Synthesis of embryonic tendon-like tissue by human marrow stromal/mesenchymal stem cells requires a three-dimensional environment and transforming growth factor β3

Matrix Biology

Volumn 29, Issue 8, 2010, Pages 668-677

  Kapacee, Zoher ^a   Yeung, Ching Yan Chloé ^a   Lu, Yinhui ^a   Crabtree, David ^a   Holmes, David F ^a   Kadler, Karl E ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Collagen; Differentiation; Fibrin; Forces; Signaling

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; ACTIN; COLLAGEN FIBRIL; COLLAGEN TYPE 1; FIBRIN; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA3;

ARTICLE; BONE MARROW CELL; CELL MEMBRANE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; EMBRYONAL TISSUE; GENE CONTROL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MESENCHYMAL STEM CELL; MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; STROMA CELL; TENDON; TISSUE ENGINEERING; UPREGULATION; WESTERN BLOTTING;

ADIPOCYTES; ADULT; ANTIGENS, CD; BONE MARROW CELLS; CELL DIFFERENTIATION; CHONDROCYTES; COLLAGEN TYPE I; EXTRACELLULAR MATRIX; FIBRILLAR COLLAGENS; FIBRIN; FIBRINOGEN; GELS; GENE EXPRESSION; HUMANS; INTEGRIN BETA CHAINS; MESENCHYMAL STEM CELLS; MONOCYTE-MACROPHAGE PRECURSOR CELLS; OSTEOBLASTS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; STROMAL CELLS; TENDONS; THROMBIN; TRANSFORMING GROWTH FACTOR BETA3; YOUNG ADULT;

EID: 78649448105     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2010.08.005     Document Type: Article

References (60)

1. Aluwihare P., Mu Z., Zhao Z., Yu D., Weinreb P.H., Horan G.S., Violette S.M., Munger J.S. Mice that lack activity of alphavbeta6- and alphavbeta8-integrins reproduce the abnormalities of Tgfb1- and Tgfb3-null mice. J. Cell Sci. 2009, 122:227-232.
2. Amarnath S., Dong L., Li J., Wu Y., Chen W. Endogenous TGF-beta activation by reactive oxygen species is key to Foxp3 induction in TCR-stimulated and HIV-1-infected human CD4+CD25- T cells. Retrovirology 2007, 4:57.
3. Annes J.P., Chen Y., Munger J.S., Rifkin D.B. Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J. Cell Biol. 2004, 165:723-734.
4. Annes J.P., Munger J.S., Rifkin D.B. Making sense of latent TGFbeta activation. J. Cell Sci. 2003, 116:217-224.
5. Asou Y., Nifuji A., Tsuji K., Shinomiya K., Olson E.N., Koopman P., Noda M. Coordinated expression of scleraxis and Sox9 genes during embryonic development of tendons and cartilage. J. Orthop. Res. 2002, 20:827-833.
6. Attisano L., Wrana J.L. Signal transduction by the TGF-beta superfamily. Science 2002, 296:1646-1647.
7. Baker S.M., Sugars R.V., Wendel M., Smith A.J., Waddington R.J., Cooper P.R., Sloan A.J. TGF-beta/extracellular matrix interactions in dentin matrix: a role in regulating sequestration and protection of bioactivity. Calcif. Tissue Int. 2009, 85:66-74.
8. 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., Young M.F. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat. Med. 2007, 13:1219-1227.
9. Birk D.E., Trelstad R.L. Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation. J. Cell Biol. 1986, 103:231-240.
10. Butler D.L., Juncosa-Melvin N., Boivin G.P., Galloway M.T., Shearn J.T., Gooch C., Awad H. Functional tissue engineering for tendon repair: a multidisciplinary strategy using mesenchymal stem cells, bioscaffolds, and mechanical stimulation. J. Orthop. Res. 2008, 26:1-9.
11. Canty E.G., Lu Y., Meadows R.S., Shaw M.K., Holmes D.F., Kadler K.E. Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon. J. Cell Biol. 2004, 165:553-563.
12. Caplan A.I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell. Physiol. 2007, 213:341-347.
13. Chang H., Brown C.W., Matzuk M.M. Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr. Rev. 2002, 23:787-823.
14. Chen X., Song X.-H., Yin Z., Zou X.-H., Wang L.-L., Hu H., Cao T., Zheng M., Ouyang H.W. Stepwise differentiation of human embryonic stem cells promotes tendon regeneration by secreting fetal tendon matrix and differentiation factors. Stem Cells 2009, 27:1276-1287.
15. Colter D.C., Sekiya I., Prockop D.J. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc. Natl Acad. Sci. USA 2001, 98:7841-7845.
16. Crawford S.E., Stellmach V., Murphy-Ullrich J.E., Ribeiro S.M., Lawler J., Hynes R.O., Boivin G.P., Bouck N. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 1998, 93:1159-1170.
17. Cserjesi P., Brown D., Ligon K.L., Lyons G.E., Copeland N.G., Gilbert D.J., Jenkins N.A., Olson E.N. Scleraxis: a basic helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development 1995, 121:1099-1110.
18. de Caestecker M. The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev. 2004, 15:1-11.
19. de Mos M., Joosten L.A., Oppers-Walgreen B., van Schie J.T., Jahr H., van Osch G.J., Verhaar J.A. Tendon degeneration is not mediated by regulation of Toll-like receptors 2 and 4 in human tenocytes. J. Orthop. Res. 2009, 27:1043-1047.
20. Droguett R., Cabello-Verrugio C., Santander C., Brandan E. TGF-beta receptors, in a Smad-independent manner, are required for terminal skeletal muscle differentiation. Exp. Cell Res. 2009, 316:2487-2503.
21. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
22. Friedenstein A.J., Chailakhjan R.K., Lalykina K.S. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 1970, 3:393-403.
23. Ge G., Greenspan D.S. BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein. J. Cell Biol. 2006, 175:111-120.
24. Hargus G., Kist R., Kramer J., Gerstel D., Neitz A., Scherer G., Rohwedel J. Loss of Sox9 function results in defective chondrocyte differentiation of mouse embryonic stem cells in vitro. Int. J. Dev. Biol. 2008, 52:323-332.
25. Hecker L., Baar K., Dennis R.G., Bitar K.N. Development of a three-dimensional physiological model of the internal anal sphincter bioengineered in vitro from isolated smooth muscle cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289:G188-G196.
26. Hinz B., Celetta G., Tomasek J.J., Gabbiani G., Chaponnier C. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol. Biol. Cell 2001, 12:2730-2741.
27. Huang Y.C., Dennis R.G., Baar K. Cultured slow vs. fast skeletal muscle cells differ in physiology and responsiveness to stimulation. Am. J. Physiol. Cell Physiol. 2006, 291:C11-C17.
28. Huang Y.C., Dennis R.G., Larkin L., Baar K. Rapid formation of functional muscle in vitro using fibrin gels. J. Appl. Physiol. 2005, 98:706-713.
29. Huang Y.C., Khait L., Birla R.K. Contractile three-dimensional bioengineered heart muscle for myocardial regeneration. J. Biomed. Mater. Res. A 2007, 80:719-731.
30. Inman G.J., Nicolas F.J., Callahan J.F., Harling J.D., Gaster L.M., Reith A.D., Laping N.J., Hill C.S. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 2002, 62:65-74.
31. Kapacee Z., Richardson S.H., Lu Y., Starborg T., Holmes D.F., Baar K., Kadler K.E. Tension is required for fibripositor formation. Matrix Biol. 2008, 27:371-375.
32. Kitano Y., Radu A., Shaaban A., Flake A.W. Selection, enrichment, and culture expansion of murine mesenchymal progenitor cells by retroviral transduction of cycling adherent bone marrow cells. Exp. Hematol. 2000, 28:1460-1469.
33. Kuo C.K., Petersen B.C., Tuan R.S. Spatiotemporal protein distribution of TGF-betas, their receptors, and extracellular matrix molecules during embryonic tendon development. Dev. Dyn. 2008, 237:1477-1489.
34. Lapsys N.M., Kriketos A.D., Lim-Fraser M., Poynten A.M., Lowy A., Furler S.M., Chisholm D.J., Cooney G.J. Expression of genes involved in lipid metabolism correlate with peroxisome proliferator-activated receptor gamma expression in human skeletal muscle. J. Clin. Endocrinol. Metab. 2000, 85:4293-4297.
35. Liu Y., Cserjesi P., Nifuji A., Olson E.N., Noda M. Sclerotome-related helix-loop-helix type transcription factor (scleraxis) mRNA is expressed in osteoblasts and its level is enhanced by type-beta transforming growth factor. J. Endocrinol. 1996, 151:491-499.
36. Liu Y., Watanabe H., Nifuji A., Yamada Y., Olson E.N., Noda M. Overexpression of a single helix-loop-helix-type transcription factor, scleraxis, enhances aggrecan gene expression in osteoblastic osteosarcoma ROS17/2.8 cells. J. Biol. Chem. 1997, 272:29880-29885.
37. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
38. Mackley J.R., Ando J., Herzyk P., Winder S.J. Phenotypic responses to mechanical stress in fibroblasts from tendon, cornea and skin. Biochem. J. 2006, 396:307-316.
39. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19:2783-2810.
40. Mu D., Cambier S., Fjellbirkeland L., Baron J.L., Munger J.S., Kawakatsu H., Sheppard D., Broaddus V.C., Nishimura S.L. The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J. Cell Biol. 2002, 157:493-507.
41. Munger J.S., Huang X., Kawakatsu H., Griffiths M.J., Dalton S.L., Wu J., Pittet J.F., Kaminski N., Garat C., Matthay M.A., Rifkin D.B., Sheppard D. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 1999, 96:319-328.
42. Murdoch A.D., Grady L.M., Ablett M.P., Katopodi T., Meadows R.S., Hardingham T.E. Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: generation of scaffold-free cartilage. Stem Cells 2007, 25:2786-2796.
43. Nunes I., Gleizes P.E., Metz C.N., Rifkin D.B. Latent transforming growth factor-beta binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-beta. J. Cell Biol. 1997, 136:1151-1163.
44. Ogawa K., Ito M., Takeuchi K., Nakada A., Heishi M., Suto H., Mitsuishi K., Sugita Y., Ogawa H., Ra C. Tenascin-C is upregulated in the skin lesions of patients with atopic dermatitis. J. Dermatol. Sci. 2005, 40:35-41.
45. Owen T.A., Aronow M., Shalhoub V., Barone L.M., Wilming L., Tassinari M.S., Kennedy M.B., Pockwinse S., Lian J.B., Stein G.S. Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J. Cell. Physiol. 1990, 143:420-430.
46. Phinney D.G., Prockop D.J. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 2007, 25:2896-2902.
47. Popova A.P., Bozyk P.D., Goldsmith A.M., Linn M.J., Lei J., Bentley J.K., Hershenson M.B. Autocrine production of TGF-beta1 promotes myofibroblastic differentiation of neonatal lung mesenchymal stem cells. Am J Physiol Lung Cell Mol Physiol. 2010, 298:L735-743.
48. Pryce B.A., Brent A.E., Murchison N.D., Tabin C.J., Schweitzer R. Generation of transgenic tendon reporters, ScxGFP and ScxAP, using regulatory elements of the scleraxis gene. Dev. Dyn. 2007, 236:1677-1682.
49. Rifkin D.B. Latent transforming growth factor-beta (TGF-beta) binding proteins: orchestrators of TGF-beta availability. J. Biol. Chem. 2005, 280:7409-7412.
50. Saharinen J., Keski-Oja J. Specific sequence motif of 8-Cys repeats of TGF-beta binding proteins, LTBPs, creates a hydrophobic interaction surface for binding of small latent TGF-beta. Mol. Biol. Cell 2000, 11:2691-2704.
51. Salingcarnboriboon R., Yoshitake H., Tsuji K., Obinata M., Amagasa T., Nifuji A., Noda M. Establishment of tendon-derived cell lines exhibiting pluripotent mesenchymal stem cell-like property. Exp. Cell Res. 2003, 287:289-300.
52. Schoen D.C. Injuries of the wrist. Orthop. Nurs. 2005, 24:304-307.
53. Schulze-Tanzil G., Mobasheri A., Clegg P.D., Sendzik J., John T., Shakibaei M. Cultivation of human tenocytes in high-density culture. Histochem. Cell Biol. 2004, 122:219-228.
54. Schweitzer R., Chyung J.H., Murtaugh L.C., Brent A.E., Rosen V., Olson E.N., Lassar A., Tabin C.J. Analysis of the tendon cell fate using scleraxis, a specific marker for tendons and ligaments. Development 2001, 128:3855-3866.
55. Stewart A., Guan H., Yang K. BMP-3 promotes mesenchymal stem cell proliferation through the TGF-beta/activin signaling pathway. J Cell Physiol. 2010, 223:658-666.
56. Wipff P.J., Rifkin D.B., Meister J.J., Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J. Cell Biol. 2007, 179:1311-1323.
57. Wolf K., Mazo I., Leung H., Engelke K., von Andrian U.H., Deryugina E.I., Strongin A.Y., Brocker E.B., Friedl P. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 2003, 160:267-277.
58. Wong J.K., Lui Y.H., Kapacee Z., Kadler K.E., Ferguson M.W., McGrouther D.A. The cellular biology of flexor tendon adhesion formation: an old problem in a new paradigm. Am. J. Pathol. 2009, 175:1938-1951.
59. Xu J., Attisano L. Mutations in the tumor suppressors Smad2 and Smad4 inactivate transforming growth factor beta signaling by targeting Smads to the ubiquitin-proteasome pathway. Proc. Natl Acad. Sci. USA 2000, 97:4820-4825.
60. Yamagiwa H., Endo N., Tokunaga K., Hayami T., Hatano H., Takahashi H.E. In vivo bone-forming capacity of human bone marrow-derived stromal cells is stimulated by recombinant human bone morphogenetic protein-2. J. Bone Miner. Metab. 2001, 19:20-28.