Skip to main content

Advertisement

Log in

Shear stress magnitude is critical in regulating the differentiation of mesenchymal stem cells even with endothelial growth medium

  • Original Research Paper
  • Published:
Biotechnology Letters Aims and scope Submit manuscript

Abstract

Human mesenchymal stem cells (MSC) were seeded onto the inner surface of a tubular silicon construct and, after 24 h, were exposed to a shearing stress of either 2.5 or 10 dyne/cm2 for 1 day. The fluid contained endothelial growth factors in both cases. Morphological changes and cytoskeletal rearrangements were observed in the stimulated cells. Immunofluorescence staining showed that low (2.5 dyne/cm2) and high shear stress (10 dyne/cm2) resulted in the expression of von Willebrand factor (vWF) and calponin, respectively. At low shear stress, CD31 (PECAM-1) was significantly expressed whereas vWF and KDR expression was only slightly higher than those under 10 dyne/cm2. All three markers related to smooth muscle cells (myocardin, myosin heavy chain, and SM‐22α) had significantly higher expression under shear stress of 10 dyne/cm2 compared with a 2.5 dyne/cm2, even in endothelial growth medium. Shear stress plays a critical role in regulating MSC differentiation and must be considered for bioengineered blood vessels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alsberg E, von Recum HA, Mahoney MJ (2006) Environmental cues to guide stem cell fate decision for tissue engineering applications. Expert Opin Biol Ther 6:847–866

    Article  PubMed  CAS  Google Scholar 

  • Bai K, Huang Y, Jia X, Fan Y, Wang W (2010) Endothelium oriented differentiation of bone marrow mesenchymal stem cells under chemical and mechanical stimulations. J Biomech 43:1176–1181

    Article  PubMed  Google Scholar 

  • Ball SG, Shuttleworth AC, Kielty CM (2004) Direct cell contact influences bone marrow mesenchymal stem cell fate. Int J Biochem Cell Biol 36:714–727

    Article  PubMed  CAS  Google Scholar 

  • Davani S, Marandin A, Mersin N, Royer B, Kantelip B, Hervé P, Etievent JP, Kantelip JP (2003) Mesenchymal progenitor cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a rat cellular cardiomyoplasty model. Circulation 108:253–258

    Article  Google Scholar 

  • Dong JD, Gu YQ, Li CM, Wang CR, Feng ZG, Qiu RX, Chen B, Li JX, Zhang SW, Wang ZG, Zhang J (2009) Response of mesenchymal stem cells to shear stress in tissue-engineered vascular grafts. Acta Pharmacol Sin 30:530–536

    Article  PubMed  CAS  Google Scholar 

  • Elhadj S, Akers RM, Forsten-Williams K (2003) Chronic pulsatile shear stress alters insulin-like growth factor-I (IGF-I) binding protein release in vitro. Ann Biomed Eng 31:163–170

    Article  PubMed  Google Scholar 

  • Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 25:677–689

    Article  Google Scholar 

  • Fischer LJ, McIlhenny S, Tulenko T, Golesorkhi N, Zhang P, Larson R, Lombardi J, Shapiro I, DiMuzio PJ (2009) Endothelial differentiation of adipose-derived stem cells: effects of endothelial cell growth supplement and shear force. J Surg Res 152:157–166

    Article  PubMed  CAS  Google Scholar 

  • Ghazanfari S, Tafazzoli-Shadpour M, Shokrgozar MA (2009) Effects of cyclic stretch on proliferation of mesenchymal stem cells and their differentiation to smooth muscle cells. Biochem Biophys Res Commun 23:601–605

    Article  Google Scholar 

  • Haga M, Yamashita A, Paszkowiak J, Sumpio BE, Dardik A (2003) Oscillatory shear stress increases smooth muscle cell proliferation and Akt phosphorylation. J Vasc Surg 37:1277–1284

    Article  PubMed  Google Scholar 

  • Hahn MS, McHale MK, Wang E, Schmedlen RH, West JL (2007) Physiologic pulsatile flow bioreactor conditioning of poly(ethylene glycol)-based tissue engineered vascular grafts. Ann Biomed Eng 35:190–200

    Article  PubMed  Google Scholar 

  • Katritsis D, Kaiktsis L, Chaniotis A, Pantos J, Efstathopoulos EP, Marmarelis V (2007) Wall shear stress: theoretical considerations and methods of measurement. Prog Cardiovasc Di 49:307–329

    Article  Google Scholar 

  • Kim S, von Recum H (2008) Endothelial stem cells and precursors for tissue engineering: cell source, differentiation, selection, and application. Tissue Eng Part B Rev 14:133–147

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi N, Yasu T, Ueba H, Sata M, Hashimoto S, Kuroki M, Saito M, Kawakami M (2004) Mechanical stress promotes the expression of smooth muscle-like properties in marrow stromal cells. Exp Hematol 32:1238–1245

    Article  PubMed  CAS  Google Scholar 

  • Liu SQ, Goldman J (2001) Role of blood shear stress in the regulation of vascular smooth muscle cell migration. IEEE Trans Biomed Eng 48:474–483

    Article  PubMed  CAS  Google Scholar 

  • Matthias PL, Penney MG, Helen MB (2009) Designing materials to direct stem-cell fate. Nature 462:433–441

    Article  Google Scholar 

  • McCann JA, Peterson SD, Plesniak MW, Webster TJ, Haberstroh KM (2005) Non-uniform flow behavior in a parallel plate flow chamber: alters endothelial cell responses. Ann Biomed Eng 33:328–336

    Article  PubMed  Google Scholar 

  • Meinel L, Karageorgiou V, Fajardo R, Snyder B, Shinde-Patil V, Zichner L, Kaplan D, Langer R, Vunjak-Novakovic G (2004) Bone tissue engineering using human mesenchymal stem cells: effects of scaffold material and medium flow. Ann Biomed Eng 32:112–122

    Article  PubMed  Google Scholar 

  • Obi S, Yamamoto K, Shimizu N, Kumagaya S, Masumura T, Sokabe T, Asahara T, Ando J (2009) Fluid shear stress induces arterial differentiation of endothelial progenitor cells. J Appl Physiol 106:203–211

    Article  PubMed  CAS  Google Scholar 

  • O’Cearbhaill ED, Punchard MA, Murphy M, Barry FP, McHugh PE, Barron V (2008) Response of mesenchymal stem cells to the biomechanical environment of the endothelium on a flexible tubular silicone substrate. Biomaterials 29:1610–1619

    Article  PubMed  Google Scholar 

  • Oswald J, Boxberger S, Jørgensen B, Feldmann S, Ehninger G, Bornhäuser M, Werner C (2004) Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22:377–384

    Article  PubMed  Google Scholar 

  • Owens GK (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75:487–517

    PubMed  CAS  Google Scholar 

  • Punchard MA, Stenson-Cox C, O’cearbhaill ED, Lyons E, Gundy S, Murphy L, Pandit A, McHugh PE, Barron V (2007) Endothelial cell response to biomechanical forces under simulated vascular loading conditions. J Biomech 40:3146–3154

    Article  PubMed  CAS  Google Scholar 

  • Reilly GC, Engler AJ (2010) Intrinsic extracellular matrix properties regulate stem cell differentiation. J Biomech 43:55–62

    Article  PubMed  Google Scholar 

  • Riha GM, Lin PH, Lumsden AB, Yao Q, Chen C (2005) Roles of hemodynamic forces in vascular cell differentiation. Ann Biomed Eng 33:772–779

    Article  PubMed  Google Scholar 

  • Tada S, Tarbell JM (2002) Flow through internal elastic lamina affects shear stress on smooth muscle cells (3D simulations). Am J Physiol Heart Circ Physiol 282:H576–H584

    PubMed  CAS  Google Scholar 

  • Topper JN, Cai J, Falb D, Gimbrone MA Jr (1996) Identification of vascular endothelial genes differentially responsive to fluid mechanical stimuli: cyclooxygenase-2, manganese superoxide dismutase, and endothelial cell nitric oxide synthase are selectively up-regulated by steady laminar shear stress. Proc Natl Acad Sci USA 17:10417–10422

    Article  Google Scholar 

  • Wang DM, Tarbell JM (1995) Modeling interstitial flow in an artery wall allows estimation of wall shear stress on smooth muscle cells. J Biomech Eng 117:358–363

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Andersson M, Karlsson L, Watson MA, Cousens DJ, Jern S, Erlinge D (2003) Increased mitogenic and decreased contractile P2 receptors in smooth muscle cells by shear stress in human vessels with intact endothelium. Arterioscler Thromb Vasc Biol 1 23:1370–1376

    Article  CAS  Google Scholar 

  • Wang H, Riha GM, Yan S, Li M, Chai H, Yang H, Yao Q, Chen C (2005) Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol 25:1817–1823

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Yan S, Chai H, Riha GM, Li M, Yao Q, Chen C (2006) Shear stress induces endothelial transdifferentiation from mouse smooth muscle cells. Biochem Biophys Res Commun 346:860–865

    Article  PubMed  CAS  Google Scholar 

  • Wu CC, Chao YC, Chen CN, Chien S, Chen YC, Chien CC, Chiu JJ, Linju Yen B (2008) Synergism of biochemical and mechanical stimuli in the differentiation of human placenta-derived multipotent cells into endothelial cells. J Biomech 41:813–821

    Article  PubMed  Google Scholar 

  • Yamamoto K, Sokabe T, Watabe T, Miyazono K, Yamashita JK, Obi S, Ohura N, Matsushita A, Kamiya A, Ando J (2005) Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am J Physiol Heart Circ Physiol 288:1915–1924

    Article  Google Scholar 

  • Zhang P, Baxter J, Vinod K, Tulenko TN, Di Muzio PJ (2009) Endothelial differentiation of amniotic fluid-derived stem cells: synergism of biochemical and shear force stimuli. Stem Cells Dev 18:1299–1308

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the grants of Technology Innovation Program (10038667, Ministry of Knowledge Economy, ROK) and Priority Research Centers Program(2010-0020224, the Ministry of Education, Science and Technology).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jung-Woog Shin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 32 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, D.H., Heo, SJ., Kim, SH. et al. Shear stress magnitude is critical in regulating the differentiation of mesenchymal stem cells even with endothelial growth medium. Biotechnol Lett 33, 2351–2359 (2011). https://doi.org/10.1007/s10529-011-0706-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10529-011-0706-5

Keywords

Navigation