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Original Articles

The influence of cyclic tensile strain on multi-compartment collagen-GAG scaffolds for tendon-bone junction repair

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Pages 530-543 | Received 27 Jul 2018, Accepted 08 Mar 2019, Published online: 22 Apr 2019

References

  • Moffat KL, Wang I-NE, Rodeo SA, Lu HH. Orthopedic interface tissue engineering for the biological fixation of soft tissue grafts. Clin Sports Med. 2009;28(1):157–176. doi:10.1016/j.csm.2008.08.006
  • Yang PJ, Temenoff JS. Engineering orthopedic tissue interfaces. Tissue Eng Part B Rev. 2009;15(2):127–141.
  • Shaw HM, Benjamin M. Structure–function relationships of entheses in relation to mechanical load and exercise. Scand J Med Sci Sports. 2007;17(4):303–315. doi:10.1111/j.1600-0838.2007.00689.x
  • Genin GM, Kent A, Birman V, Wopenka B, Pasteris JD, Marquez PJ, Thomopoulos S. Functional grading of mineral and collagen in the attachment of tendon to bone. Biophys J. 2009;97(4):976–985. doi:10.1016/j.bpj.2009.05.043
  • Lu HH, Thomopoulos S. Functional attachment of soft tissues to bone: development, healing, and tissue engineering. Annu Rev Biomed Eng. 2013;15(1):201–226. doi:10.1146/annurev-bioeng-071910-124656
  • Font Tellado S, Balmayor ER, Van Griensven M. Strategies to engineer tendon/ligament-to-bone interface: biomaterials, cells and growth factors. Adv Drug Deliv Rev. 2015;94:126–140. doi:10.1016/j.addr.2015.03.004
  • 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 Pt 1):617–628. doi:10.1016/S0006-3495(04)74140-5
  • Dalby MJ, Gadegaard N, Oreffo ROC. Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate. Nat Mater. 2014;13(6):558–569. doi:10.1038/nmat3980
  • Lipner J, Liu W, Liu Y, Boyle J, Genin GM, Xia Y, Thomopoulos S. The mechanics of PLGA nanofiber scaffolds with biomimetic gradients in mineral for tendon-to-bone repair. J Mech Behav Biomed Mater. 2014;40:59–68. doi:10.1016/j.jmbbm.2014.08.002
  • Font Tellado S, et al. Fabrication and characterization of biphasic silk fibroin scaffolds for tendon/ligament-to-bone tissue engineering. Tissue Eng Part A. 2017;23:15–16.
  • Spalazzi JP, Dagher E, Doty SB, Guo XE, Rodeo SA, Lu HH. In vivo evaluation of a multiphased scaffold designed for orthopaedic interface tissue engineering and soft tissue-to-bone integration. J Biomed Mater Res Part A. 2008;86A(1):1–12. doi:10.1002/(ISSN)1552-4965
  • Zhang X, Bogdanowicz D, Erisken C, Lee NM, Lu HH.. Biomimetic scaffold design for functional and integrative tendon repair. J Shoulder Elbow Surg. 2012;21(2):266–277. doi:10.1016/j.jse.2011.11.016
  • Wu Y, Fuh J, Wong YS, Sun J. A hybrid electrospinning and electrospraying 3D printing for tissue engineered scaffolds. Rapid Prototyping J. 2017;23(6):1011–1019. doi:10.1108/RPJ-08-2015-0111
  • Wu Y, Han Y, Wong YS, Fuh JYH. Fibre-based scaffolding techniques for tendon tissue engineering. J Tissue Eng Regen Med. 2018;12(7):1798–1821. doi:10.1002/term.2701
  • Yannas IV, Lee E, Orgill DP, Skrabut EM, Murphy GF. Synthesis and characterization of a model extracellular matrix that induces partial regeneration of adult mammalian skin. Proc Natl Acad Sci USA. 1989;86(3):933–937.
  • Chamberlain LJ, Yannas IV, Hsu HP, Strichartz GR, Spector M. Near-terminus axonal structure and function following rat sciatic nerve regeneration through a collagen-GAG matrix in a ten-millimeter gap. J Neurosci Res. 2000;60(5):666–677. doi:10.1002/(SICI)1097-4547(20000601)60:5<666::AID-JNR12>3.0.CO;2-0
  • Vickers SM, Gotterbarm T, Spector M. Cross-linking affects cellular condensation and chondrogenesis in type II collagen-GAG scaffolds seeded with bone marrow-derived mesenchymal stem cells. J Orthop Res. 2010;28(9):1184–1192. doi:10.1002/jor.21113
  • Caliari SR, Harley BAC. The effect of anisotropic collagen-GAG scaffolds and growth factor supplementation on tendon cell recruitment, alignment, and metabolic activity. Biomaterials. 2011;32(23):5330–5340. doi:10.1016/j.biomaterials.2011.04.021
  • Caliari SR, Weisgerber DW, Ramirez MA, Kelkhoff DO, Harley BAC. The influence of collagen–glycosaminoglycan scaffold relative density and microstructural anisotropy on tenocyte bioactivity and transcriptomic stability. J Mech Behav Biomed Mater. 2012;11:27–40. doi:10.1016/j.jmbbm.2011.12.004
  • Caliari SR, Harley BAC. Structural and biochemical modification of a collagen scaffold to selectively enhance MSC tenogenic, chondrogenic, and osteogenic differentiation. Adv Healthc Mater. 2014;3(7):1086–1096. doi:10.1002/adhm.201300646
  • Grier WK, Moy AS, Harley BA. Cyclic tensile strain enhances human mesenchymal stem cell Smad 2/3 activation and tenogenic differentiation in anisotropic collagen-glycosaminoglycan scaffolds. Eur Cell Mater. 2017;33:227–239. doi:10.22203/eCM.v033a14
  • Grier WK, Iyoha EM, Harley BAC. The influence of pore size and stiffness on tenocyte bioactivity and transcriptomic stability in collagen-GAG scaffolds. J Mech Behav Biomed Mater. 2017;65:295–305. doi:10.1016/j.jmbbm.2016.08.034
  • Harley BA, Lynn AK, Wissner-Gross Z, Bonfield W, Yannas IV, Gibson LJ. Design of a multiphase osteochondral scaffold. II. Fabrication of a mineralized collagen-glycosaminoglycan scaffold. J Biomed Mater Res A. 2010;92(3):1066–1077. doi:10.1002/jbm.a.32361
  • Weisgerber DW, Caliari SR, Harley BAC. Mineralized collagen scaffolds induce hMSC osteogenesis and matrix remodeling. Biomater Sci. 2015;3(3):533–542. doi:10.1039/C4BM00397G
  • Lee JC, Pereira CT, Ren X, Huang W, Bischoff D, Weisgerber DW, Yamaguchi DT, Harley BA, Miller TA. Optimizing collagen scaffolds for bone engineering: effects of cross-linking and mineral content on structural contraction and osteogenesis. J Craniofacial Surg. 2015;26(6):1992–1996. doi:10.1097/SCS.0000000000001918
  • Ren X, Bischoff D, Weisgerber DW, Lewis MS, Tu V, Yamaguchi DT, Miller TA, Harley BAC, Lee JC. Osteogenesis on nanoparticulate mineralized collagen scaffolds via autogenous activation of the canonical BMP receptor signaling pathway. Biomaterials. 2015;50:107–114. doi:10.1016/j.biomaterials.2015.01.059
  • Ren X, Tu V, Bischoff D, Weisgerber DW, Lewis MS, Yamaguchi DT, Miller TA, Harley BAC, Lee JC. Nanoparticulate mineralized collagen scaffolds induce in vivo bone regeneration independent of progenitor cell loading or exogenous growth factor stimulation. Biomaterials. 2016;89:67–78. doi:10.1016/j.biomaterials.2016.02.020
  • Ren X, Weisgerber DW, Bischoff D, Lewis MS, Reid RR, He T-C, Yamaguchi DT, Miller TA, Harley BAC, Lee JC. Nanoparticulate mineralized collagen scaffolds and BMP-9 induce a long-term bone cartilage construct in human mesenchymal stem cells. Adv Healthc Mater. 2016;5(14):1821–1830. doi:10.1002/adhm.201600187
  • Harley BA, Lynn AK, Wissner-Gross Z, Bonfield W, Yannas IV, Gibson LJ. Design of a multiphase osteochondral scaffold III: fabrication of layered scaffolds with continuous interfaces. J Biomed Mater Res A. 2010;92(3):1078–1093. doi:10.1002/jbm.a.32387
  • Getgood AMJ, Kew SJ, Brooks R, Aberman H, Simon T, Lynn AK, Rushton N. Evaluation of early-stage osteochondral defect repair using a biphasic scaffold based on a collagen–glycosaminoglycan biopolymer in a caprine model. Knee. 2012;19(4):422–430. doi:10.1016/j.knee.2011.03.011
  • Caliari SR, Weisgerber DW, Grier WK, Mahmassani Z, Boppart MD, Harley BAC. Collagen scaffolds incorporating coincident gradations of instructive structural and biochemical cues for osteotendinous junction engineering. Adv Healthc Mater. 2015;4(6):831–837. doi:10.1002/adhm.201400809
  • Holladay C, et al. Preferential tendon stem cell response to growth factor supplementation. J Tissue Eng Regen Med. 2014;10(9):783–798.
  • Jiang D, Gao P, Zhang Y, Yang S. Combined effects of engineered tendon matrix and GDF-6 on bone marrow mesenchymal stem cell-based tendon regeneration. Biotechnol Lett. 2016;38(5):885–892. doi:10.1007/s10529-016-2037-z
  • Lyons FG, Gleeson JP, Partap S, Coghlan K, O’Brien FJ. Novel microhydroxyapatite particles in a collagen scaffold: a bioactive bone void filler? Clin Orthop Relat Res. 2014;472(4):1318–1328. doi:10.1007/s11999-013-3438-0
  • Hettiaratchi MH, Miller T, Temenoff JS, Guldberg RE, McDevitt TC. Heparin microparticle effects on presentation and bioactivity of bone morphogenetic protein-2. Biomaterials. 2014;35(25):7228–7238. doi:10.1016/j.biomaterials.2014.05.011
  • Quinlan E, Thompson EM, Matsiko A, O’Brien FJ, López-Noriega A. Long-term controlled delivery of rhBMP-2 from collagen-hydroxyapatite scaffolds for superior bone tissue regeneration. J Controlled Release: off J Controlled Release Soc. 2015;207:112–119. doi:10.1016/j.jconrel.2015.03.028
  • Lyons FG, Gleeson JP, Partap S, Coghlan K, O’Brien FJ. Novel microhydroxyapatite particles in a collagen scaffold: a bioactive bone void filler? Clin Orthop Relat Res. 2014;472(4):1318–1328. doi:10.1007/s11999-013-3438-0
  • Chen X, et al. Force and scleraxis synergistically promote the commitment of human ES cells derived MSCs to tenocytes. Sci Rep. 2012;2:977.
  • Schweitzer R, Zelzer E, Volk T. Connecting muscles to tendons: tendons and musculoskeletal development in flies and vertebrates. Development. 2010;137(17):2807–2817. doi:10.1242/dev.047498
  • Galloway MT, Lalley AL, Shearn JT. The role of mechanical loading in tendon development, maintenance, injury, and repair. J Bone Joint Surg Am. 2013;95(17):1620–1628. doi:10.2106/JBJS.L.01004
  • Thomopoulos S, Zampiakis E, Das R, Silva MJ, Gelberman RH. The effect of muscle loading on flexor tendon-to-bone healing in a canine model. J Orthop Res. 2008;26(12):1611–1617. doi:10.1002/jor.20689
  • Paxton JZ, Hagerty P, Andrick JJ, Baar K. Optimizing an intermittent stretch paradigm using ERK1/2 phosphorylation results in increased collagen synthesis in engineered ligaments. Tissue Eng Part A. 2012;18(3–4):277–284. doi:10.1089/ten.TEA.2011.0336
  • Doroski DM, Levenston ME, Temenoff JS. Cyclic tensile culture promotes fibroblastic differentiation of marrow stromal cells encapsulated in poly(ethylene glycol)-based hydrogels. Tissue Eng Part A. 2010;16(11):3457–3466. doi:10.1089/ten.tea.2010.0233
  • Bosworth LA, Rathbone SR, Bradley RS, Cartmell SH. Dynamic loading of electrospun yarns guides mesenchymal stem cells towards a tendon lineage. J Mech Behav Biomed Mater. 2014;39:175–183. doi:10.1016/j.jmbbm.2014.07.009
  • Govoni M, Muscari C, Lovecchio J, Guarnieri C, Giordano E. Mechanical actuation systems for the phenotype commitment of stem cell-based tendon and ligament tissue substitutes. Stem Cell Rev Rep. 2016;12(2):189–201. doi:10.1007/s12015-015-9640-6
  • Laboureau J, Dubertret L, Lebreton-De Coster C, Coulomb B. ERK activation by mechanical strain is regulated by the small G proteins rac-1 and rhoA. Exp Dermatol. 2004;13(2):70–77. doi:10.1111/j.0906-6705.2004.00117.x
  • Papakrivopoulou J, Lindahl GE, Bishop JE, Laurent GJ. Differential roles of extracellular signal-regulated kinase 1/2 and p38MAPK in mechanical load-induced procollagen α1(I) gene expression in cardiac fibroblasts. Cardiovasc Res. 2004;61:736–744. doi:10.1016/j.cardiores.2003.12.018
  • Weinbaum J, Schmidt J, Tranquillo R. Combating adaptation to cyclic stretching by prolonging activation of extracellular signal-regulated kinase. Cell Mol Bioeng. 2013;6(3):279–286. doi:10.1007/s12195-013-0289-4
  • Caliari SR, Weisgerber DW, Grier WK, Mahmassani Z, Boppart MD, Harley BAC. Collagen scaffolds incorporating coincident gradations of instructive structural and biochemical cues for osteotendinous junction engineering. Adv Healthc Mater. 2015;4(6):831–837. doi:10.1002/adhm.201400809
  • Madaghiele M, Sannino A, Yannas IV, Spector M. Collagen-based matrices with axially oriented pores. J Biomed Mater Res Part A. 2008;85A(3):757–767. doi:10.1002/(ISSN)1552-4965
  • Lynn AK, Best SM, Cameron RE, Harley BA, Yannas IV, Gibson LJ, Bonfield W. Design of a multiphase osteochondral scaffold. I. Control of chemical composition. J Biomed Mater Res A. 2010;92(3):1057–1065. doi:10.1002/jbm.a.32415
  • O‘Brien FJ, Harley BA, Yannas IV, Gibson L. Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds. Biomaterials. 2004;25(6):1077–1086.
  • Olde Damink LHH, Dijkstra PJ, van Luyn MJ, van Wachem PB, Nieuwenhuis P, Feijen J. Cross-linking of dermal sheep collagen using a water soluble carbodiimide. Biomaterials. 1996;17:765–773.
  • Harley BA, Leung JH, Silva ECCM, Gibson LJ. Mechanical characterization of collagen-glycosaminoglycan scaffolds. Acta Biomater. 2007;3(4):463–474. doi:10.1016/j.actbio.2006.12.009
  • Grier WK, et al. Incorporation of β-cyclodextrin into collagen-GAG scaffolds for the selective sequestration and presentation of growth factors to guide MSC fate. Acta Biomater. 2018 ( in revision). doi:10.1016/j.actbio.2018.06.033
  • Weisgerber DW, Kelkhoff DO, Caliari SR, Harley BAC. The impact of discrete compartments of a multi-compartment collagen-GAG scaffold on overall construct biophysical properties. J Mech Behav Biomed Mater. 2013;28:26–36. doi:10.1016/j.jmbbm.2013.07.016
  • O‘Brien FJ, Harley BA, Yannas IV, Gibson LJ. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials. 2005;26(4):433–441. doi:10.1016/j.biomaterials.2004.02.052
  • Tierney EG, Duffy GP, Cryan S-A, Curtin CM, O’Brien FJ. Non-viral gene-activated matrices-next generation constructs for bone repair. Organogenesis. 2013;9(1). doi:10.4161/org.24329
  • Duffy GP, McFadden TM, Byrne EM, Gill S-L, Farrell E, O’Brien FJ. Towards in vitro vascularisation of collagen-GAG scaffolds. Eur Cell Mater. 2011;21:15–30. doi:10.22203/eCM
  • Hayashida T, Wu M-H, Pierce A, Poncelet A-C, Varga J, Schnaper HW. MAP-kinase activity necessary for TGFβ1-stimulated mesangial cell type I collagen expression requires adhesion-dependent phosphorylation of FAK tyrosine 397. J Cell Sci. 2007;120(23):4230–4240. doi:10.1242/jcs.03492
  • Papakrivopoulou J, Lindahl GE, Bishop JE, Laurent GJ. Differential roles of extracellular signal-regulated kinase 1/2 and p38MAPK in mechanical load-induced procollagen α1(I) gene expression in cardiac fibroblasts. Cardiovasc Res. 2004;61(4):736–744. doi:10.1016/j.cardiores.2003.12.018
  • Kelly-Arnold A, Maldonado N, Laudier D, Aikawa E, Cardoso L, Weinbaum S. Revised microcalcification hypothesis for fibrous cap rupture in human coronary arteries. Proc National Acad Sci. 2013;110(26):10741–10746. doi:10.1073/pnas.1308814110
  • Shen H, Gelberman RH, Silva MJ, Sakiyama-Elbert SE, Thomopoulos S, Awad H. BMP12 induces tenogenic differentiation of adipose-derived stromal cells. PLoS One. 2013;8(10):e77613. doi:10.1371/journal.pone.0077613
  • Maeda T, Sakabe T, Sunaga A, Sakai K, Rivera AL, Keene DR, Sasaki T, Stavnezer E, Iannotti J, Schweitzer R, Ilic D, Baskaran H, Sakai T. Conversion of mechanical force into TGF-β-mediated biochemical signals. Curr Biol. 2011;21(11):933–941. doi:10.1016/j.cub.2011.04.007
  • Klatte-Schulz F, Pauly S, Scheibel M, Greiner S, Gerhardt C, Hartwig J, Schmidmaier G, Wildemann B, Laird EG. Characteristics and stimulation potential with BMP-2 and BMP-7 of tenocyte-like cells isolated from the rotator cuff of female donors. PLoS One. 2013;8(6):e67209. doi:10.1371/journal.pone.0067209
  • Pauly S, Klatte F, Strobel C, Schmidmaier G, Greiner S, Scheibel M, Wildemann B. Characterization of tendon cell cultures of the human rotator cuff. Eur Cell Mater. 2010;20:84–97. doi:10.22203/eCM
  • Lorda-Diez CI, Canga-Villegas A, Cerezal L, Plaza S, Hurlé JM, García-Porrero JA, Montero JA. Comparative transcriptional analysis of three human ligaments with distinct biomechanical properties. J Anat. 2013;223(6):593–602. doi:10.1111/joa.12124
  • Zhou J, Xu C, Wu G, Cao X, Zhang L, Zhai Z, Zheng Z, Chen X, Wang Y. In vitro generation of osteochondral differentiation of human marrow mesenchymal stem cells in novel collagen–hydroxyapatite layered scaffolds. Acta Biomater. 2011;7(11):3999–4006. doi:10.1016/j.actbio.2011.06.040
  • Frank O, Heim M, Jakob M, Barbero A, Schäfer D, Bendik I, Dick W, Heberer M, Martin I. Real-time quantitative RT-PCR analysis of human bone marrow stromal cells during osteogenic differentiation in vitro. J Cell Biochem. 2002;85(4):737–746. doi:10.1002/jcb.10174
  • Murchison ND, Price BA, Conner DA, Keene DR, Olson EN, Tabin CJ, Schweitzer R. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development. 2007;134(14):2697–2708. doi:10.1242/dev.001933
  • Pryce BA, Watson SS, Murchison ND, Staverosky JA, Dünker N, Schweitzer R. Recruitment and maintenance of tendon progenitors by TGFbeta signaling are essential for tendon formation. Development. 2009;136(8):1351–1361. doi:10.1242/dev.027342
  • Blitz E, Viukov S, Sharir A, Shwartz Y, Galloway JL, Pryce BA, Johnson RL, Tabin CJ, Schweitzer R, Zelzer E. Bone ridge patterning during musculoskeletal assembly is mediated through SCX regulation of Bmp4 at the tendon-skeleton junction. Dev Cell. 2009;17(6):861–873. doi:10.1016/j.devcel.2009.10.010
  • Weisgerber DW, Kelkhoff DO, Caliari SR, Harley BAC. The impact of discrete compartments of a multi-compartment collagen–GAG scaffold on overall construct biophysical properties. J Mech Behav Biomed Mater. 2013;28:26–36. doi:10.1016/j.jmbbm.2013.07.016
  • Jiang Y, Wang Y, Tang G. Cyclic tensile strain promotes the osteogenic differentiation of a bone marrow stromal cell and vascular endothelial cell co-culture system. Arch Biochem Biophys. 2016;607:37–43. doi:10.1016/j.abb.2016.08.015
  • Yourek G, McCormick SM, Mao JJ, Reilly GC. Shear stress induces osteogenic differentiation of human mesenchymal stem cells. Regen Med. 2010;5(5):713–724. doi:10.2217/rme.10.60
  • Liu H, et al. Mohawk promotes the tenogenesis of mesenchymal stem cells through activation of the TGFβ signaling pathway. Stem Cells. 2014;33(2):443–455.
  • Zhou Q, Ren X, Bischoff D, Weisgerber DW, Yamaguchi DT, Miller TA, Harley BAC, Lee JC. Nonmineralized and mineralized collagen scaffolds induce differential osteogenic signaling pathways in human mesenchymal stem cells. Adv Healthc Mater. 2017;6(23):1700641. doi:10.1002/adhm.v6.23
  • He P, Ng KS, Toh SL, Goh JCH. In vitro ligament–bone interface regeneration using a trilineage coculture system on a hybrid silk scaffold. Biomacromolecules. 2012;13(9):2692–2703. doi:10.1021/bm300651q
  • Liu H, et al. Biomimetic tendon extracellular matrix composite gradient scaffold enhances ligament-to-bone junction reconstruction. Acta Biomater. 2017;56:129–140.
  • Allen JL, Cooke ME, Alliston T. ECM stiffness primes the TGF pathway to promote chondrocyte differentiation. Mol Biol Cell. 2012;23(18):3731–3742. doi:10.1091/mbc.E12-03-0172
  • Grier WK, et al. The influence of cyclic tensile strain on multi-compartment collagen-GAG scaffolds for tendon-bone junction regeneration. bioRxiv. 2018.
  • Ren X, Weisgerber DW, Bischoff D, Lewis MS, Reid RR, He T-C, Yamaguchi DT, Miller TA, Harley BAC, Lee JC. Nanoparticulate mineralized collagen scaffolds and BMP-9 induce a long term bone cartilage construct in human mesenchymal stem cells. Adv Healthc Mater. 2016;5(14):1821–1830. doi:10.1002/adhm.201600187

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