Stem cells for tendon tissue engineering and regeneration

Expert Opinion on Biological Therapy

Volumn 10, Issue 5, 2010, Pages 689-700

  Yin, Zi ^a   Chen, Xiao ^a   Chen, Jia Lin ^a   Ouyang, Hong Wei ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Regeneration; Stem cells; Tendon; Tissue engineering

Indexed keywords

BIOLOGICAL MARKER; BIOMATERIAL; CARBON FIBER; COLLAGEN FIBRIL; ELASTIN; GLYCOPROTEIN; GLYCOSAMINOGLYCAN; GROWTH FACTOR; POLITEF; POLYESTER; POLYETHYLENE; POLYGLYCOLIC ACID; PROTEOGLYCAN; SILICON;

AUTOGRAFT; BIOREACTOR; CELL DIFFERENTIATION; CELL LINEAGE; COCULTURE; DNA MODIFICATION; EMBRYONIC STEM CELL; FIBROBLAST; HUMAN; MECHANICAL STIMULATION; MECHANICAL STRESS; MESENCHYMAL STEM CELL; NONHUMAN; PROSTHESIS; PROSTHESIS FAILURE; REVIEW; TENDON; TENDON INJURY; TENSILE STRENGTH; TISSUE ENGINEERING; TISSUE REGENERATION;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINEAGE; HUMANS; STEM CELL TRANSPLANTATION; STEM CELLS; TENDON INJURIES; TENDONS; TISSUE ENGINEERING; TREATMENT OUTCOME; WOUND HEALING;

EID: 77951116574     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712591003769824     Document Type: Review

References (111)

1. Maffulli N, Wong J, Almekinders LC. Types and epidemiology of tendinopathy. Clin Sports Med 2003;22:675-692
2. Favata M, Beredjiklian PK, Zgonis MH, et al. Regenerative properties of fetal sheep tendon are not adversely affected by transplantation into an adult environment. J Orthop Res 2006;24:2124-2132
3. Goh JC, Ouyang HW, Teoh SH, et al. Tissue-engineering approach to the repair and regeneration of tendons and ligaments. Tissue Engineering 2003;9:S31-31S44
4. Jozsa L, Kannus P, Balint JB, Reffy A. Three-dimensional ultrastructure of human tendons. Acta Anat (Basel) 1991;142:306-312
5. Rowe RW. The structure of rat tail tendon fascicles. Connect Tissue Res 1985;14:21-30
6. Kastelic J, Galeski A, Baer E. The multicomposite structure of tendon. Connect Tissue Res 1978;6:11-23
7. Moore MJ, De Beaux A. A quantitative ultrastructural study of rat tendon from birth to maturity. J Anat 1987;153:163-169
8. Amiel D, Frank C, Harwood F, et al. Tendons and ligaments: a morphological and biochemical comparison. J Orthop Res 1984;1:257-265
9. Benjamin M, Kumai T, Milz S, et al. The skeletal attachment of tendons--tendon "entheses". Comp Biochem Physiol A Mol Integr Physiol 2002;133:931-945
10. Benjamin M, Ralphs JR. Fibrocartilage in tendons and ligaments-an adaptation to compressive load. J Anat 1998;193(Pt 4):481-494
11. Salamon A, Hamori J, Deak G, Mayer F. Submicroscopic investigation of autogenous tendon grafts. Acta Morphol Acad Sci Hung 1970;18:23-42
12. Levine SN. Survey of biomedical materials and some relevant problems. Ann NY Acad Sci 1968;146:3-10
13. Grau HR. The artificial tendon: an experimental study. Plast Reconstr Surg Transplant Bull 1958;22:562-566
14. Gonzalez RI. Experimental use of teflon in tendon surgery. Plast Reconstr Surg Transplant Bull 1959;23:535-539
15. Goodship AE, Brown PN, Yeats JJ, et al. An assessment of filamentous carbon fibre for the treatment of tendon injury in the horse. Vet Rec 1980;106:217-221
16. Cao Y, Vacanti JP, Ma X, et al. Generation of neo-tendon using synthetic polymers seeded with tenocytes. Transplant Proc 1994;26:3390-3392
17. Calve S, Dennis RG, Kosnik PE II, et al. Engineering of functional tendon. Tissue Eng 2004;10:755-761
18. Bi Y, Ehirchiou D, Kilts TM, et al. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med 2007;13:1219-1227
19. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997;276:71-74
20. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001;44:1928-1942
21. De Bari C, Dell'Accio F, Vanlauwe J, et al. Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis Rheum 2006;54:1209-1221
22. Miro D, Julia MV, Sitges-Serra A. Wound breaking strength and healing after suturing noninjured tissues. J Am Coll Surg 1995;180:659-665
23. Lee HS, Huang GT, Chiang H, et al. Multipotential mesenchymal stem cells from femoral bone marrow near the site of osteonecrosis. Stem Cells 2003;21:190-199
24. Kim JW, Kim SY, Park SY, et al. Mesenchymal progenitor cells in the human umbilical cord. Ann Hematol 2004;83:733-738
25. Salingcarnboriboon R, Yoshitake H, Tsuji K, et al. Establishment of tendon-derived cell lines exhibiting pluripotent mesenchymal stem cell-like property. Exp Cell Res 2003;287:289-300
26. Dowthwaite GP, Bishop JC, Redman SN, et al. The surface of articular cartilage contains a progenitor cell population. J Cell Sci 2004;117:889-897
27. Seo BM, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004;364:149-155
28. Young RG, Butler DL, Weber W, et al. Use of mesenchymal stem cells in a collagen matrix for Achilles tendon repair. J Orthop Res 1998;16:406-413
29. Juncosa-Melvin N, Boivin GP, Galloway MT, et al. Effects of cell-to-collagen ratio in stem cell-seeded constructs for Achilles tendon repair. Tissue Eng 2006;12:681-689
30. Awad HA, Butler DL, Boivin GP, et al. Autologous mesenchymal stem cell-mediated repair of tendon. Tissue Eng 1999;5:267-277
31. Juncosa-Melvin N, Boivin GP, Galloway MT, et al. Effects of cell-to-collagen ratio in mesenchymal stem cell-seeded implants on tendon repair biomechanics and histology. Tissue Eng 2005;11:448-457
32. Ouyang HW, Cao T, Zou XH, et al. Mesenchymal stem cell sheets revitalize nonviable dense grafts: implications for repair of large-bone and tendon defects. Transplantation 2006;82:170-174
33. Ouyang HW, Toh SL, Goh J, et al. Assembly of bone marrow stromal cell sheets with knitted poly (L-lactide) scaffold for engineering ligament analogs. J Biomed Mater Res B Appl Biomater 2005;75:264-271
34. Chong AK, Ang AD, Goh JC, et al. Bone marrow-derived mesenchymal stem cells influence early tendon-healing in a rabbit achilles tendon model. J Bone Joint Surg Am 2007;89:74-81
35. Harris MT, Butler DL, Boivin GP, et al. Mesenchymal stem cells used for rabbit tendon repair can form ectopic bone and express alkaline phosphatase activity in constructs. J Orthop Res 2004;22:998-1003
36. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 2005;52:2521-2529
37. Beredjiklian PK, Favata M, Cartmell JS, et al. Regenerative versus reparative healing in tendon: a study of biomechanical and histological properties in fetal sheep. Ann Biomed Eng 2003;31:1143-1152
38. Wobus AM, Boheler KR. Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 2005;85:635-678
39. Duplomb L, Dagouassat M, Jourdon P, Heymann D. Concise review: embryonic stem cells: a new tool to study osteoblast and osteoclast differentiation. Stem Cells 2007;25:544-552
40. Bradley JA, Bolton EM, Pedersen RA. Stem cell medicine encounters the immune system. Nat Rev Immunol 2002;2:859-871
41. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981;78:7634-7638
42. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981;292:154-156
43. Guillot PV, Cui W, Fisk NM, Polak DJ. Stem cell differentiation and expansion for clinical applications of tissue engineering. J Cell Mol Med 2007;11:935-944
44. Crook JM, Peura TT, Kravets L, et al. The generation of six clinical-grade human embryonic stem cell lines. Cell Stem Cell 2007;1:490-494
45. Barberi T, Willis LM, Socci ND, Studer L. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2005;2:e161: published online 28 June 2005, doi:10.1371/journal.pmed.0020161 (Pubitemid 40973509)
46. Olivier EN, Rybicki AC, Bouhassira EE. Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells 2006;24:1914-1922
47. Chen X, Song XH, Yin Z, et al. Stepwise differentiation of human embryonic stem cells promotes tendon regeneration by secreting fetal tendon matrix and differentiation factors. Stem Cells 2009;27:1276-1287
48. Mendias CL, Bakhurin KI, Faulkner JA. Tendons of myostatin-deficient mice are small, brittle, and hypocellular. Proc Natl Acad Sci USA 2008;105:388-393
49. Hankemeier S, Keus M, Zeichen J, et al. Modulation of proliferation and differentiation of human bone marrow stromal cells by fibroblast growth factor 2: potential implications for tissue engineering of tendons and ligaments. Tissue Eng 2005;11:41-49
50. Chan BP, Chan KM, Maffulli N, et al. Effect of basic fibroblast growth factor. An in vitro study of tendon healing. Clin Orthop Relat Res 1997;342:9-47
51. Costa MA, Wu C, Pham BV, et al. Tissue engineering of flexor tendons: optimization of tenocyte proliferation using growth factor supplementation. Tissue Eng 2006;12:1937-1943
52. Folkman J, Klagsbrun M. Angiogenic factors. Science 1987;235:442-447
53. Moreau JE, Chen J, Bramono DS, et al. Growth factor induced fibroblast differentiation from human bone marrow stromal cells in vitro. Journal of Orthopaedic Research 2005;23:164-174
54. Wolfman NM, Hattersley G, Cox K, et al. Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5, 6, and 7, members of the TGF-beta gene family. J Clin Invest 1997;100:321-330
55. Forslund C, Aspenberg P. CDMP-2 induces bone or tendon-like tissue depending on mechanical stimulation. J Orthop Res 2002;20:1170-1174
56. Forslund C, Aspenberg P. Tendon healing stimulated by injected CDMP-2. Med Sci Sports Exerc 2001;33:685-687
57. Forslund C, Rueger D, Aspenberg P. A comparative dose-response study of cartilage-derived morphogenetic protein (CDMP)-1, -2 and -3 for tendon healing in rats. J Orthop Res 2003;21:617-621
58. Maffulli N, Moller HD, Evans CH. Tendon healing: can it be optimised. Br J Sports Med 2002;36:315-316
59. Helm GA, Li JZ, Alden TD, et al. A light and electron microscopic study of ectopic tendon and ligament formation induced by bone morphogenetic protein-13 adenoviral gene therapy. J Neurosurg 2001;95:298-307
60. Wang XT, Liu PY, Tang JB. Tendon healing in vitro: genetic modification of tenocytes with exogenous PDGF gene and promotion of collagen gene expression. J Hand Surg [Am] 2004;29:884-890
61. Nakamura N, Shino K, Natsuume T, et al. Early biological effect of in vivo gene transfer of platelet-derived growth factor (PDGF)-B into healing patellar ligament. Gene Ther 1998;5:1165-1170
62. Hou Y, Mao Z, Wei X, et al. Effects of transforming growth factor-beta1 and vascular endothelial growth factor 165 gene transfer on Achilles tendon healing. Matrix Biol 2009;28:324-335
63. Schnabel LV, Lynch ME, van der Meulen MC, et al. Mesenchymal stem cells and insulin-like growth factor-I gene-enhanced mesenchymal stem cells improve structural aspects of healing in equine flexor digitorum superficialis tendons. J Orthop Res 2009;27:1392-1398
64. Wang QW, Chen ZL, Piao YJ. Mesenchymal stem cells differentiate into tenocytes by bone morphogenetic protein (BMP) 12 gene transfer. J Biosci Bioeng 2005;100:418-422
65. Lou J, Tu Y, Ludwig FJ, et al. Effect of bone morphogenetic protein-12 gene transfer on mesenchymal progenitor cells. Clin Orthop Relat Res 1999;333-339
66. Takeuchi JK, Bruneau BG. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 2009;459:708-711
67. Viczian AS, Solessio EC, Lyou Y, Zuber ME. Generation of functional eyes from pluripotent cells. PLoS Biol 2009;7:e1000174: published online 18 August 2009, doi: 10.1371/journal.pbio.1000174
68. Li Y, Zhang R, Qiao H, et al. Generation of insulin-producing cells from PDX-1 gene-modified human mesenchymal stem cells. J Cell Physiol 2007;211:36-44
69. Satomura K, Krebsbach P, Bianco P, Gehron RP. Osteogenic imprinting upstream of marrow stromal cell differentiation. J Cell Biochem 2000;78:391-403
70. Buckingham ME. Muscle: the regulation of myogenesis. Curr Opin Genet Dev 1994;4:745-751
71. Cserjesi P, Brown D, Ligon KL, et al. Scleraxis: a basic helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development 1995;121:1099-1110
72. Brent AE, Schweitzer R, Tabin CJ. A somitic compartment of tendon progenitors. Cell 2003;113:235-248
73. Murchison ND, Price BA, Conner DA, et al. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development 2007;134:2697-2708
74. Léjard V, Brideau G, Blais F, et al. Scleraxis and NFATc regulate the expression of the pro-alpha1(I) collagen gene in tendon fibroblasts. J Biol Chem 2007;282:17665-17675
75. Shukunami C, Takimoto A, Oro M, Hiraki Y. Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev Biol 2006;298:234-247
76. Aslan H, Kimelman-Bleich N, Pelled G, Gazit D. Molecular targets for tendon neoformation. J Clin Invest 2008;118:439-444
77. Hoffmann A, Pelled G, Turgeman G, et al. Neotendon formation induced by manipulation of the Smad8 signalling pathway in mesenchymal stem cells. J Clin Invest 2006;116(4):940-952
78. van Eijk F, Saris DB, Creemers LB, et al. The effect of timing of mechanical stimulation on proliferation and differentiation of goat bone marrow stem cells cultured on braided PLGA scaffolds. Tissue Eng Part A 2008;14:1425-1433
79. Sen B, Styner M, Xie Z, et al. Mechanical loading regulates NFATc1 and beta-catenin signaling through a GSK3beta control node. J Biol Chem 2009;284:34607-34617
80. J Juncosa-Melvin N, Matlin KS, Holdcraft RW, et al. Mechanical stimulation increases collagen type I and collagen type III gene expression of stem cell-collagen sponge constructs for patellar tendon repair. Tissue Eng 2007;13:1219-1226
81. Yang G, Crawford RC, Wang JH. Proliferation and collagen production of human patellar tendon fibroblasts in response to cyclic uniaxial stretching in serum-free conditions. J Biomech 2004;37:1543-1550
82. Scott A, Cook JL, Hart DA, et al. Tenocyte responses to mechanical loading in vivo: A role for local insulin-like growth factor 1 signaling in early tendinosis in rats. Arthritis Rheum 2007;56:871-881
83. Feng Z, Ishibashi M, Nomura Y, et al. Constraint stress, microstructural characteristics, and enhanced mechanical properties of a special fibroblast-embedded collagen construct. Artif Organs 2006;30:870-877
84. Chen J, Horan RL, Bramono D, et al. Monitoring mesenchymal stromal cell developmental stage to apply on-time mechanical stimulation for ligament tissue engineering. Tissue Eng 2006 12:3085-3095
85. Webb K, Hitchcock RW, Smeal RM, et al. Cyclic strain increases fibroblast proliferation, matrix accumulation, and elastic modulus of fibroblast-seeded polyurethane constructs. J Biomech 2006;39:1136-1144
86. Kuo CK, Tuan RS. Mechanoactive tenogenic differentiation of human mesenchymal stem cells. Tissue Eng Part A 2008;14:1615-1627
87. Kahn CJ, Vaquette C, Rahouadj R, Wang X. A novel bioreactor for ligament tissue engineering. Biomed Mater Eng 2008;18:283-287
88. Butler DL, Hunter SA, Chokalingam K, et al. Using functional tissue engineering and bioreactors to mechanically stimulate tissue-engineered constructs. Tissue Eng Part A 2009;15:741-749
89. Joshi SD, Webb K. Variation of cyclic strain parameters regulates development of elastic modulus in fibroblast/substrate constructs. J Orthop Res 2008;26:1105-1113
90. Lee CH, Shin HJ, Cho IH, et al. Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast. Biomaterials 2005;26:1261-1270
91. Henshaw DR, Attia E, Bhargava M, Hannafin JA. Canine ACL fibroblast integrin expression and cell alignment in response to cyclic tensile strain in three-dimensional collagen gels. J Orthop Res 2006;24:481-490
92. Ma PX. Biomimetic materials for tissue engineering. Adv Drug Deliv Rev 2008;60:184-198
93. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006;126:677-689
94. McBeath R, Pirone DM, Nelson CM, et al. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004;6:483-495
95. Teixeira AI, McKie GA, Foley JD, et al. The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography. Biomaterials 2006;27:3945-3954
96. Recknor JB, Sakaguchi DS, Mallapragada SK. Directed growth and selective differentiation of neural progenitor cells on micropatterned polymer substrates. Biomaterials 2006;27:4098-4108
97. Lenhert S, Meier MB, Meyer U, et al. Osteoblast alignment, elongation and migration on grooved polystyrene surfaces patterned by Langmuir-Blodgett lithography. Biomaterials 2005;26:563-570
98. Dalby MJ, Gadegaard N, Tare R, et al. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 2007;6:997-1003
99. Smith LA, Liu X, Hu J, et al. Enhancing osteogenic differentiation of mouse embryonic stem cells by nanofibers. Tissue Eng Part A 2009;15:1855-1864
100. Yim EK, Pang SW, Leong KW. Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res 2007;313:1820-1829
101. Arnold M, Hirschfeld-Warneken VC, Lohmuller T, et al. Induction of cell polarization and migration by a gradient of nanoscale variations in adhesive ligand spacing. Nano Lett 2008;8:2063-2069
102. Nisbet DR, Yu LM, Zahir T, et al. Characterization of neural stem cells on electrospun poly(epsilon-caprolactone) submicron scaffolds: evaluating their potential in neural tissue engineering. J Biomater Sci Polym Ed 2008;19:623-634
103. Yin Z, Chen X, Chen JL, et al. The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials 2010;31:2163-2175
104. Koyanagi M, Haendeler J, Badorff C, et al. Non-canonical Wnt signaling enhances differentiation of human circulating progenitor cells to cardiomyogenic cells. J Biol Chem 2005;280:16838-16842
105. Fan H, Liu H, Toh SL, Goh JC. Enhanced differentiation of mesenchymal stem cells co-cultured with ligament fibroblasts on gelatin/silk fibroin hybrid scaffold. Biomaterials 2008;29:1017-1027
106. Krassowska A, Gordon-Keylock S, Samuel K, et al. Promotion of haematopoietic activity in embryonic stem cells by the aorta-gonad-mesonephros microenvironment. Exp Cell Res 2006;312:3595-3603
107. Lee HJ, Yu C, Chansakul T, et al. Enhanced chondrogenic differentiation of embryonic stem cells by coculture with hepatic cells. Stem Cells Dev 2008;17:555-563
108. InançB, Elçin AE, Unsal E, et al. Differentiation of human embryonic stem cells on periodontal ligament fibroblasts in vitro. Artif Organs 2008;32:100-109
109. Plotnikov EY, Khryapenkova TG, Vasileva AK, et al. Cell-to-cell cross-talk between mesenchymal stem cells and cardiomyocytes in co-culture. J Cell Mol Med 2008;12:1622-1631
110. Boland MJ, Hazen JL, Nazor KL, et al. Adult mice generated from induced pluripotent stem cells. Nature 2009;461:91-94
111. Jelinsky SA, Archambault J, Li L, Seeherman H. Tendon-selective genes identified from rat and human musculoskeletal tissues. J Orthop Res 2010;28:289-297