Engineered scaffold-free tendon tissue produced by tendon-derived stem cells

Biomaterials

Volumn 34, Issue 8, 2013, Pages 2024-2037

  Ni, Ming ^a,b   Rui, Yun Feng ^a,c   Tan, Qi ^a   Liu, Yang ^a   Xu, Liang Liang ^a   Chan, Kai Ming ^a   Wang, Yan ^b   Li, Gang ^a  

^a Prince of Wales Hospital   (Hong Kong)

^b CHINESE PLA GENERAL HOSPITAL   (China)

^c MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

Author keywords

Cell sheet; Connective tissue growth factor; Scaffold free; Tendon tissue engineering; Tendon derived stem cells; Tenogenic differentiation

Indexed keywords

ASCORBIC ACID; BIOCOMPATIBILITY; CELL ENGINEERING; CELL PROLIFERATION; COLLAGEN; CYTOLOGY; FLUORESCENCE IMAGING; HISTOLOGY; REPAIR; SCAFFOLDS (BIOLOGY); STEM CELLS;

BIOMECHANICAL TESTING; CELL SHEET; CONNECTIVE TISSUE GROWTH FACTOR; IMMUNOHISTOCHEMISTRY; PATELLAR TENDON; PROOF OF CONCEPT; TENDON TISSUES; TENOGENIC;

TENDONS;

ASCORBIC ACID; CONNECTIVE TISSUE GROWTH FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; CONTROLLED STUDY; FLUORESCENCE IMAGING; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; TENDON; TISSUE ENGINEERING;

MUS MUSCULUS; RATTUS;

EID: 84871479816     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.11.046     Document Type: Article

References (50)

1. Maffulli N., Wong J., Almekinders L.C. Types and epidemiology of tendinopathy. Clin Sports Med 2003, 22:675-692.
2. Pennisi E. Tending tender tendons. Science 2002, 295:1011.
3. Bhandari M., Guyatt G.H., Siddiqui F., Morrow F., Busse J., Leighton R.K., et al. Treatment of acute Achilles tendon ruptures: a systematic overview and metaanalysis. Clin Orthop Relat Res 2002, 400:190-200.
4. Leppilahti J., Puranen J., Orava S. Incidence of Achilles tendon rupture. Acta Orthop Scand 1996, 67:277-279.
5. Butler D.L., Juncosa-Melvin N., Boivin G.P., Galloway M.T., Shearn J.T., Gooch C., et al. Functional tissue engineering for tendon repair: a multidisciplinary strategy using mesenchymal stem cells, bioscaffolds, and mechanical stimulation. J Orthop Res 2008, 26:1-9.
6. Miyashita H., Ochi M., Ikuta Y. Histological and biomechanical observations of the rabbit patellar tendon after removal of its central one-third. Arch Orthop Trauma Surg 1997, 116:454-462.
7. Evans R.B. Managing the injured tendon: current concepts. J Hand Ther 2012, 25:173-189.
8. Yamada N., Okano T., Sakai H., Karikusa F., Sawasaki Y., Sakurai Y. Thermo-responsive polymeric surfaces; control of attachment and detachment of cultured cells. Die Makromolekulare Chemie, Rapid Commun 1990, 11:571-576.
9. Yamato M., Okanoa T. Cell sheet engineering. Mater Today 2004, 7:42-47.
10. L'Heureux N., Dusserre N., Konig G., Victor B., Keire P., Wight T.N., et al. Human tissue-engineered blood vessels for adult arterial revascularization. Nat Med 2006, 12:361-365.
11. Yang J., Yamato M., Shimizu T., Sekine H., Ohashi K., Kanzaki M., et al. Reconstruction of functional tissues with cell sheet engineering. Biomaterials 2007, 28:5033-5043.
12. Wei F., Qu C., Song T., Ding G., Fan Z., Liu D., et al. Vitamin C treatment promotes mesenchymal stem cell sheet formation and tissue regeneration by elevating telomerase activity. J Cell Physiol 2012, 227:3216-3224.
13. Bi Y., Ehirchiou D., Kilts T.M., Inkson C.A., Embree M.C., Sonoyama W., et al. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med 2007, 13:1219-1227.
14. Rui Y.F., Lui P.P.Y., Li G., Fu S.C., Lee Y.W., Chan K.M. Isolation and characterization of multi-potent rat tendon-derived stem cells. Tissue Eng Part A 2010, 16:1549-1558.
15. Rui Y.F., Lui P.P., Ni M., Chan L.S., Lee Y.W., Chan K.M. Mechanical loading increased BMP-2 expression which promoted osteogenic differentiation of tendon-derived stem cells. J Orthop Res 2011, 29:390-396.
16. Tan Q., Lui P.P., Rui Y.F., Wong Y.M. Comparison of potentials of stem cells isolated from tendon and bone marrow for musculoskeletal tissue engineering. Tissue Eng Part A 2012, 18:840-851.
17. Ni M., Lui P.P., Rui Y.F., Lee Y.W., Lee Y.W., Tan Q., et al. Tendon-derived stem cells (TDSCs) promote tendon repair in a rat patellar tendon window defect model. J Orthop Res 2012, 30:613-619.
18. Awad H.A., Boivin G.P., Dressler M.R., Smith F.N., Young R.G., Butler D.L. Repair of patellar tendon injuries using a cell-collagen composite. J Orthop Res 2003, 21:420-431.
19. Harris M.T., Butler D.L., Boivin G.P., Florer J.B., Schantz E.J., Wenstrup R.J. 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.
20. Wang J.F., Olson M.E., Ball D.K., Brigstock D.R., Hart D.A. Recombinant connective tissue growth factor modulates porcine skin fibroblast gene expression. Wound Repair Regen 2003, 11:220-229.
21. Ivkovic S., Yoon B.S., Popoff S.N., Safadi F.F., Libuda D.E., Stephenson R.C., et al. Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 2003, 130:2779-2791.
22. Chen C.H., Cao Y., Wu Y.F., Bais A.J., Gao J.S., Tang J.B. Tendon healing in vivo: gene expression and production of multiple growth factors in early tendon healing period. J Hand Surg Am 2008, 33:1834-1842.
23. Lee C.H., Moioli E.K., Mao J.J. Fibroblastic differentiation of human mesenchymal stem cells using connective tissue growth factor. Conf Proc IEEE Eng Med Biol Soc 2006, 1:775-778.
24. Lee C.H., Shah B., Moioli E.K., Mao J.J. CTGF directs fibroblast differentiation from human mesenchymal stem/stromal cells and defines connective tissue healing in a rodent injury model. J Clin Invest 2010, 120:3340-3349.
25. Stone N., Meister A. Function of ascorbic acid in the conversion of proline to collagen hydroxyproline. Nature 1962, 194:555-557.
26. Nandi D., Patra R.C., Swarup D. Effect of cysteine, methionine, ascorbic acid and thiamine on arsenic-induced oxidative stress and biochemical alterations in rats. Toxicology 2005, 211:26-35.
27. Korkmaz A., Kolankaya D. The protective effects of ascorbic acid against renal ischemia-reperfusion injury in male rats. Ren Fail 2009, 31:36-43.
28. Ji A.R., Ku S.Y., Cho M.S., Kim Y.Y., Kim Y.J., Oh S.K., et al. Reactive oxygen species enhance differentiation of human embryonic stem cells into mesodermal lineage. Exp Mol Med 2010, 42:175-186.
29. Potdar P.D., D'Souza S.B. Ascorbic acid induces in vitro proliferation of human subcutaneous adipose tissue derived mesenchymal stem cells with upregulation of embryonic stem cell pluripotency markers Oct4 and SOX 2. Hum Cell 2010, 23:152-155.
30. Omeroĝlu S., Peker T., Türközkan N., Omeroĝlu H. High-dose vitamin C supplementation accelerates the Achilles tendon healing in healthy rats. Arch Orthop Trauma Surg 2009, 129:281-286.
31. Lui P.P.Y., Cheuk Y.C., Hung L.K., Fu S.C., Chan K.M. Increased apoptosis at late stage of tendon healing. Wound Repair Regen 2007, 15:702-707.
32. Lui P.P.Y., Fu S.C., Chan L.S., Hung L.K., Chan K.M. Chondrocyte phenotype and ectopic ossification in collagenase-induced tendon degeneration. J Histochem Cytochem 2009, 57:91-100.
33. Langer R., Vacanti J.P. Tissue engineering. Science 1993, 260:920-926.
34. Nishida K., Yamato M., Hayashida Y., Watanabe K., Yamamoto K., Adachi E., et al. Corneal reconstruction with tissueengineered cell sheets composed of autologous oral mucosal epithelium. N Engl J Med 2004, 351:1187-1196.
35. Shimizu T., Sekine H., Yang J., Isoi Y., Yamato M., Kikuchi A., et al. Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. FASEB J 2006, 20:708-710.
36. Ohashi K., Yokoyama T., Yamato M., Kuge H., Kanehiro H., Tsutsumi M., et al. Engineering functional two- and three-dimensional liver systems in vivo using hepatic tissue sheets. Nat Med 2007, 13:880-885.
37. Ding G., Liu Y., Wang W., Wei F., Liu D., Fan Z., et al. Allogeneic periodontal ligament stem cell therapy for periodontitis. Stem Cells 2010, 28:1829-1838.
38. Jelinsky S.A., Archambault J., Li L., Seeherman H. Tendon-selective genes identified from rat and human musculoskeletal tissues. J Orthop Res 2010, 28:289-297.
39. Docheva D., Hunziker E.B., Fassler R., Brandau O. Tenomodulin is necessary for tenocyte proliferation and tendon maturation. Mol Cell Biol 2005, 25:699-705.
40. Schweitzer R., Chyung J.H., Murtaugh L.C., Brent A.E., Rosen V., Olson E.N., et al. Analysis of the tendon cell fate using Scleraxis, a specific marker for tendons and ligaments. Development 2001, 128:3855-3866.
41. Murchison N.D., Price B.A., Conner D.A., Keene D.R., Olson E.N., Tabin C.J., et al. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development 2007, 134:2697-2708.
42. Wang B., Liu W., Zhang Y., Jiang Y., Zhang W.J., Zhou G., et al. Engineering of extensor tendon complex by an ex vivo approach. Biomaterials 2008, 29:2954-2961.
43. Cao D., Liu W., Wei X., Xu F., Cui L., Cao Y. In vitro tendon engineering with avian tenocytes and polyglycolic acids: a preliminary report. Tissue Eng 2006, 12:1369-1377.
44. Saber S., Zhang A.Y., Ki S.H., Lindsey D.P., Smith R.L., Riboh J., et al. Flexor tendon tissue engineering: bioreactor cyclic strain increases construct strength. Tissue Eng Part A 2010, 16:2085-2090.
45. Abousleiman R.I., Reyes Y., McFetridge P., Sikavitsas V. Tendon tissue engineering using cell-seeded umbilical veins cultured in a mechanical stimulator. Tissue Eng Part A 2009, 15:787-795.
46. Ouyang H.W., Goh J.C., Thambyah A., Teoh S.H., Lee E.H. Knitted poly-lactide-co-glycolide scaffold loaded with bone marrow stromal cells in repair and regeneration of rabbit Achilles tendon. Tissue Eng 2003, 9:431-439.
47. Kryger G.S., Chong A.K., Costa M., Pham H., Bates S.J., Chang J. A comparison of tenocytes and mesenchymal stem cells for use in flexor tendon tissue engineering. J Hand Surg Am 2007, 32:597-605.
48. Juncosa-Melvin N., Boivin G.P., Gooch C., Galloway M.T., West J.R., Dunn M.G., et al. The effect of autologous mesenchymal stem cells on the biomechanics and histology of gel-collagen sponge constructs used for rabbit patellar tendon repair. Tissue Eng 2006, 12:369-379.
49. Chong A.K., Ang A.D., Goh J.C., Hui J.H., Lim A.Y., Lee E.H., et al. Bone marrow-derived mesenchymal stem cells influence early tendon-healing in a rabbit Achilles tendon model. J Bone Jt Surg Am 2007, 89:74-81.
50. Hankemeier S., van Griensven M., Ezechieli M., Barkhausen T., Austin M., Jagodzinski M., et al. Tissue engineering of tendons and ligaments by human bone marrow stromal cells in a liquid fibrin matrix in immunodeficient rats: results of a histologic study. Arch Orthop Trauma Surg 2007, 127:815-821.