Determination of optimal cyclic uniaxial stretches for stem cell-to-tenocyte differentiation under a wide range of mechanical stretch conditions by evaluating gene expression and protein synthesis levels

• Autorzy: Morita Y. , Watanabe S. , Ju Y. , Xu B.
• Języki publikacji: EN

Abstrakty

EN

We examined optimal cyclic uniaxial stretches for stem cell-to-tenocyte differentiation by applying a wide range of cyclic mechanical stimuli. Human bone marrow mesenchymal stem cells (hBMSCs) were subjected to three types of cyclic elongation of 5%, 10%, or 15% at a cyclic frequency of 1 Hz for 24 h or 48 h, and differentiation into tenocytes was assessed by two methods: real-time polymerase chain reaction determination of gene expression levels and western blotting analysis of protein expression levels. The gene expression levels of the differentiation markers type I collagen (Col I), type III collagen (Col III), tenascin-C (Tnc), and scleraxis (Scx), all of which are constituents of tendon tissue, were increased when cells were exposed to 10% stretching stimulation. The levels of Col I and Tnc protein synthesis levels were also higher in the cells with 10% stretching stimulation than in those subjected to other stimuli. The results indicated that 10% stretching stimulus was efficient to induce the differentiation of hBMSCs into tenocytes. In addition, the changes in gene and protein expression levels were strongly correlated with cell orientation angle. The results presented here suggest that mesenchymal stem cell-to-tenocyte differentiation is strongly associated with cumulative elongation load on the cells. This work provides novel insights into the differentiation of tenogenesis in a strain-induced environment and supports the therapeutic potential of hBMSCs.

Słowa kluczowe

EN

hBMSC; differentiation; mechanical stretch; tenocyte

PL

różniczkowanie; tenocyte; wydłużanie

• Wydawca: Oficyna Wydawnicza Politechniki Wrocławskiej
• Czasopismo: Acta of Bioengineering and Biomechanics
• Rocznik: 2013
• Tom: Vol. 15, no. 3
• Strony: 71--79
• Opis fizyczny: Bibliogr. 43 poz., rys., tab., wykr.

Twórcy

autor

Morita Y.

• Department of Mechanical Science & Engineering, Graduate School of Engineering, Nagoya University, Japan

autor

Watanabe S.

• Department of Mechanical Science & Engineering, Graduate School of Engineering, Nagoya University, Japan

autor

Ju Y.

• Department of Mechanical Science & Engineering, Graduate School of Engineering, Nagoya University, Japan

autor

Xu B.

• Department of Mechanical Science & Engineering, Graduate School of Engineering, Nagoya University, Japan
• Department of Mechanical Science & Engineering, Graduate School of Engineering, Nagoya University, Japan

Bibliografia

• [1] WOLFMAN N.M., HATTERSLEY G., COX K., CELESTE A.J., NELSON R., YAMAJI N., DUBE J.L., DIBLASIOSMITH E., NOVE J., SONG J.J., WOZNEY J.M., ROSEN V., 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, Vol. 100(2), 321–330.
• [2] WANG J.H.C., Mechanobiology of tendon, J. Biomech., 2006, Vol. 39(9), 1563–1583.
• [3] GOH J.C.H., OUYANG H.W., TEOH S.H., CHAN C.K.C., LEE E.H., Tissue-engineering approach to the repair and regeneration of tendons and ligaments, Tissue Eng., 2003, Vol. 9(1), S31–S44.
• [4] SHARMA P., MAFFULLI N., Biology of tendon injury: healing, modeling and remodeling, J. Musculoskelet. Neuronal. Interact., 2006, Vol. 6(2), 181–190.
• [5] SHARMA P., MAFFULLI N., Current concepts review tendon injury and tendinopathy: Healing and repair, J. Bone Joint Surg. Am., 2005, Vol. 87A(1), 187–202.
• [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. Traum. Su., 1997, Vol. 116(8), 454–462.
• [7] TOHYAMA H., YASUDA K., KITAMURA Y., YAMAMOTO E., HAYASHI K., The changes in mechanical properties of regenerated and residual tissues in the patellar tendon after removal of its central portion, Clin. Biomech., 2003, Vol. 18(8), 765–772.
• [8] CHAN B.P., FU S.C., QIN L., ROLF C., CHAN K.M., Pyridinoline in relation to ultimate stress of the patellar tendon during healing: An animal study, J. Orthop. Res., 1998, Vol. 16(5), 597–603.
• [9] BAGNANINCHI P.O., YANG Y., EL HAJ A.J., MAFFULLI N., Tissue engineering for tendon repair, Brit. J. Sport. Med., 2007, Vol. 41(8), e10.
• [10] BULLOUGH R., FINNIGAN T., KAY A., MAFFULLI N., FORSYTH N.R., Tendon repair through stem cell intervention: Cellular and molecular approaches, Disabil. Rehabil., 2008, Vol. 30(20–22), 1746–1751.
• [11] HAMPSON K., FORSYTH N.R., EL HAJ A., MAFFULLI N., Tendon Tissue Engineering, [in:] N. Ashammakhi, R. Reis, F. Chiellini (eds.), Topics in Tissue Engineering, Vol. 4, Chapter 3, 2008.
• [12] PITTENGER M.F., MACKAY A.M., BECK S.C., JAISWAL R.K., DOUGLAS R., MOSCA J.D., MOORMAN MA., SIMONETTI DW., CRAIG S., MARSHAK DR., Multilineage potential of adult human mesenchymal stem cells, Science, 1999, Vol. 284(5411), 143–147.
• [13] CAPLAN A., BRUDER S.P., Mesenchymal stem cells: Building blocks for molecular medicine in the 21st century, Trends Mol. Med., 2001, Vol. 7(6), 259–264.
• [14] GIOVANNINI S., BREHM W., MAINIL-VARLET P., NESIC D., Multilineage differentiation potential of equine bloodderived fibroblast-like cells, Differentiation, 2008, Vol. 76(2), 118–129.
• [15] AWAD H., BUTLER D.L., BOIVIN G.P., SMITH F.N.L., MALAVIYA P., HUIBREGTSE B., CAPLAN A.I., Autologous mesenchymal stem cell-mediated repair of tendon, Tissue Eng., 1999, Vol. 5(3), 267–277.
• [16] FRIEDENS A.J., PETRAKOV K.V., KUROLESO A.I., FROLOVA G.P., Heterotopic transplants of bone marrow – analysis of precursor cells for osteogenic and hematopoietic tissues, Transplantation, 1968, Vol. 6(2), 230–247.
• [17] 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, Vol. 1, 775–778.
• [18] KOCH H., JADLOWIEC J.A., FU F.H., NONN J., MERK H.R., HOLLINGER J.O., CAMPBELL P.G., The effect of growth/differentiation factor-5 (GDF-5) on genotype and phenotype in human adult mesenchymal stem cells, Z. Orthop. Ihre Grenz., 2004, Vol. 142(2), 248–253.
• [19] PARK A., HOGAN M.V., KESTURU G.S., JAMES R., BALIAN G., CHHABRA A.B., Adipose-derived mesenchymal stem cells treated with growth differentiation factor-5 express tendonspecific markers, Tissue Eng. A, 2010, Vol. 16(9), 2941–2951.
• [20] HADDAD-WEBER M., PRAGER P., KUNZ M., SEEFRIED L., JAKOB F., MURRAY M.M., EVANS C.H., NÖTH U., STEINERT A.F., BMP12 and BMP13 gene transfer induce ligamentogenic differentiation in mesenchymal progenitor and anterior cruciate ligament cells, Cytotherapy, 2010, Vol. 12(4), 505–513.
• [21] ZEICHEN J., VAN GRIENSVEN M., BOSCH U., The proliferative response of isolated human tendon fibroblasts to cyclic biaxial mechanical strain, Am. J. Sport Med., 2000, Vol. 28(6), 888–892.
• [22] TANAKA H., MANSKE P.R., PRUITT D.L., LARSON B.J., Effect of cyclic tension on lacerated flexor tendons in-vitro, J. Hand Surg.-AM., 1995, Vol. 20A(3), 467–473.
• [23] NÖTH U., SCHUPP K., HEYMER A., KALL S., JAKOB F., SCHUTZE N., BAUMANN B., BARTHEL T., EULERT J., HENDRICH C., Anterior cruciate ligament constructs fabricated from human mesenchymal stem cells in a collagen type I hydrogel, Cytotherapy, 2005, Vol. 7(5), 447–455.
• [24] YANG G.G., CRAWFORD R.C., WANG J.H.C., Proliferation and collagen production of human patellar tendon fibroblasts in response to cyclic uniaxial stretching in serum-free conditions, J. Biomech., 2004, Vol. 37(10), 1543–1550.
• [25] ALTMAN G.H., HORAN R.L., MARTIN I., FARHADI J., STARK P.R.H., VOLLOCH V., RICHMOND J.C., VUNJAKNOVAKOVIC G., KAPLAN D.L., Cell differentiation by mechanical stress, Faseb J., 2001, Vol. 16(2), 270–272.
• [26] KUO C.K., TUAN R.S., Mechanoactive tenogenic differentiation of human mesenchymal stem cells, Tissue Eng. A, 2008, Vol. 14(10), 1615–1627.
• [27] ZHANG L., TRAN N., CHEN H.Q., KAHN C.J.F., MARCHAL S., GROUBATCH F., 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., 2008, Vol. 332(1), 101–109.
• [28] CHEN Y.J., HUANG C.H., LEE I.C., LEE Y.T., CHEN M.H., YOUNG T.H., Effects of cyclic mechanical stretching on the mRNA expression of tendon/ligament-related and osteoblastspecific genes in human mesenchymal stem cells, Connect. Tissue Res., 2008, Vol. 49(1), 7–14.
• [29] ZHANG L., KAHN C.J.F., CHEN H.Q., TRAN N., WANG X., Effect of uniaxial stretching on rat bone mesenchymal stem cell: Orientation and expressions of collagen types I and III and tenascin-C, Cell Biol. Int., 2008, Vol. 32(3), 344–352.
• [30] LUI P.P.Y., RUI Y.F., NI M., CHAN K.M., Tenogenic differentiation of stem cells for tendon repair – what is the current evidence?, J. Tissue Eng. Regen. M., 2011, Vol. 5(8), e144–e163.
• [31] EYRE D.R., PAZ M.A., GALLOP P.M., Cross-linking in collagen and elastin, Annu. Rev. Biochem., 1984, Vol. 53, 717–748.
• [32] LEJARD V., BRIDEAU G., BLASIS F., SALINGCARNBORIBOON R., WAGNER G., ROEHRL M.H.A., NODA M., DUPREZ D., HOUILLIER P., ROSSERT J., Scleraxis and NFATc regulate the expression of the pro-alpha1(I) collagen gene in tendon fibroblasts, J. Biol. Chem., 2007, Vol. 282(24), 17665–17675.
• [33] LAPIERE C.M., NUSGENS B., PIERARD G.E., Interaction between collagen type-1 and type-3 in conditioning bundles organization, Connect. Tissue Res., 1977, Vol. 5(1), 21–29.
• [34] ELEFTERIOU F., EXPOSITO J.Y., GARRONE R., LETHIAS C., Binding of tenascin-X to decorin, FEBS Lett., 2001, Vol. 495(1–2), 44–47.
• [35] SONG G., JU Y., SOYAMA H., OHASHI T., SATO M., Regulation of cyclic longitudinal mechanical stretch on proliferation of human bone marrow mesenchymal stem cells, Mol. Cell. Biomech., 2007, Vol. 4(4), 201–210.
• [36] XU B., SONG G., JU Y., Effect of focal adhesion kinase on the regulation of realignment and tenogenic differentiation of human mesenchymal stem cells by mechanical stretch, Connect. Tissue Res., 2011, Vol. 52(5), 373–379.
• [37] XU B., SONG G., JU Y., LI X., SONG Y., WATANABE S., RhoA/ROCK, cytoskeletal dynamics, and focal adhesion kinase are required for mechanical stretch-induced tenogenic differentiation of human mesenchymal stem cells, J. Cell Physiol., 2012, Vol. 227(6), 2722–2729.
• [38] LEE I.C., WANG J.H., LEE Y.T., YOUNG T.H., The differentiation of mesenchymal stem cells by mechanical stress or/and co-culture system, Biochem. Bioph. Res. Co., 2007, Vol. 352(1), 147–152.
• [39] COSTA K.D., HUCKER W.J., YIN F.C.P., Buckling of actin stress fibers: A new wrinkle in the cytoskeletal tapestry, Cell Motil. Cytoskel., 2002, Vol. 52(4), 266–274.
• [40] NEIDLINGER-WILKE C., GROOD E.S., WANG J.H.C., BRAND R.A., CLAES L., Cell alignment is induced by cyclic changes in cell length: studies of cells grown in cyclically stretched substrates, J. Orthop. Res., 2001, Vol. 19(2), 286–293.
• [41] WANG H.C., IP W., BOISSY R., GROOD E.S., Cell orientation response to cyclically deformed substrates: Experimental validation of a cell model, J. Biomech., 1995, Vol. 28(12), 1543–1552.
• [42] MORITA Y., MUKAI T., JU Y., WATANABE S., Evaluation of stem cell-to-tenocyte differentiation using atomic force microscopy to measure cellular elastic moduli, Cell Biochem. Biophys., 2013, Vol. 66(1), 73–80.
• [43] KOIKE M., SHIMOKAWA H., KANNO Z., OHYA K., SOMA K., Effects of mechanical strain on proliferation and differentiation of bone marrow stromal cell line ST2, J. Bone Miner. Metab., 2005, Vol. 23(3), 219–225. Department of Mechanical Science & Engineering, Graduate School of Engineering, Nagoya University, Japan