [PMID: 30121644]
[136]
Abraham A, Krasnodembskaya A. Mesenchymal stem cell-derived extracellular vesicles for the treatment of acute respiratory distress syndrome. Stem Cells Transl Med 2020; 9(1): 28-38.
[http://dx.doi.org/10.1002/sctm.19-0205] [PMID: 31647191]
[137]
Duncan T, Valenzuela M. Alzheimer’s disease, dementia, and stem cell therapy. Stem Cell Res Ther 2017; 8(1): 111.
[http://dx.doi.org/10.1186/s13287-017-0567-5] [PMID: 28494803]
[138]
Zalis MC, Johansson S, Johansson F, Johansson UE. Exploration of physical and chemical cues on retinal cell fate. Mol Cell Neurosci 2016; 75: 122-32.
[http://dx.doi.org/10.1016/j.mcn.2016.07.006] [PMID: 27497842]
[139]
Chen Q, Shou P, Zheng C, et al. Fate decision of mesenchymal stem cells: adipocytes or osteoblasts? Cell Death Differ 2016; 23(7): 1128-39.
[http://dx.doi.org/10.1038/cdd.2015.168] [PMID: 26868907]
[140]
Engler AJ, Rehfeldt F, Sen S, Discher DE. Microtissue elasticity: measurements by atomic force microscopy and its influence on cell differentiation. Methods Cell Biol 2007; 83: 521-45.
[http://dx.doi.org/10.1016/S0091-679X(07)83022-6] [PMID: 17613323]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy