Tendon-derived stem cells as a new cell source for tendon tissue engineering

Frontiers in Bioscience

Volumn 18, Issue 2, 2013, Pages 756-764

  Zhang, Qiang ^a   Cheng, Biao ^a  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Regeneration; Review; Stem Cells; TDSCS; Tendon; Tendon Derived; Tissue Engineering

Indexed keywords

SCLEROPROTEIN;

ADULT; AGED; ANIMAL; BIOMECHANICS; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; HUMAN; METABOLISM; REGENERATION; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION; TENDON; TENDON INJURY; TISSUE ENGINEERING;

ADULT; AGED; ANIMALS; BIOMECHANICS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EXTRACELLULAR MATRIX PROTEINS; HUMANS; REGENERATION; STEM CELL TRANSPLANTATION; STEM CELLS; TENDON INJURIES; TENDONS; TISSUE ENGINEERING;

MLCS; MLOWN;

EID: 84878787566     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4138     Document Type: Article

References (64)

1. J. Zhang and J. H. Wang: Platelet-rich plasma releasate promotes differentiation of tendon stem cells into active tenocytes. AmJ Sports Med 38(12), 2477-86 (2010)
2. E. Pennisi: Tending tender tendons. Science 295(5557), 1011 (2002) (Pubitemid 34132216)
3. D. L. Butler, N. Juncosa and M. R. Dressler: Functional efficacy of tendon repair processes. Annu Rev Biomed Eng 6, 303-29 (2004) (Pubitemid 39209501)
4. C. S. Proctor, D. W. Jackson and T. M. Simon: Characterization of the repair tissue after removal of the central one-third of the patellar ligament. An experimental study in a goat model. J Bone Joint Surg Am 79(7), 997-1006 (1997) (Pubitemid 27310569)
5. Y. Bi, D. Ehirchiou, T. M. Kilts, C. A. Inkson, M. C. Embree, W. Sonoyama, L. Li, A. I. Leet, B. M. Seo, L. Zhang, S. Shi and M. F. Young: Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med 13(10), 1219-27 (2007) (Pubitemid 47530625)
6. J. Zhang and J. H. Wang: Characterization of differential properties of rabbit tendon stem cells and tenocytes. BMC Musculoskelet Disord 11, 10 (2010)
7. Y. F. Rui, P. P. Lui, G. Li, S. C. Fu, Y. W. Lee and K. M. Chan: Isolation and characterization of multipotent rat tendonderived stem cells. Tissue Eng Part A 16(5), 1549-58 (2010)
8. A. B. Lovati, B. Corradetti, A. Lange Consiglio, C. Recordati, E. Bonacina, D. Bizzaro and F. Cremonesi: Characterization and differentiation of equine tendon-derived progenitor cells. J Biol Regul Homeost Agents 25(2 Suppl), S75-84 (2011)
9. Z. Yin, X. Chen, J. L. Chen, W. L. Shen, T. M. Hieu Nguyen, L. Gao and H. W. Ouyang: The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials 31(8), 2163-75 (2010)
10. D. C. Chow, L. A. Wenning, W. M. Miller and E. T. Papoutsakis: Modeling pO(2) distributions in the bone marrow hematopoietic compartment. II. Modified Kroghian models. Biophys J 81(2), 685-96 (2001) (Pubitemid 32721444)
11. M. Rocca, G. Giavaresi, N. Nicoli Aldini, M. Fini, M. Marcacci, S. Zaffagnini and R. Giardino: pO2 measurement in an experimental model of patellar tendon autograft proanterior cruciate ligament. Int J Artif Organs 21(3), 174-8 (1998) (Pubitemid 28238226)
12. W. Y. Lee, P. P. Lui and Y. F. Rui: Hypoxia-mediated efficient expansion of human tendon-derived stem cells in vitro. Tissue Eng Part A 18(5-6), 484-98 (2012)
13. D. C. Colter, R. Class, C. M. DiGirolamo and D. J. Prockop: Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci U S A, 97(7) 3213-8 (2000)
14. M. Dezawa, H. Ishikawa, Y. Itokazu, T. Yoshihara, M. Hoshino, S. Takeda, C. Ide and Y. Nabeshima: Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science 309(5732), 314-7 (2005) (Pubitemid 40967871)
15. Y. Shi, Y. Fu, W. Tong, Y. Geng, P. P. Lui, T. Tang, X. Zhang and K. Dai: Uniaxial mechanical tension promoted osteogenic differentiation of rat tendon-derived stem cells (rTDSCs) via the Wnt5a-RhoA pathway. J Cell Biochem (2012)
16. Q. Tan, P. P. Lui and Y. F. Rui: Effect of in vitro passaging on the stem cell-related properties of tendonderived stem cells-implications in tissue engineering. Stem Cells Dev 21(5), 790-800 (2012)
17. Z. Zhou, T. Akinbiyi, L. Xu, M. Ramcharan, D. J. Leong, S. J. Ros, A. C. Colvin, M. B. Schaffler, R. J. Majeska, E. L. Flatow and H. B. Sun: Tendon-derived stem/progenitor cell aging: defective self-renewal and altered fate. Aging Cell 9(5), 911-5 (2010)
18. F. Haasters, H. Polzer, W. C. Prall, M. M. Saller, J. Kohler, S. Grote, W. Mutschler, D. Docheva and M. Schieker: Bupivacaine, ropivacaine, and morphine: comparison of toxicity on human hamstring-derived stem/progenitor cells. Knee Surg Sports Traumatol Arthrosc 19(12), 2138-44 (2011)
19. Q. Tan, P. P. Lui, Y. F. Rui and Y. M. Wong: Comparison of potentials of stem cells isolated from tendon and bone marrow for musculoskeletal tissue engineering. Tissue Eng Part A 18(7-8), 840-51 (2012)
20. L. Chen, S. W. Dong, J. P. Liu, X. Tao, K. L. Tang and J. Z. Xu: Synergy of tendon stem cells and platelet-rich plasma in tendon healing. J Orthop Res 30(6), 991-7 (2012)
21. Y. F. Rui, P. P. Lui, Y. W. Lee and K. M. Chan: Higher BMP receptor expression and BMP-2-induced osteogenic differentiation in tendon-derived stem cells compared with bone-marrow-derived mesenchymal stem cells. Int Orthop 36(5), 1099-107 (2012)
22. H. Tempfer, A. Wagner, R. Gehwolf, C. Lehner, M. Tauber, H. Resch and H. C. Bauer: Perivascular cells of the supraspinatus tendon express both tendon- and stem cellrelated markers. Histochem Cell Biol 131(6), 733-41 (2009)
23. A. I. Caplan: All MSCs are pericytes? Cell Stem Cell 3(3), 229-30 (2008)
24. L. da Silva Meirelles, P. C. Chagastelles and N. B. Nardi: Mesenchymal stem cells reside in virtually all postnatal organs and tissues. J Cell Sci 119(Pt 11), 2204-13 (2006) (Pubitemid 43960310)
25. P. Alberton, C. Popov, M. Pragert, J. Kohler, C. Shukunami, M. Schieker and D. Docheva: Conversion of human bone marrow-derived mesenchymal stem cells into tendon progenitor cells by ectopic expression of scleraxis. Stem Cells Dev 21(6), 846-58 (2012)
26. J. Zhang and J. H. Wang: Mechanobiological response of tendon stem cells: implications of tendon homeostasis and pathogenesis of tendinopathy. J Orthop Res 28(5), 639- 43 (2010)
27. H. B. Sun, Y. X. Zhu, T. Yin, G. Sledge and Y. C. Yang: MRG1, the product of a melanocyte-specific gene related gene, is a cytokine-inducible transcription factor with transformation activity. Proc Natl Acad Sci U S A 95(23), 13555-60 (1998)
28. K. R. Kranc, S. D. Bamforth, J. Braganca, C. Norbury, M. van Lohuizen and S. Bhattacharya: Transcriptional coactivator Cited2 induces Bmi1 and Mel18 and controls fibroblast proliferation via Ink4a/ARF. Mol Cell Biol 23(21), 7658-66 (2003) (Pubitemid 37271464)
29. H. Yokota, M. B. Goldring and H. B. Sun: CITED2- mediated regulation of MMP-1 and MMP-13 in human chondrocytes under flow shear. J Biol Chem 278(47), 47275-80 (2003)
30. H. B. Sun: CITED2 mechanoregulation of matrix metalloproteinases. Ann N Y Acad Sci 1192, 429-36 (2010)
31. D. T. Scadden: The stem-cell niche as an entity of action. Nature 441(7097), 1075-9 (2006)
32. D. S. Krause: Regulation of hematopoietic stem cell fate. Oncogene 21(21), 3262-9 (2002)
33. B. A. Pryce, S. S. Watson, N. D. Murchison, J. A. Staverosky, N. Dunker and R. Schweitzer: Recruitment and maintenance of tendon progenitors by TGF-beta signaling are essential for tendon formation. Development 136(8), 1351-61 (2009)
34. S. S. Durgam, A. A. Stewart, H. C. Pondenis, A. C. Yates, R. B. Evans and M. C. Stewart: Responses of equine tendon- and bone marrow-derived cells to monolayer expansion with fibroblast growth factor-2 and sequential culture with pulverized tendon and insulin-like growth factor-I. Am J Vet Res 73(1), 162-70 (2012)
35. S. S. Durgam, A. A. Stewart, H. C. Pondenis, S. M. Gutierrez-Nibeyro, R. B. Evans and M. C. Stewart: Comparison of equine tendon- and bone marrow-derived cells cultured on tendon matrix with or without insulin-like growth factor-I supplementation. Am J Vet Res 73(1), 153- 61 (2012)
36. M. Kjaer, H. Langberg, K. Heinemeier, M. L. Bayer, M. Hansen, L. Holm, S. Doessing, M. Kongsgaard, M. R. Krogsgaard and S. P. Magnusson: From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Sports 19(4), 500-10 (2009)
37. C. Beckham, R. Dimond and T. K. Greenlee, Jr.: The role of movement in the development of a digital flexor tendon. Am J Anat 150(3), 443-59 (1977) (Pubitemid 8229230)
38. M. Kjaer, H. Langberg, B. F. Miller, R. Boushel, R. Crameri, S. Koskinen, K. Heinemeier, J. L. Olesen, S. Dossing, M. Hansen, S. G. Pedersen, M. J. Rennie and P. Magnusson: Metabolic activity and collagen turnover in human tendon in response to physical activity. J Musculoskelet Neuronal Interact 5(1), 41-52 (2005) (Pubitemid 40667622)
39. J. Zhang, T. Pan, Y. Liu and J. H. Wang: Mouse treadmill running enhances tendons by expanding the pool of tendon stem cells (TSCs) and TSC-related cellular production of collagen. J Orthop Res 28(9), 1178-83 (2010)
40. Y. F. Rui, P. P. Lui, M. Ni, L. S. Chan, Y. W. Lee and K. M. Chan: Mechanical loading increased BMP-2 expression which promoted osteogenic differentiation of tendon-derived stem cells. J Orthop Res 29(3), 390-6 (2011)
41. A. Scott, P. Danielson, T. Abraham, G. Fong, A. V. Sampaio and T. M. Underhill: Mechanical force modulates scleraxis expression in bioartificial tendons. J Musculoskelet Neuronal Interact 11(2), 124-32 (2011)
42. J. Zhang and J. H. Wang: Production of PGE(2) increases in tendons subjected to repetitive mechanical loading and induces differentiation of tendon stem cells into non-tenocytes. J Orthop Res 28(2), 198-203 (2010)
43. J. Zhang and J. H. Wang: BMP-2 mediates PGE(2) - induced reduction of proliferation and osteogenic differentiation of human tendon stem cells. J Orthop Res 30(1), 47-52 (2012)
44. D. C. Kirouac and P. W. Zandstra: The systematic production of cells for cell therapies. Cell Stem Cell 3(4), 369- 81 (2008)
45. H. W. Ouyang, J. C. Goh, A. Thambyah, S. H. Teoh and E. H. Lee: Knitted poly-lactide-co-glycolide scaffold loaded with bone marrow stromal cells in repair and regeneration of rabbit Achilles tendon. Tissue Eng 9(3), 431-9 (2003) (Pubitemid 36736126)
46. Y. J. Ju, T. Muneta, H. Yoshimura, H. Koga and I. Sekiya: Synovial mesenchymal stem cells accelerate early remodeling of tendon-bone healing. Cell Tissue Res 332(3), 469-78 (2008)
47. K. Stenderup, J. Justesen, E. F. Eriksen, S. I. Rattan and M. Kassem: Number and proliferative capacity of osteogenic stem cells are maintained during aging and in patients with osteoporosis. J Bone Miner Res 16(6), 1120-9 (2001)
48. M. F. Pittenger, A. M. Mackay, S. C. Beck, R. K. Jaiswal, R. Douglas, J. D. Mosca, M. A. Moorman, D. W. Simonetti, S. Craig and D. R. Marshak: Multilineage potential of adult human mesenchymal stem cells. Science 284(5411), 143-7 (1999) (Pubitemid 29282067)
49. G. F. Muschler, C. Boehm and K. Easley: Aspiration to obtain osteoblast progenitor cells from human bone marrow: the influence of aspiration volume. J Bone Joint Surg Am 79(11), 1699-709 (1997) (Pubitemid 27508530)
50. R. Tasso, A. Augello, M. Carida, F. Postiglione, M. G. Tibiletti, B. Bernasconi, S. Astigiano, F. Fais, M. Truini, R. Cancedda and G. Pennesi: Development of sarcomas in mice implanted with mesenchymal stem cells seeded onto bioscaffolds. Carcinogenesis 30(1), 150-7 (2009)
51. M. T. Harris, D. L. Butler, G. P. Boivin, J. B. Florer, E. J. Schantz and R. J. Wenstrup: Mesenchymal stem cells used for rabbit tendon repair can form ectopic bone and express alkaline phosphatase activity in constructs. J Orthop Res 22(5), 998-1003 (2004) (Pubitemid 39145116)
52. R. Izadpanah, C. Trygg, B. Patel, C. Kriedt, J. Dufour, J. M. Gimble and B. A. Bunnell: Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 99(5), 1285-97 (2006)
53. R. Izadpanah, D. Kaushal, C. Kriedt, F. Tsien, B. Patel, J. Dufour and B. A. Bunnell: Long-term in vitro expansion alters the biology of adult mesenchymal stem cells. Cancer Res 68(11), 4229-38 (2008)
54. M. Ni, P. P. Lui, Y. F. Rui, Y. W. Lee, Q. Tan, Y. M. Wong, S. K. Kong, P. M. Lau, G. Li and K. M. Chan: Tendon-derived stem cells (TDSCs) promote tendon repair in a rat patellar tendon window defect model. J Orthop Res 30(4), 613-9 (2012)
55. J. Zhang, B. Li and J. H. Wang: The role of engineered tendon matrix in the stemness of tendon stem cells in vitro and the promotion of tendon-like tissue formation in vivo. Biomaterials 32(29), 6972-81 (2011)
56. W. Shen, J. Chen, Z. Yina, X. Chen, H. Liua, B. C. Heng, W. Chen and H. W. Ouyang: Allogenous tendon stem/progenitor cells in silk scaffold for functional shoulder repair. Cell Transplant (2012)
57. J. Chang, D. Most, E. Stelnicki, J. W. Siebert, M. T. Longaker, K. Hui and W. C. Lineaweaver: Gene expression of transforming growth factor beta-1 in rabbit zone II flexor tendon wound healing: evidence for dual mechanisms of repair. Plast Reconstr Surg, 100(4) 937-44 (1997) (Pubitemid 27386236)
58. J. Chang, R. Thunder, D. Most, M. T. Longaker and W. C. Lineaweaver: Studies in flexor tendon wound healing: neutralizing antibody to TGF-beta1 increases postoperative range of motion. Plast Reconstr Surg 105(1) 148-55 (2000) (Pubitemid 30027042)
59. L. A. Dahlgren, H. O. Mohammed and A. J. Nixon: Temporal expression of growth factors and matrix molecules in healing tendon lesions. J Orthop Res, 23(1) 84-92 (2005) (Pubitemid 40045081)
60. U. G. Longo, A. Lamberti, N. Maffulli and V. Denaro: Tissue engineered biological augmentation for tendon healing: a systematic review. Br Med Bull 98, 31-59 (2011)
61. H. Liu, D. M. Kemeny, B. C. Heng, H. W. Ouyang, A. J. Melendez and T. Cao: The immunogenicity and immunomodulatory function of osteogenic cells differentiated from mesenchymal stem cells. J Immunol 176(5), 2864-71 (2006)
62. M. Dominici, K. Le Blanc, I. Mueller, I. Slaper- Cortenbach, F. Marini, D. Krause, R. Deans, A. Keating, D. Prockop and E. Horwitz: Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4), 315-7 (2006) (Pubitemid 44269669)
63. H. J. Buhring, V. L. Battula, S. Treml, B. Schewe, L. Kanz and W. Vogel: Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci 1106, 262-71 (2007) (Pubitemid 47443036)
64. B. Mazzanti, A. Aldinucci, T. Biagioli, A. Barilaro, S. Urbani, S. Dal Pozzo, M. P. Amato, G. Siracusa, C. Crescioli, C. Manuelli, A. Bosi, R. Saccardi, L. Massacesi and C. Ballerini: Differences in mesenchymal stem cell cytokine profiles between MS patients and healthy donors: implication for assessment of disease activity and treatment. J Neuroimmunol 199(1-2), 142-50 (2008)