1932

Abstract

The connective tissues of the musculoskeletal system can be grouped into fibrous, cartilaginous, and calcified tissues. While each tissue type has a distinct composition and function, the intersections between these tissues result in the formation of complex, composite, and graded junctions. The complexity of these interfaces is a critical aspect of their healthy function, but poses a significant challenge for their repair. In this review, we describe the organization and structure of complex musculoskeletal interfaces, identify emerging technologies for engineering such structures, and outline the requirements for assessing the complex nature of these tissues in the context of recapitulating their function through tissue engineering.

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2018-06-04
2024-03-29
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Literature Cited

  1. 1.  Delale F 1984. Stress singularities in bonded anisotropic materials. Int. J. Solids Struct. 20:31–40
    [Google Scholar]
  2. 2.  Jeffery AK, Blunn GW, Archer CW, Bentley G 1991. Three-dimensional collagen architecture in bovine articular cartilage. J. Bone Joint Surg. Br. 73:795–801
    [Google Scholar]
  3. 3.  Klein TJ, Chaudhry M, Bae WC, Sah RL 2007. Depth-dependent biomechanical and biochemical properties of fetal, newborn, and tissue-engineered articular cartilage. J. Biomech. 40:182–90
    [Google Scholar]
  4. 4.  Buckley MR, Gleghorn JP, Bonassar LJ, Cohen I 2008. Mapping the depth dependence of shear properties in articular cartilage. J. Biomech. 41:2430–37
    [Google Scholar]
  5. 5.  Ferguson VL, Bushby AJ, Boyde A 2003. Nanomechanical properties and mineral concentration in articular calcified cartilage and subchondral bone. J. Anat. 203:191–202
    [Google Scholar]
  6. 6.  Liu Y, Birman V, Chen C, Thomopoulos S, Genin GM 2011. Mechanisms of bimaterial attachment at the interface of tendon to bone. J. Eng. Mater. Technol. 133:011006
    [Google Scholar]
  7. 7.  Thomopoulos S, Birman V, Genin GM 2013. The challenge of attaching dissimilar materials. Structural Interfaces and Attachments in Biology3–17 New York: Springer
    [Google Scholar]
  8. 8.  Deymier AC, An Y, Boyle JJ, Schwartz AG, Birman V et al. 2017. Micro-mechanical properties of the tendon-to-bone attachment. Acta Biomater 56:25–35
    [Google Scholar]
  9. 9.  Ruggiero L, Zimmerman BK, Park M, Han L, Wang L et al. 2015. Roles of the fibrous superficial zone in the mechanical behavior of TMJ condylar cartilage. Ann. Biomed. Eng. 43:2652–62
    [Google Scholar]
  10. 10.  Singh M, Detamore MS 2008. Tensile properties of the mandibular condylar cartilage. J. Biomech. Eng. 130:011009
    [Google Scholar]
  11. 11.  Nerurkar NL, Elliott DM, Mauck RL 2010. Mechanical design criteria for intervertebral disc tissue engineering. J. Biomech. 43:1017–30
    [Google Scholar]
  12. 12.  Cross M, Smith E, Hoy D, Nolte S, Ackerman I et al. 2014. The global burden of hip and knee osteoarthritis: estimates from the Global Burden of Disease 2010 study. Ann. Rheum. Dis. 73:1323–30
    [Google Scholar]
  13. 13.  Buchbinder R, Blyth FM, March LM, Brooks P, Woolf AD, Hoy DG 2013. Placing the global burden of low back pain in context. Best Pract. Res. Clin. Rheumatol. 27:575–89
    [Google Scholar]
  14. 14.  Tanaka E, Detamore MS, Mercuri LG 2008. Degenerative disorders of the temporomandibular joint: etiology, diagnosis, and treatment. J. Dent. Res. 87:296–307
    [Google Scholar]
  15. 15.  Sharma P 2005. Tendon injury and tendinopathy: healing and repair. J. Bone Jt. Surg. 87:187–202
    [Google Scholar]
  16. 16.  Buxboim A, Rajagopal K, Brown A, Discher DE 2010. How deeply cells feel: methods for thin gels. J. Phys. Condens. Matter 22:194116
    [Google Scholar]
  17. 17.  Huang C-Y, Soltz MA, Kopacz M, Mow VC, Ateshian GA 2003. Experimental verification of the roles of intrinsic matrix viscoelasticity and tension–compression nonlinearity in the biphasic response of cartilage. J. Biomech. Eng. 125:84–93
    [Google Scholar]
  18. 18.  Soltz MA, Ateshian GA 2000. A conewise linear elasticity mixture model for the analysis of tension-compression nonlinearity in articular cartilage. J. Biomech. Eng. 122:576–86
    [Google Scholar]
  19. 19.  Lai WM, Hou JS, Mow VC 1991. A triphasic theory for the swelling and deformation behaviors of articular cartilage. J. Biomech. Eng. 113:245–58
    [Google Scholar]
  20. 20.  Maroudas A, Muir H, Wingham J 1969. The correlation of fixed negative charge with glycosaminoglycan content of human articular cartilage. Biochim. Biophys. Acta 177:492–500
    [Google Scholar]
  21. 21.  Minns RJ, Steven FS 1977. The collagen fibril organization in human articular cartilage. J. Anat. 123:Part 2437–57
    [Google Scholar]
  22. 22.  Jay GD 2009. Characterization of a bovine synovial fluid lubricating factor. I. Chemical, surface activity and lubricating properties. Connect. Tissue Res. 28:71–88
    [Google Scholar]
  23. 23.  Jones ARC, Gleghorn JP, Hughes CE, Fitz LJ, Zollner R et al. 2007. Binding and localization of recombinant lubricin to articular cartilage surfaces. J. Orthop. Res. 25:283–92
    [Google Scholar]
  24. 24.  Bonnevie ED, Galesso D, Secchieri C, Cohen I, Bonassar LJ 2015. Elastoviscous transitions of articular cartilage reveal a mechanism of synergy between lubricin and hyaluronic acid. PLOS ONE 10:e0143415
    [Google Scholar]
  25. 25.  Schinagl RM, Gurskis D, Chen AC, Sah RL 1997. Depth-dependent confined compression modulus of full-thickness bovine articular cartilage. J. Orthop. Res. 15:499–506
    [Google Scholar]
  26. 26.  Buckley MR, Bergou AJ, Fouchard J, Bonassar LJ, Cohen I 2010. High-resolution spatial mapping of shear properties in cartilage. J. Biomech. 43:796–800
    [Google Scholar]
  27. 27.  Charlebois M, McKee MD, Buschmann MD 2004. Nonlinear tensile properties of bovine articular cartilage and their variation with age and depth. J. Biomech. Eng. 126:129–37
    [Google Scholar]
  28. 28.  Buckley MR, Bonassar LJ, Cohen I 2013. Localization of viscous behavior and shear energy dissipation in articular cartilage under dynamic shear loading. J. Biomech. Eng. 135:031002
    [Google Scholar]
  29. 29.  Bartell LR, Fortier LA, Bonassar LJ, Cohen I 2015. Measuring microscale strain fields in articular cartilage during rapid impact reveals thresholds for chondrocyte death and a protective role for the superficial layer. J. Biomech. 48:3440–46
    [Google Scholar]
  30. 30.  Pearle AD, Warren RF, Rodeo SA 2005. Basic science of articular cartilage and osteoarthritis. Clin. Sports Med. 24:1–12
    [Google Scholar]
  31. 31.  Bi X, Yang X, Bostrom MPG, Bartusik D, Ramaswamy S et al. 2007. Fourier transform infrared imaging and MR microscopy studies detect compositional and structural changes in cartilage in a rabbit model of osteoarthritis. Anal. Bioanal. Chem. 387:1601–12
    [Google Scholar]
  32. 32.  Boskey A, Pleshko Camacho N 2007. FT-IR imaging of native and tissue-engineered bone and cartilage. Biomaterials 28:2465–78
    [Google Scholar]
  33. 33.  Bae WC, Temple MM, Amiel D, Coutts RD, Niederauer GG, Sah RL 2003. Indentation testing of human cartilage: sensitivity to articular surface degeneration. Arthritis Rheum 48:3382–94
    [Google Scholar]
  34. 34.  Oettmeier R, Abendroth K 1989. Osteoarthritis and bone: osteologic types of osteoarthritis of the hip. Skelet. Radiol. 18:165–74
    [Google Scholar]
  35. 35.  Vacanti JP, Langer R 1999. Tissue engineering: the design and fabrication of living replacement devices for surgical reconstruction and transplantation. Lancet 354:S32–34
    [Google Scholar]
  36. 36.  Dimicco MA, Sah RL 2001. Integrative cartilage repair: Adhesive strength is correlated with collagen deposition. J. Orthop. Res. 19:1105–12
    [Google Scholar]
  37. 37.  Klein TJ, Schumacher BL, Schmidt TA, Li KW, Voegtline MS et al. 2003. Tissue engineering of stratified articular cartilage from chondrocyte subpopulations. Osteoarthr. Cartil. 11:595–602
    [Google Scholar]
  38. 38.  Kim M, Farrell MJ, Steinberg DR, Burdick JA, Mauck RL 2017. Enhanced nutrient transport improves the depth-dependent properties of tri-layered engineered cartilage constructs with zonal co-culture of chondrocytes and MSCs. Acta Biomater 58:1–11
    [Google Scholar]
  39. 39.  Kim T-K, Sharma B, Williams C, Ruffner M, Malik A et al. 2003. Experimental model for cartilage tissue engineering to regenerate the zonal organization of articular cartilage. Osteoarthr. Cartil. 11:653–64
    [Google Scholar]
  40. 40.  Sharma B, Williams CG, Kim TK, Sun D, Malik A et al. 2007. Designing zonal organization into tissue-engineered cartilage. Tissue Eng 13:405–14
    [Google Scholar]
  41. 41.  Ng KW, Ateshian GA, Hung CT 2009. Zonal chondrocytes seeded in a layered agarose hydrogel create engineered cartilage with depth-dependent cellular and mechanical inhomogeneity. Tissue Eng. A 15:2315–24
    [Google Scholar]
  42. 42.  Benya PD, Padilla SR, Nimni ME 1978. Independent regulation of collagen types by chondrocytes during the loss of differentiated function in culture. Cell 15:1313–21
    [Google Scholar]
  43. 43.  Darling EM, Athanasiou KA 2005. Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J. Orthop. Res. 23:425–32
    [Google Scholar]
  44. 44.  Li W-J, Tuli R, Okafor C, Derfoul A, Danielson KG et al. 2005. A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials 26:599–609
    [Google Scholar]
  45. 45.  Caplan AI 2007. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell. Physiol. 213:341–47
    [Google Scholar]
  46. 46.  Alhadlaq A, Elisseeff JH, Hong L, Williams CG, Caplan AI et al. 2004. Adult stem cell driven genesis of human-shaped articular condyle. Ann. Biomed. Eng. 32:911–23
    [Google Scholar]
  47. 47.  Vinardell T, Sheehy EJ, Buckley CT, Kelly DJ 2012. A comparison of the functionality and in vivo phenotypic stability of cartilaginous tissues engineered from different stem cell sources. Tissue Eng. A 18:1161–70
    [Google Scholar]
  48. 48.  Pelttari K, Winter A, Steck E, Goetzke K, Hennig T et al. 2006. Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum 54:3254–66
    [Google Scholar]
  49. 49.  Chawla K, Klein TJ, Schumacher BL, Jadin KD, Shah BH et al. 2007. Short-term retention of labeled chondrocyte subpopulations in stratified tissue-engineered cartilaginous constructs implanted in vivo in mini-pigs. Tissue Eng 13:1525–37
    [Google Scholar]
  50. 50.  Schaefer D, Martin I, Shastri P, Padera R, Langer R et al. 2000. In vitro generation of osteochondral composites. Biomaterials 21:2599–606
    [Google Scholar]
  51. 51.  Steinmetz NJ, Aisenbrey EA, Westbrook KK, Qi HJ, Bryant SJ 2015. Mechanical loading regulates human MSC differentiation in a multi-layer hydrogel for osteochondral tissue engineering. Acta Biomater 21:142–53
    [Google Scholar]
  52. 52.  Sherwood JK, Riley SL, Palazzolo R, Brown SC, Monkhouse DC et al. 2002. A three-dimensional osteochondral composite scaffold for articular cartilage repair. Biomaterials 23:4739–51
    [Google Scholar]
  53. 53.  Ahn J-H, Lee T-H, Oh J-S, Kim S-Y, Kim H-J et al. 2009. A novel hyaluronate-atelocollagen/β-TCP-hydroxyapatite biphasic scaffold for the repair of osteochondral defects in rabbits. Tissue Eng. A 15:2595–604
    [Google Scholar]
  54. 54.  Guo X, Park H, Young S, Kretlow JD, van den Beucken JJ et al. 2010. Repair of osteochondral defects with biodegradable hydrogel composites encapsulating marrow mesenchymal stem cells in a rabbit model. Acta Biomater 6:39–47
    [Google Scholar]
  55. 55.  Cao Z, Hou S, Sun D, Wang X, Tang J 2012. Osteochondral regeneration by a bilayered construct in a cell-free or cell-based approach. Biotechnol. Lett. 34:1151–57
    [Google Scholar]
  56. 56.  Chen J, Chen H, Li P, Diao H, Zhu S et al. 2011. Simultaneous regeneration of articular cartilage and subchondral bone in vivo using MSCs induced by a spatially controlled gene delivery system in bilayered integrated scaffolds. Biomaterials 32:4793–805
    [Google Scholar]
  57. 57.  Cui W, Wang Q, Chen G, Zhou S, Chang Q et al. 2011. Repair of articular cartilage defects with tissue-engineered osteochondral composites in pigs. J. Biosci. Bioeng. 111:493–500
    [Google Scholar]
  58. 58.  Griffin DJ, Bonnevie ED, Lachowsky DJ, Hart JCA, Sparks HD et al. 2015. Mechanical characterization of matrix-induced autologous chondrocyte implantation (MACI®) grafts in an equine model at 53 weeks. J. Biomech. 48:1944–49
    [Google Scholar]
  59. 59.  Wang X, Wenk E, Zhang X, Meinel L, Vunjak-Novakovic G, Kaplan DL 2009. Growth factor gradients via microsphere delivery in biopolymer scaffolds for osteochondral tissue engineering. J. Control. Release 134:81–90
    [Google Scholar]
  60. 60.  Mohan N, Dormer NH, Caldwell KL, Key VH, Berkland CJ, Detamore MS 2011. Continuous gradients of material composition and growth factors for effective regeneration of the osteochondral interface. Tissue Eng. A 17:2845–55
    [Google Scholar]
  61. 61.  Grayson WL, Bhumiratana S, Chao PHG, Hung CT, Vunjak-Novakovic G 2010. Spatial regulation of human mesenchymal stem cell differentiation in engineered osteochondral constructs: effects of pre-differentiation, soluble factors and medium perfusion. Osteoarthr. Cartil. 18:714–23
    [Google Scholar]
  62. 62.  Lu S, Lam J, Trachtenberg JE, Lee EJ, Seyednejad H et al. 2014. Dual growth factor delivery from bilayered, biodegradable hydrogel composites for spatially-guided osteochondral tissue repair. Biomaterials 35:8829–39
    [Google Scholar]
  63. 63.  Alexander PG, Gottardi R, Lin H, Lozito TP, Tuan RS 2014. Three-dimensional osteogenic and chondrogenic systems to model osteochondral physiology and degenerative joint diseases. Exp. Biol. Med. 239:1080–95
    [Google Scholar]
  64. 64.  Chen SS, Falcovitz YH, Schneiderman R, Maroudas A, Sah RL 2001. Depth-dependent compressive properties of normal aged human femoral head articular cartilage: relationship to fixed charge density. Osteoarthr. Cartil. 9:561–69
    [Google Scholar]
  65. 65.  Kelly T-AN, Ng KW, Wang CC-B, Ateshian GA, Hung CT 2006. Spatial and temporal development of chondrocyte-seeded agarose constructs in free-swelling and dynamically loaded cultures. J. Biomech. 39:1489–97
    [Google Scholar]
  66. 66.  Farrell MJ, Comeau ES, Mauck RL 2012. Mesenchymal stem cells produce functional cartilage matrix in three-dimensional culture in regions of optimal nutrient supply. Eur. Cell. Mater. 23:425–40
    [Google Scholar]
  67. 67.  Campbell SE, Ferguson VL, Hurley DC 2012. Nanomechanical mapping of the osteochondral interface with contact resonance force microscopy and nanoindentation. Acta Biomater 8:4389–96
    [Google Scholar]
  68. 68.  Stolz M, Gottardi R, Raiteri R, Miot S, Martin I et al. 2009. Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy. Nat. Nanotechnol. 4:186–92
    [Google Scholar]
  69. 69.  Kim M, Bi X, Horton WE, Spencer RG, Pleshko Camacho N 2005. Fourier transform infrared imaging spectroscopic analysis of tissue engineered cartilage: histologic and biochemical correlations. J. Biomed. Opt. 10:031105
    [Google Scholar]
  70. 70.  Pleshko Camacho N, West P, Torzilli PA, Mendelsohn R 2001. FTIR microscopic imaging of collagen and proteoglycan in bovine cartilage. Biopolymers 62:1–8
    [Google Scholar]
  71. 71.  Bonifacio A, Beleites C, Vittur F, Marsich E, Semeraro S et al. 2010. Chemical imaging of articular cartilage sections with Raman mapping, employing uni- and multi-variate methods for data analysis. Analyst 135:3193–204
    [Google Scholar]
  72. 72.  Bergholt MS, St-Pierre J-P, Offeddu GS, Parmar PA, Albro MB et al. Raman spectroscopy reveals new insights into the zonal organization of native and tissue-engineered articular cartilage. ACS Cent. Sci. 2:885–95
    [Google Scholar]
  73. 73.  Griffin DJ, Ortved KF, Nixon AJ, Bonassar LJ 2016. Mechanical properties and structure–function relationships in articular cartilage repaired using IGF-I gene–enhanced chondrocytes. J. Orthop. Res. 34:149–53
    [Google Scholar]
  74. 74.  Thomopoulos S, Marquez JP, Weinberger B, Birman V, Genin GM 2006. Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations. J. Biomech. 39:1842–51
    [Google Scholar]
  75. 75.  Genin GM, Kent A, Birman V, Wopenka B, Pasteris JD et al. 2009. Functional grading of mineral and collagen in the attachment of tendon to bone. Biophys. J. 97:976–85
    [Google Scholar]
  76. 76.  Rossetti L, Kuntz LA, Kunold E, Schock J, Müller KW et al. 2017. The microstructure and micromechanics of the tendon–bone insertion. Nat. Mater. 16:664–70
    [Google Scholar]
  77. 77.  Spalazzi JP, Boskey AL, Pleshko N, Lu HH, Kepler C 2013. Quantitative mapping of matrix content and distribution across the ligament-to-bone insertion. PLOS ONE 8:e74349
    [Google Scholar]
  78. 78.  Hyman J, Rodeo SA 2000. Injury and repair of tendons and ligaments. Phys. Med. Rehabil. Clin. N. Am. 11:267–88
    [Google Scholar]
  79. 79.  Woo SL-Y, Debski RE, Zeminski J, Abramowitch SD, Saw SS, Fenwick JA 2000. Injury and repair of ligaments and tendons. Annu. Rev. Biomed. Eng. 2:83–118
    [Google Scholar]
  80. 80.  Lin TW, Cardenas L, Soslowsky LJ 2004. Biomechanics of tendon injury and repair. J. Biomech. 37:865–77
    [Google Scholar]
  81. 81.  Gomez M 1995. The physiology and biochemistry of soft tissue healing. Rehabilitation of the Injured Knee L Griffin 34–44 St. Louis, MO: Mosby
    [Google Scholar]
  82. 82.  Rodeo SA, Arnoczky SP, Torzilli PA, Hidaka C, Warren RF 1993. Tendon-healing in a bone tunnel. A biomechanical and histological study in the dog. J. Bone Jt. Surg. Am. 75:1795–803
    [Google Scholar]
  83. 83.  Dyment NA, Breidenbach AP, Schwartz AG, Russell RP, Aschbacher-Smith L et al. 2015. Gdf5 progenitors give rise to fibrocartilage cells that mineralize via hedgehog signaling to form the zonal enthesis. Dev. Biol. 405:96–107
    [Google Scholar]
  84. 84.  Schwartz AG, Long F, Thomopoulos S 2014. Enthesis fibrocartilage cells originate from a population of Hedgehog-responsive cells modulated by the loading environment. Development 142:196–206
    [Google Scholar]
  85. 85.  Killian ML, Thomopoulos S 2016. Scleraxis is required for the development of a functional tendon enthesis. FASEB J 30:301–11
    [Google Scholar]
  86. 86.  Smith L, Xia Y, Galatz LM, Genin GM, Thomopoulos S 2012. Tissue-engineering strategies for the tendon/ligament-to-bone insertion. Connect. Tissue Res. 53:95–105
    [Google Scholar]
  87. 87.  Lu HH, Thomopoulos S 2013. Functional attachment of soft tissues to bone: development, healing, and tissue engineering. Annu. Rev. Biomed. Eng. 15:201–26
    [Google Scholar]
  88. 88.  Kryger GS, Chong AKS, Costa M, Pham H, Bates SJ, Chang J 2007. A comparison of tenocytes and mesenchymal stem cells for use in flexor tendon tissue engineering. J. Hand Surg. Am. 32:597–605
    [Google Scholar]
  89. 89.  Chen X, Yin Z, Chen J, Liu H, Shen W et al. 2014. Scleraxis-overexpressed human embryonic stem cell–derived mesenchymal stem cells for tendon tissue engineering with knitted silk-collagen scaffold. Tissue Eng. A 20:1583–92
    [Google Scholar]
  90. 90.  Pham QP, Sharma U, Mikos AG 2006. Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng 12:1197–211
    [Google Scholar]
  91. 91.  Li W-J, Mauck RL, Cooper JA, Yuan X, Tuan RS 2007. Engineering controllable anisotropy in electrospun biodegradable nanofibrous scaffolds for musculoskeletal tissue engineering. J. Biomech. 40:1686–93
    [Google Scholar]
  92. 92.  Shin HJ, Lee CH, Cho IH, Kim Y-J, Lee Y-J et al. 2006. Electrospun PLGA nanofiber scaffolds for articular cartilage reconstruction: mechanical stability, degradation and cellular responses under mechanical stimulation in vitro. J. Biomater. Sci. Polym. Ed. 17:103–19
    [Google Scholar]
  93. 93.  Li W-J, Cooper JA, Mauck RL, Tuan RS 2006. Fabrication and characterization of six electrospun poly(α-hydroxy ester)-based fibrous scaffolds for tissue engineering applications. Acta Biomater 2:377–85
    [Google Scholar]
  94. 94.  Zhang X, Reagan MR, Kaplan DL 2009. Electrospun silk biomaterial scaffolds for regenerative medicine. Adv. Drug Deliv. Rev. 61:988–1006
    [Google Scholar]
  95. 95.  Huang Z-M, Zhang Y, Ramakrishna S, Lim C 2004. Electrospinning and mechanical characterization of gelatin nanofibers. Polymer 45:5361–68
    [Google Scholar]
  96. 96.  Kim IL, Mauck RL, Burdick JA 2011. Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid. Biomaterials 32:8771–82
    [Google Scholar]
  97. 97.  Matthews JA, Wnek GE, Simpson DG, Bowlin GL 2002. Electrospinning of collagen nanofibers. Biomacromolecules 3:232–38
    [Google Scholar]
  98. 98.  Choi JS, Lee SJ, Christ GJ, Atala A, Yoo JJ 2008. The influence of electrospun aligned poly(ε-caprolactone)/collagen nanofiber meshes on the formation of self-aligned skeletal muscle myotubes. Biomaterials 29:2899–906
    [Google Scholar]
  99. 99.  Awad HA, Butler DL, Harris MT, Ibrahim RE, Wu Y et al. 2000. In vitro characterization of mesenchymal stem cell–seeded collagen scaffolds for tendon repair: effects of initial seeding density on contraction kinetics. J. Biomed. Mater. Res. 51:233–40
    [Google Scholar]
  100. 100.  Barocas VH, Tranquillo RT 1997. An anisotropic biphasic theory of tissue-equivalent mechanics: the interplay among cell traction, fibrillar network deformation, fibril alignment, and cell contact guidance. J. Biomech. Eng. 119:137–45
    [Google Scholar]
  101. 101.  Puetzer JL, Koo E, Bonassar LJ 2015. Induction of fiber alignment and mechanical anisotropy in tissue engineered menisci with mechanical anchoring. J. Biomech. 48:1436–43
    [Google Scholar]
  102. 102.  Sander EA, Stylianopoulos T, Tranquillo RT, Barocas VH 2009. Image-based multiscale modeling predicts tissue-level and network-level fiber reorganization in stretched cell-compacted collagen gels. PNAS 106:17675–80
    [Google Scholar]
  103. 103.  Li X, Xie J, Lipner J, Yuan X, Thomopoulos S, Xia Y 2009. Nanofiber scaffolds with gradations in mineral content for mimicking the tendon-to-bone insertion site. Nano Lett 9:2763–68
    [Google Scholar]
  104. 104.  Erisken C, Kalyon DM, Wang H 2008. Functionally graded electrospun polycaprolactone and β-tricalcium phosphate nanocomposites for tissue engineering applications. Biomaterials 29:4065–73
    [Google Scholar]
  105. 105.  Phillips JE, Burns KL, Le Doux JM, Guldberg RE, Garcia AJ 2008. Engineering graded tissue interfaces. PNAS 105:12170–75
    [Google Scholar]
  106. 106.  Smith LJ, Deymier AC, Boyle JJ, Li Z, Linderman SW et al. 2016. Tunability of collagen matrix mechanical properties via multiple modes of mineralization. Interface Focus 6:20150070
    [Google Scholar]
  107. 107.  Boyle JJ, Kume M, Wyczalkowski MA, Taber LA, Pless RB et al. 2014. Simple and accurate methods for quantifying deformation, disruption, and development in biological tissues. J. R. Soc. Interface 11:20140685
    [Google Scholar]
  108. 108.  Furseth Klinge R 2001. The structure of the fibrous tissue on the articular surface of the temporal bone in the monkey (Macaca mulatta). Micron 32:551–57
    [Google Scholar]
  109. 109.  Furseth Klinge R 1996. The structure of the mandibular condyle in the monkey (Macaca mulatta). Micron 27:381–87
    [Google Scholar]
  110. 110.  Delatte M, Von den Hoff JW, van Rheden REM, Kuijpers-Jagtman AM 2004. Primary and secondary cartilages of the neonatal rat: the femoral head and the mandibular condyle. Eur. J. Oral Sci. 112:156–62
    [Google Scholar]
  111. 111.  Dormer NH, Busaidy K, Berkland CJ, Detamore MS 2011. Osteochondral interface regeneration of rabbit mandibular condyle with bioactive signal gradients. J. Oral Maxillofac. Surg. 69:e50–57
    [Google Scholar]
  112. 112.  Hollister S, Lin C, Saito E, Lin C, Schek R et al. 2005. Engineering craniofacial scaffolds. Orthod. Craniofac. Res. 8:162–73
    [Google Scholar]
  113. 113.  Murphy MK, MacBarb RF, Wong ME, Athanasiou KA 2013. Temporomandibular disorders: a review of etiology, clinical management, and tissue engineering strategies. Int. J. Oral Maxillofac. Implants 28:e393–414
    [Google Scholar]
  114. 114.  Bailey MM, Wang L, Bode CJ, Mitchell KE, Detamore MS 2007. A comparison of human umbilical cord matrix stem cells and temporomandibular joint condylar chondrocytes for tissue engineering temporomandibular joint condylar cartilage. Tissue Eng 13:2003–10
    [Google Scholar]
  115. 115.  Wang L, Detamore MS 2007. Tissue engineering the mandibular condyle. Tissue Eng 13:1955–71
    [Google Scholar]
  116. 116.  Detamore MS, Athanasiou KA 2003. Structure and function of the temporomandibular joint disc: Implications for tissue engineering. J. Oral Maxillofac. Surg. 61:494–506
    [Google Scholar]
  117. 117.  Detamore MS, Athanasiou KA 2003. Motivation, characterization, and strategy for tissue engineering the temporomandibular joint disc. Tissue Eng 9:1065–87
    [Google Scholar]
  118. 118.  Zimmerman BK, Bonnevie ED, Park M, Zhou Y, Wang L et al. 2015. Role of interstitial fluid pressurization in TMJ lubrication. J. Dent. Res. 94:85–92
    [Google Scholar]
  119. 119.  Bonnevie ED, Baro V, Wang L, Burris DL 2011. In-situ studies of cartilage microtribology: roles of speed and contact area. Tribol. Lett. 41:83–95
    [Google Scholar]
  120. 120.  Ateshian GA 2009. The role of interstitial fluid pressurization in articular cartilage lubrication. J. Biomech. 42:1163–76
    [Google Scholar]
  121. 121.  Bonnevie ED, Baro VJ, Wang L, Burris DL 2012. Fluid load support during localized indentation of cartilage with a spherical probe. J. Biomech. 45:1036–41
    [Google Scholar]
  122. 122.  Weng Y, Cao Y, Arevalo C, Vacanti MP, Vacanti CA 2001. Tissue-engineered composites of bone and cartilage for mandible condylar reconstruction. J. Oral Maxillofac. Surg. 59:185–90
    [Google Scholar]
  123. 123.  Schek R, Taboas J, Hollister S, Krebsbach P 2005. Tissue engineering osteochondral implants for temporomandibular joint repair. Orthod. Craniofac. Res. 8:313–19
    [Google Scholar]
  124. 124.  Alhadlaq A, Mao JJ 2003. Tissue-engineered neogenesis of human-shaped mandibular condyle from rat mesenchymal stem cells. J. Dent. Res. 82:951–56
    [Google Scholar]
  125. 125.  Feinberg SE, Hollister SJ, Halloran JW, Chu TM, Krebsbach PH 2001. Image-based biomimetic approach to reconstruction of the temporomandibular joint. Cells Tissues Organs 169:309–21
    [Google Scholar]
  126. 126.  Johannessen W, Elliott DM 2005. Effects of degeneration on the biphasic material properties of human nucleus pulposus in confined compression. Spine 30:E724–29
    [Google Scholar]
  127. 127.  Urban JP, McMullin JF 1988. Swelling pressure of the lumbar intervertebral discs: influence of age, spinal level, composition, and degeneration. Spine 13:179–87
    [Google Scholar]
  128. 128.  Cassidy JJ, Hiltner A, Baer E 1989. Hierarchical structure of the intervertebral disc. Connect. Tissue Res. 23:75–88
    [Google Scholar]
  129. 129.  Moon SM, Yoder JH, Wright AC, Smith LJ, Vresilovic EJ, Elliott DM 2013. Evaluation of intervertebral disc cartilaginous endplate structure using magnetic resonance imaging. Eur. Spine J. 22:1820–28
    [Google Scholar]
  130. 130.  Gullbrand SE, Ashinsky BG, Martin JT, Pickup S, Smith LJ et al. 2016. Correlations between quantitative T2 and T1 ρ MRI, mechanical properties and biochemical composition in a rabbit lumbar intervertebral disc degeneration model. J. Orthop. Res. 34:1382–88
    [Google Scholar]
  131. 131.  Luoma K, Riihimäki H, Luukkonen R, Raininko R, Viikari-Juntura E, Lamminen A 2000. Low back pain in relation to lumbar disc degeneration. Spine 25:487–92
    [Google Scholar]
  132. 132.  Bhattacharjee M, Miot S, Gorecka A, Singha K, Loparic M et al. 2012. Oriented lamellar silk fibrous scaffolds to drive cartilage matrix orientation: towards annulus fibrosus tissue engineering. Acta Biomater 8:3313–25
    [Google Scholar]
  133. 133.  Wan Y, Feng G, Shen FH, Laurencin CT, Li X 2008. Biphasic scaffold for annulus fibrosus tissue regeneration. Biomaterials 29:643–52
    [Google Scholar]
  134. 134.  Sato M, Asazuma T, Ishihara M, Ishihara M, Kikuchi T et al. 2003. An experimental study of the regeneration of the intervertebral disc with an allograft of cultured annulus fibrosus cells using a tissue-engineering method. Spine 28:548–53
    [Google Scholar]
  135. 135.  Moriguchi Y, Borde B, Grunert P, Khair T, Hudson K et al. 2015. Annular repair using high-density collagen gels seeded with fibrochondrocytes: in vivo outcome in the rodent spine. Spine J 15:S187–88
    [Google Scholar]
  136. 136.  Nerurkar NL, Elliott DM, Mauck RL 2007. Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering. J. Orthop. Res. 25:1018–28
    [Google Scholar]
  137. 137.  Nerurkar NL, Baker BM, Sen S, Wible EE, Elliott DM, Mauck RL 2009. Nanofibrous biologic laminates replicate the form and function of the annulus fibrosus. Nat. Mater. 8:986–92
    [Google Scholar]
  138. 138.  Moriguchi Y, Mojica-Santiago J, Grunert P, Pennicooke B, Berlin C et al. 2017. Total disc replacement using tissue-engineered intervertebral discs in the canine cervical spine. PLOS ONE 12:e0185716
    [Google Scholar]
  139. 139.  Mwale F, Roughley P, Antoniou J 2004. Distinction between the extracellular matrix of the nucleus pulposus and hyaline cartilage: a requisite for tissue engineering of intervertebral disc. Eur. Cell. Mater. 8:58–63
    [Google Scholar]
  140. 140.  Iatridis JC, Setton LA, Weidenbaum M, Mow VC 1997. The viscoelastic behavior of the non-degenerate human lumbar nucleus pulposus in shear. J. Biomech. 30:1005–13
    [Google Scholar]
  141. 141.  Séguin CA, Grynpas MD, Pilliar RM, Waldman SD, Kandel RA 2004. Tissue engineered nucleus pulposus tissue formed on a porous calcium polyphosphate substrate. Spine 29:1299–306
    [Google Scholar]
  142. 142.  Chou AI, Akintoye SO, Nicoll SB 2009. Photo-crosslinked alginate hydrogels support enhanced matrix accumulation by nucleus pulposus cells in vivo. Osteoarthr. Cartil. 17:1377–84
    [Google Scholar]
  143. 143.  Roughley P, Hoemann C, DesRosiers E, Mwale F, Antoniou J, Alini M 2006. The potential of chitosan-based gels containing intervertebral disc cells for nucleus pulposus supplementation. Biomaterials 27:388–96
    [Google Scholar]
  144. 144.  Risbud MV, Albert TJ, Guttapalli A, Vresilovic EJ, Hillibrand AS et al. 2004. Differentiation of mesenchymal stem cells towards a nucleus pulposus–like phenotype in vitro: implications for cell-based transplantation therapy. Spine 29:2627–32
    [Google Scholar]
  145. 145.  Hunter CJ, Matyas JR, Duncan NA 2003. The notochordal cell in the nucleus pulposus: a review in the context of tissue engineering. Tissue Eng 9:667–77
    [Google Scholar]
  146. 146.  Lee K-I, Moon S-H, Kim H, Kwon U-H, Kim H-J et al. 2012. Tissue engineering of the intervertebral disc with cultured nucleus pulposus cells using atelocollagen scaffold and growth factors. Spine 37:452–58
    [Google Scholar]
  147. 147.  Stoyanov J V, Gantenbein-Ritter B, Bertolo A, Aebli N, Baur M et al. 2011. Role of hypoxia and growth and differentiation factor 5 on differentiation of human mesenchymal stem cells towards intervertebral nucleus pulposus–like cells. Eur. Cell. Mater. 21:533–47
    [Google Scholar]
  148. 148.  Mizuno H, Roy AK, Zaporojan V, Vacanti CA, Ueda M, Bonassar LJ 2006. Biomechanical and biochemical characterization of composite tissue-engineered intervertebral discs. Biomaterials 27:362–70
    [Google Scholar]
  149. 149.  Mizuno H, Roy AK, Vacanti CA, Kojima K, Ueda M, Bonassar LJ 2004. Tissue-engineered composites of anulus fibrosus and nucleus pulposus for intervertebral disc replacement. Spine 29:1290–87
    [Google Scholar]
  150. 150.  Nerurkar NL, Sen S, Huang AH, Elliott DM, Mauck RL 2010. Engineered disc-like angle-ply structures for intervertebral disc replacement. Spine 35:867–73
    [Google Scholar]
  151. 151.  Nesti LJ, Li W-J, Shanti RM, Jiang YJ, Jackson W et al. 2008. Intervertebral disc tissue engineering using a novel hyaluronic acid–nanofibrous scaffold (HANFS) amalgam. Tissue Eng. A 14:1527–37
    [Google Scholar]
  152. 152.  Bowles RD, Williams RM, Zipfel WR, Bonassar LJ 2010. Self-assembly of aligned tissue-engineered annulus fibrosus and intervertebral disc composite via collagen gel contraction. Tissue Eng. A 16:1339–48
    [Google Scholar]
  153. 153.  Bowles RD, Gebhard HH, Hartl R, Bonassar LJ 2011. Tissue-engineered intervertebral discs produce new matrix, maintain disc height, and restore biomechanical function to the rodent spine. PNAS 108:13106–11
    [Google Scholar]
  154. 154.  Martin JT, Kim DH, Milby AH, Pfeifer CG, Smith LJ et al. 2017. In vivo performance of an acellular disc-like angle ply structure (DAPS) for total disc replacement in a small animal model. J. Orthop. Res. 35:23–31
    [Google Scholar]
  155. 155.  Martin JT, Milby AH, Chiaro JA, Kim DH, Hebela NM et al. 2014. Translation of an engineered nanofibrous disc-like angle-ply structure for intervertebral disc replacement in a small animal model. Acta Biomater 10:2473–81
    [Google Scholar]
  156. 156.  Benneker LM, Heini PF, Alini M, Anderson SE, Ito K 2005. 2004 Young Investigator Award Winner: Vertebral endplate marrow contact channel occlusions and intervertebral disc degeneration. Spine 30:167–73
    [Google Scholar]
  157. 157.  Martin JT, Gullbrand SE, Kim DH, Ikuta K, Pfeifer CG et al. 2017. In vitro maturation and in vivo integration and function of an engineered cell-seeded disc-like angle ply structure (DAPS) for total disc arthroplasty. Sci. Rep. 7:15765
    [Google Scholar]
  158. 158.  Engler AJ, Sen S, Sweeney HL, Discher DE 2006. Matrix elasticity directs stem cell lineage specification. Cell 126:677–89
    [Google Scholar]
  159. 159.  Han WM, Heo SJ, Driscoll TP, Delucca JF, McLeod CM et al. 2016. Microstructural heterogeneity directs micromechanics and mechanobiology in native and engineered fibrocartilage. Nat. Mater. 15:477–84
    [Google Scholar]
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