Cell and Tissue Research

, Volume 332, Issue 1, pp 101–109 | Cite as

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

  • Lei Zhang
  • Nguyen Tran
  • Huai-Qing Chen
  • Cyril J.-F. Kahn
  • Sophie Marchal
  • Frederique Groubatch
  • Xiong Wang
Regular Article

Abstract

Adult bone-marrow-derived mesenchymal stroma cells (BMSC) seem to be a potential cell source for tissue engineering of the ligament. The objective of this work was to study the time-related changes in mRNA expression and protein levels of collagen types I and III and of tenascin-C in BMSC under co-culture with fibroblasts or under a uniaxial cyclic condition. Rat BMSC harvested from the femur and tibial bone marrow were co-cultured with ligament fibroblasts or stimulated by cyclic 10% uniaxial stretching at 1 Hz. Image analysis showed significant cell loss in stretched BMSC, particularly in the directions close to the stretching direction. However, these BMSC displayed an equivalent growth rate to that of non-stretched cells. Real-time reverse transcription/polymerase chain reaction revealed that the mRNA expression of collagen types I and III and of tenascin-C by BMSC was significantly up-regulated by co-culture and cyclic stretching. Radioimmunoassay results confirmed the effects of these stimulations, showing increases in the level of these proteins. Thus, BMSC might be useful as a cell source for the tissue engineering of ligament.

Keywords

Bone-marrow-derived mesenchymal stroma cells Collagen Tenascin-C Co-culture Uniaxial stretching Tissue engineering Ligament Rat (Wistar, male) 

References

  1. Awad HA, Butler DL, Boivin GP, Smith FN, Malaviya P, Huibregtse B, Caplan AI (1999) Autologous mesenchymal stem cell-mediated repair of tendon. Tissue Eng 5:267–277PubMedCrossRefGoogle Scholar
  2. Ball SG, Shuttleworth AC, Kielty CM (2004) Direct cell contact influences bone marrow mesenchymal stem cell fate. Int J Biochem Cell Biol 36:714–727PubMedCrossRefGoogle Scholar
  3. Beeres SL, Bax JJ, Kaandorp TA, Zeppenfeld K, Lamb HJ, Dibbets-Schneider P, Stokkel MP, Fibbe WE, Roos A de, Wall EE van der, Schalij MJ, Atsma DE (2006) Usefulness of intramyocardial injection of autologous bone marrow-derived mononuclear cells in patients with severe angina pectoris and stress-induced myocardial ischemia. Am J Cardiol 97:1326–1331PubMedCrossRefGoogle Scholar
  4. Chiba M, Mitani H (2004) Cytoskeletal changes and the system of regulation of alkaline phosphatase activity in human periodontal ligament cells induced by mechanical stress. Cell Biochem Funct 22:249–256PubMedCrossRefGoogle Scholar
  5. Chiquet M (1999) Regulation of extracellular matrix gene expression by mechanical stress. Matrix Biol 18:417–426PubMedCrossRefGoogle Scholar
  6. Chiquet-Ehrismann R, Tucker RP (2004) Connective tissues: signalling by tenascins. Int J Biochem Cell Biol 36:1085–1089PubMedCrossRefGoogle Scholar
  7. Cho KH, Kim JS, Kwon SU, Cho AH, Kang DW (2005) Significance of susceptibility vessel sign on T2*-weighted gradient echo imaging for identification of stroke subtypes. Stroke 36:2379–2383PubMedCrossRefGoogle Scholar
  8. Cilli F, Khan M, Fu F, Wang JH (2004) Prostaglandin E2 affects proliferation and collagen synthesis by human patellar tendon fibroblasts. Clin J Sport Med 14:232–236PubMedCrossRefGoogle Scholar
  9. Fink C, Ergun S, Kralisch D, Remmers U, Weil J, Eschenhagen T (2000) Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J 14:669–679PubMedGoogle Scholar
  10. Hairfield-Stein M, England C, Paek HJ, Gilbraith KB, Dennis R, Boland E, Kosnik P (2007) Development of self-assembled, tissue-engineered ligament from bone marrow stromal cells. Tissue Eng 13:703–710PubMedCrossRefGoogle Scholar
  11. Hayakawa K, Sato N, Obinata T (2001) Dynamic reorientation of cultured cells and stress fibers under mechanical stress from periodic stretching. Exp Cell Res 268:104–114PubMedCrossRefGoogle Scholar
  12. Heckmann L, Schlenker HJ, Fiedler J, Brenner R, Dauner M, Bergenthal G, Mattes T, Claes L, Ignatius A (2007) Human mesenchymal progenitor cell responses to a novel textured poly(L-lactide) scaffold for ligament tissue engineering. J Biomed Mater Res [B] Appl Biomater 81:82–90CrossRefGoogle Scholar
  13. Iwasaki H, Yoshimoto T, Sugiyama T, Hirata Y (2003) Activation of cell adhesion kinase beta by mechanical stretch in vascular smooth muscle cells. Endocrinology 144:2304–2310PubMedCrossRefGoogle Scholar
  14. Jarvinen TA, Jozsa L, Kannus P, Jarvinen TL, Kvist M, Hurme T, Isola J, Kalimo H, Jarvinen M (1999) Mechanical loading regulates tenascin-C expression in the osteotendinous junction. J Cell Sci 112:3157–3166PubMedGoogle Scholar
  15. Kjaer M (2004) Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84:649–698PubMedCrossRefGoogle Scholar
  16. Ku CH, Johnson PH, Batten P, Sarathchandra P, Chambers RC, Taylor PM, Yacoub MH, Chester AH (2006) Collagen synthesis by mesenchymal stem cells and aortic valve interstitial cells in response to mechanical stretch. Cardiovasc Res 71:548–556PubMedCrossRefGoogle Scholar
  17. Lavaud S, Poirier B, Mandet C, Belair MF, Irinopoulou T, Heudes D, Bazin R, Bariety J, Myara I, Chevalier J (2001) Inflammation is probably not a prerequisite for renal interstitial fibrosis in normoglycemic obese rats. Am J Physiol Renal Physiol 280:F683–F694PubMedGoogle Scholar
  18. Lee IC, Wang JH, Lee YT, Young TH (2007) The differentiation of mesenchymal stem cells by mechanical stress or/and co-culture system. Biochem Biophys Res Commun 352:147–152PubMedCrossRefGoogle Scholar
  19. McAdams RM, Mustafa SB, Shenberger JS, Dixon PS, Henson BM, DiGeronimo RJ (2006) Cyclic stretch attenuates effects of hyperoxia on cell proliferation and viability in human alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 291:L166–L174PubMedCrossRefGoogle Scholar
  20. Neidlinger-Wilke C, Grood ES, Wang J-C, Brand RA, Claes L (2001) Cell alignment is induced by cyclic changes in cell length: studies of cells grown in cyclically stretched substrates. J Orthop Res 19:286–293PubMedCrossRefGoogle Scholar
  21. Noth U, Schupp K, Heymer A, Kall S, Jakob F, Schutze N, Baumann B, Barthel T, Eulert J, Hendrich C (2005) Anterior cruciate ligament constructs fabricated from human mesenchymal stem cells in a collagen type I hydrogel. Cytotherapy 7:447–455PubMedCrossRefGoogle Scholar
  22. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147PubMedCrossRefGoogle Scholar
  23. Sarasa-Renedo A, Chiquet M (2005) Mechanical signals regulating extracellular matrix gene expression in fibroblasts. Scand J Med Sci Sports 15:223–230PubMedCrossRefGoogle Scholar
  24. Shen J, Zhou AQ, Qin YM, Liang Y, Li F (2001) Levels of tenascin mRNA in monocrataline induced pulmonary hypertension in rat [in Chinese]. Chin J Contemp Pediatr 3:519–521Google Scholar
  25. Si Z, Bhardwaj R, Rosch R, Mertens PR, Klosterhalfen B, Klinge U (2002) Impaired balance of type I and type III procollagen mRNA in cultured fibroblasts of patients with incisional hernia. Surgery 131:324–331PubMedCrossRefGoogle Scholar
  26. Tran N, Li Y, Maskali F, Antunes L, Maureira P, Laurens MH, Marie PY, Karcher G, Groubatch F, Stoltz JF, Villemot JP (2006) Short-term heart retention and distribution of intramyocardial delivered mesenchymal cells within necrotic or intact myocardium. Cell Transplant 15:351–358PubMedGoogle Scholar
  27. Waggett AD, Ralphs JR, Kwan AP, Woodnutt D, Benjamin M (1998) Characterization of collagens and proteoglycans at the insertion of the human Achilles tendon. Matrix Biol 16:457–470PubMedCrossRefGoogle Scholar
  28. Wang H, Ip W, Boissy R, Grood ES (1995) Cell orientation response to cyclically deformed substrates: experimental validation of a cell model. J Biomech 28:1543–1552PubMedCrossRefGoogle Scholar
  29. Wang T, Xu Z, Jiang W, Ma A (2006) Cell-to-cell contact induces mesenchymal stem cell to differentiate into cardiomyocyte and smooth muscle cell. Int J Cardiol 109:74–81PubMedCrossRefGoogle Scholar
  30. Watanabe N, Woo SL, Papageorgiou C, Celechovsky C, Takai S (2002) Fate of donor bone marrow cells in medial collateral ligament after simulated autologous transplantation. Microsc Res Tech 58:39–44PubMedCrossRefGoogle Scholar
  31. Yoon YS, Wecker A, Heyd L, Park JS, Tkebuchava T, Kusano K, Hanley A, Scadova H, Qin G, Cha DH, Johnson KL, Aikawa R, Asahara T, Losordo DW (2005) Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J Clin Invest 115:326–338PubMedGoogle Scholar
  32. Young RG, Butler DL, Weber W, Caplan AI, Gordon SL, Fink DJ (1998) Use of mesenchymal stem cells in a collagen matrix for Achilles tendon repair. J Orthop Res 16:406–413PubMedCrossRefGoogle Scholar
  33. Zhang S, Jia Z, Ge J, Gong L, Ma Y, Li T, Guo J, Chen P, Hu Q, Zhang P, Liu Y, Li Z, Ma K, Li L, Zhou C (2005) Purified human bone marrow multipotent mesenchymal stem cells regenerate infarcted myocardium in experimental rats. Cell Transplant 14:787–798PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Lei Zhang
    • 1
    • 2
  • Nguyen Tran
    • 3
  • Huai-Qing Chen
    • 2
  • Cyril J.-F. Kahn
    • 1
  • Sophie Marchal
    • 3
  • Frederique Groubatch
    • 3
  • Xiong Wang
    • 1
  1. 1.LEMTANancy University, CNRSVandoeuvre-les-Nancy CedexFrance
  2. 2.Institute of Biomedical Engineering, West China Medical CenterSichuan UniversityChengduChina
  3. 3.School of Surgery, Faculty of MedicineNancy UniversityVandoeuvre-les-NancyFrance

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