Isolation and characterization of multipotent rat tendon-derived stem cells

Tissue Engineering - Part A

Volumn 16, Issue 5, 2010, Pages 1549-1558

  Rui, Yun Feng ^a,b   Lui, Pauline Po Yee ^a,b   Li, Gang ^a,b   Fu, Sai Chuen ^a,b   Lee, Yuk Wa ^a,b   Chan, Kai Ming ^a,b  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; COLLAGEN; OPTIMIZATION; POLYMER BLENDS; TENDONS;

ADIPOGENIC; CELL DENSITY; CELL-BASED; CHONDROGENIC; CHONDROGENIC MARKERS; COLLAGEN TYPE I; COLLAGENASE DIGESTION; COMMON PROPERTY; FLEXOR TENDON; ISOLATION AND CHARACTERIZATION; MESENCHYMAL STEM CELL; NUCLEATED CELLS; OSTEOGENIC; RAT MODEL; SEEDING DENSITY; SMOOTH MUSCLE ACTINS; SUCCESSFUL ISOLATION; TENASCIN; TENDON TISSUES; TYPE II;

STEM CELLS;

MUS; RATTUS;

BIOLOGICAL MARKER;

ANIMAL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; CELL SHAPE; CHONDROGENESIS; CLONOGENIC ASSAY; CYTOLOGY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL; METABOLISM; METHODOLOGY; MULTIPOTENT STEM CELL; RAT; SPRAGUE DAWLEY RAT; TENDON;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; CELL SHAPE; CHONDROGENESIS; COLONY-FORMING UNITS ASSAY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELLS; MULTIPOTENT STEM CELLS; RATS; RATS, SPRAGUE-DAWLEY; TENDONS;

EID: 77953856072     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0529     Document Type: Article

References (43)

1. Friedenstein, A.J. Precursor cells of mechanocytes. Int Rev Cytol 47, 327, 1976.
2. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., and Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
3. Prockop, D.J. Marrow stromal cells as stem cells for non-hematopoietic tissues. Science 276, 71, 1997.
4. De Bari, C., Dell'Accio, F., Tylzanowski, P., and Luyten, F.P. Multipotent mesenchymal stem cells from adult human sy-novial membrane. Arthritis Rheum 44, 1928, 2001.
5. De Bari, C., Dell'Accio, F., and Luyten, F.P. Human periosteum-derived cells maintain phenotypic stability and chon-drogenic potential throughout expansion regardless of donor age. Arthritis Rheum 44, 85, 2001.
6. Cao, B., Zheng, B., Jankowski, R.J., Kimura, S., Ikezawa, M., Deasy, B., Cummins, J., Epperly, M., Qu-Petersen, Z., and Huard, J. Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol 5, 640, 2003.
7. Zuk, P.A., Zhu, M., Ashjian, P., De Ugarte, D.A., Huang, J.I., Mizuno, H., Alfonso, Z.C., Fraser, J.K., Benhaim, P., and Hedrick, M.H. Human adipose tissue is a source of multi-potent stem cells. Mol Biol Cell 13, 4279, 2002.
8. Barbero, A., Ploegert, S., Heberer, M., and Martin, I. Plasticity of clonal populations of dedifferentiated adult human articular chondrocytes. Arthritis Rheum 48, 1315, 2003.
9. Salingcarnboriboon, R., Yoshitake, H., Tsuji, K., Obinata, M., Amagasa, T., Nifuji, A., and Noda, M. Establishment of tendon-derived cell lines exhibiting pluripotent mesenchy-mal stem cell-like property. Exp Cell Res 287, 289, 2003.
10. de Mos, M., Koevoet, W.J., Jahr, H., Verstegen, M.M., Heij-boer, M.P., Kops, N., van Leeuwen, J.P., Weinans, H., Ver-haar, J.A., and van Osch, G.J. Intrinsic differentiation potential of adolescent human tendon tissue: an in-vitro cell differentiation study. BMC Musculoskelet Disord 8, 16, 2007.
11. Bi, Y., Ehirchiou, D., Kilts, T.M., Inkson, C.A., Embree, M.C., Sonoyama, W., Li, L., Leet, A.I., Seo, B.M., Zhang, L., Shi, S., and Young, M.F. Identification of tendon stem=progenitor cells and the role of the extracellular matrix in their niche. Nat Med 13, 1219, 2007.
12. Martinez-Lorenzo, M.J., Royo-Canas, M., Alegre-Aguaron, E., Desportes, P., Castiella, T., Garcia-Alvarez, F., and Lar-rad, L. Phenotype and chondrogenic differentiation of mes-enchymal cells from adipose tissue of different species. J Orthop Res 27, 1499, 2009.
13. Peister, A., Mellad, J.A., Larson, B.L., Hall, B.M., Gibson, L.F., and Prockop, D.J. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103, 1662, 2004.
14. Yoshimura, H., Muneta, T., Nimura, A., Yokoyama, A., Koga, H., and Sekiya, I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res 327, 449, 2007.
15. Sekiya, I., Larson, B.L., Smith, J.R., Pochampally, R., Cui, J.G., and Prockop, D.J. Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 20, 530, 2002.
16. Simmons, D.J., Seitz, P., Kidder, L., Klein, G.L., Waeltz, M., Gundberg, C.M., Tabuchi, C., Yang, C., and Zhang, R.W. Partial characterization of rat marrow stromal cells. Calcif Tissue Int 48, 326, 1991.
17. Aubin, J.E. Osteoprogenitor cell frequency inrat bone marrow stromal populations: role for heterotypic cell-cell interactions in osteoblast differentiation. J Cell Biochem 72, 396, 1999.
18. Dobson, K.R., Reading, L., Haberey, M., Marine, X., and Scutt, A. Centrifugal isolation of bone marrow from bone: an improved method for the recovery and quantitation of bone marrow osteoprogenitor cells from rat tibiae and femurae. Calcif Tissue Int 65, 411, 1999.
19. Javazon, E.H., Colter, D.C., Schwarz, E.J., and Prockop, D.J. Rat marrow stromal cells are more sensitive to plating density and expand more rapidly from single-cell-derived colonies than human marrow stromal cells. Stem Cells 19, 219, 2001.
20. Corps, A.N., Robinson, A.H.N., Movin, T., Costa, M.L., Hazleman, B.L., and Riley, G.P. Increased expression of aggrecan and biglycan mRNA in Achilles tendinopathy. Rheumatology 45, 291, 2006.
21. Chard, M.D., Cawston, T.E., Riley, G.P., Gresham, G.A., and Hazleman, B.L. Rotator cuff degeneration and lateral epi-condylitis\a comparative histological study. Ann Rheum Dis 53, 30, 1994.
22. Archer, R.S., Bayley, J.I.L., Archer, C.W., and Ali, S.Y. Cell and matrix changes associated with pathological calcification of the human rotator cuff tendons. J Anat 182, 1, 1993.
23. Uhthoff, H.K., Sarkar, K., and Maynard, J.A. Calcifying tendinitis: a new concept of its pathogenesis. Clin Orthop Relat Res 118, 164, 1976.
24. Lui, P.P.Y., Chan, L.S., Cheuk, Y.C., Lee, Y.W., and Chan, K.M. Expression of bone morphogenetic protein-2 in the chondrogenic and ossifying sites of calcific tendinopathy and traumatic tendon injury rat models. J Orthop Surg Res 21, 27, 2009.
25. Speer, M.Y., Yang, H.Y., Brabb, T., Leaf, E., Look, A., Lin, W.L., Frutkin, A., Dichek, D., and Giachelli, C.M. Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ Res 104, 733, 2009.
26. Kim, S.Y., Choi, H.Y., Myung, K.B., and Choi, Y.W. The expression of molecular mediators in the idiopathic cutaneous calcification and ossification. J Cutan Pathol 35, 826, 2008.
27. Lounev, V.Y., Ramachandran, R., Wosczyna, M.N. Yamamoto, M., Maidment, A.D., Shore, E.M., Glaser, D.L., Gold-hamer, D.J., and Kaplan, F.S. Identification of progenitor cells that contribute to heterotopic skeletogenesis. J Bone Joint Surg Am 91, 652, 2009.
28. Warden, S.J. Animal models for the study of tendinopathy. Br J Sports Med 41, 232, 2007.
29. Lui, P.P.Y., Cheuk, Y.C., Hung, L.K., Fu, S.C., and Chan, K.M. Increased apoptosis at the late stage of tendon healing. Wound Repair Regen 15, 702, 2007.
30. Lui, P.P., Fu, S.C., Chan, L.S., Hung, L.K., and Chan, K.M. Chondrocyte phenotype and ectopic ossification in collagenase-induced tendon degeneration. J Histochem Cytochem 57, 91, 2009.
31. Fu, S.C., Cheuk, Y.C., Chan, K.M., Hung, L.K., and Wong, M.W. Is cultured tendon fibroblast a good model to study tendon healing? J Orthop Res 26, 374, 2008.
32. Sakaguchi, Y., Sekiya, I., Yagishita, K., and Muneta, T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 52, 2521, 2005.
33. Wong, M.W., Qin, L., Tai, J.K., Lee, S.K., Leung, K.S., and Chan, K.M. Engineered allogeneic chondrocyte pellet for reconstruction of fibrocartilage zone at bone-tendon junction\a preliminary histological observation. J Biomed Mater Res B Appl Biomater 70, 362, 2004.
34. Lui, P.P.Y., Chan, L.S., Lee, Y.W., Fu, S.C., and Chan, K.M. Sustained expression of proteoglycans and collagen type III=type I ratio in a calcified tendinopathy model. Rheumatology. (Oxford) 49, 231, 2010.
35. Lui, P.P.Y., Chan, L.S., Fu, S.C., and Chan, K.M. Expression of sensory neuropeptides in tendon is associated with failed healing and activity-related tendon pain in collagenase-induced tendon injury. Am J Sports Med, in press.
36. Colter, D.C., Class, R., DiGirolamo, C.M., and Prockop, D.J. Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci USA 97, 3213, 2000.
37. Dezawa, M., Ishikawa, H., Itokazu, Y., Yoshihara, T., Hos-hino, M., Takeda, S., Ide, C., and Nabeshima, Y. Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science 309, 314, 2005.
38. Shukunami, C., Takimoto, A., Oro, M., and Hiraki, Y. Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev Biol 298, 234, 2006.
39. Petrigliano, F.A., English, C.S., Barba, D., Esmende, S., Wu, B.M., and McAllister, D.R. The effects of local bFGF release and uniaxial strain on cellular adaptation and gene expression in a 3D environment: implications for ligament tissue engineering. Tissue Eng 13, 2721, 2007.
40. Omae, H., Zhao, C., Sun, Y.L., An, K.N., and Amadio, P.C. Multilayer tendon slices seeded with bone marrow stromal cells: a novel composite for tendon engineering. J Orthop Res 27, 937, 2009.
41. Zhang, L., Tran, N., Chen, H.Q., Kahn, C.J., Marchal, S., Groubatch, F., and Wang, X. Time-related changes in expression of collagen types I and III and of tenascin-C in rat bone mesenchymal stem cells under co-culture with ligament fibroblasts or uniaxial stretching. Cell Tissue Res 332, 101, 2008.
42. Archambault, J.M., Jelinsky, S.A., Lake, S.P., Hill, A.A., Glaser, D.L., and Soslowsky, L.J. Rat supraspinatus tendon expresses cartilage markers with overuse. J Orthop Res 25, 617, 2007.
43. Clegg, P.D., Strassburg, S., and Smith, R.K. Cell phenotypic variation in normal and damaged tendons. Int J Exp Pathol 88, 227, 2007.