Directed stem cell differentiation by fluid mechanical forces.

Stem cell research has opened new and exciting possibilities in the biological and biomedical sciences, and holds great promise of impacting many areas of medicine. However, despite the rapid advancements of the last decade, the precise and efficient differentiation of stem cells into distinct cell types and tissues still remains a major challenge for the field. In an effort to reproduce biologically relevant differentiation niches, or to direct stem cell differentiation into specific cellular fates, many investigators have explored the effect of biomechanical stimulation on pluripotent cells. This review focuses on a particular type of biomechanical force, namely fluid shear stress, and our current knowledge on its ability to direct differentiation and modulate function of embryonic and somatic stem cells.

[1]  R. Bareille,et al.  Responsiveness of human bone marrow stromal cells to shear stress , 2009, Journal of tissue engineering and regenerative medicine.

[2]  M. Yen,et al.  Isolation of Multipotent Cells from Human Term Placenta , 2005, Stem cells.

[3]  H. Donahue,et al.  MAP kinase and calcium signaling mediate fluid flow-induced human mesenchymal stem cell proliferation. , 2006, American journal of physiology. Cell physiology.

[4]  A. Papadimitropoulos,et al.  Effects of fluid flow and calcium phosphate coating on human bone marrow stromal cells cultured in a defined 2D model system. , 2008, Journal of biomedical materials research. Part A.

[5]  D. L. Fry.  Acute Vascular Endothelial Changes Associated with Increased Blood Velocity Gradients , 1968, Circulation research.

[6]  G. Sukhikh,et al.  Mesenchymal Stem Cells , 2002, Bulletin of Experimental Biology and Medicine.

[7]  Kimiko Yamamoto,et al.  Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. , 2003, Journal of applied physiology.

[8]  L. Griffith,et al.  Capturing complex 3D tissue physiology in vitro , 2006, Nature Reviews Molecular Cell Biology.

[9]  H. V. von Recum,et al.  Endothelial progenitor populations in differentiating embryonic stem cells I: Identification and differentiation kinetics. , 2009, Tissue engineering. Part A.

[10]  C F Dewey,et al.  The dynamic response of vascular endothelial cells to fluid shear stress. , 1981, Journal of biomechanical engineering.

[11]  S. Chien,et al.  Synergism of biochemical and mechanical stimuli in the differentiation of human placenta-derived multipotent cells into endothelial cells. , 2008, Journal of biomechanics.

[12]  Christopher R Jacobs,et al.  Mechanically induced osteogenic differentiation – the role of RhoA, ROCKII and cytoskeletal dynamics , 2009, Journal of Cell Science.

[13]  M. Capogrossi,et al.  Shear Stress‐Mediated Chromatin Remodeling Provides Molecular Basis for Flow‐Dependent Regulation of Gene Expression , 2003, Circulation research.

[14]  Moustapha Kassem,et al.  Effect of dynamic 3-D culture on proliferation, distribution, and osteogenic differentiation of human mesenchymal stem cells. , 2008, Journal of biomedical materials research. Part A.

[15]  H. Kagami,et al.  Shear stress facilitates tissue-engineered odontogenesis. , 2006, Bone.

[16]  C. Emerson,et al.  10T1/2 cells: an in vitro model for molecular genetic analysis of mesodermal determination and differentiation. , 1989, Environmental health perspectives.

[17]  Gerhard Ehninger,et al.  Mesenchymal Stem Cells Can Be Differentiated Into Endothelial Cells In Vitro , 2004, Stem cells.

[18]  Yong Woo Lee,et al.  Effect of Low-Frequency Pulsatile Flow on Expression of Osteoblastic Genes by Bone Marrow Stromal Cells , 2009, Annals of Biomedical Engineering.

[19]  R. Chella,et al.  Effects of shear stress on 3‐D human mesenchymal stem cell construct development in a perfusion bioreactor system: Experiments and hydrodynamic modeling , 2007, Biotechnology and bioengineering.

[20]  Qizhi Yao,et al.  Shear Stress Induces Endothelial Differentiation From a Murine Embryonic Mesenchymal Progenitor Cell Line , 2005, Arteriosclerosis, thrombosis, and vascular biology.

[21]  S. Cartmell,et al.  Effect of fluid flow-induced shear stress on human mesenchymal stem cells: differential gene expression of IL1B and MAP3K8 in MAPK signaling. , 2009, Gene expression patterns : GEP.

[22]  Yubo Fan,et al.  Endothelium oriented differentiation of bone marrow mesenchymal stem cells under chemical and mechanical stimulations. , 2010, Journal of biomechanics.

[23]  I. Shapiro,et al.  Linear shear conditioning improves vascular graft retention of adipose-derived stem cells by upregulation of the alpha5beta1 integrin. , 2010, Tissue engineering. Part A.

[24]  J. Tao,et al.  Shear stress increases Cu/Zn SOD activity and mRNA expression in human endothelial progenitor cells , 2007, Journal of Human Hypertension.

[25]  T. Graf,et al.  Heterogeneity of embryonic and adult stem cells. , 2008, Cell stem cell.

[26]  Yuzhi Zhang,et al.  Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. , 2005, The Journal of clinical investigation.

[27]  Jiemei Wang,et al.  Shear stress contributes to t-PA mRNA expression in human endothelial progenitor cells and nonthrombogenic potential of small diameter artificial vessels. , 2006, Biochemical and biophysical research communications.

[28]  Michael S Sacks,et al.  Cyclic flexure and laminar flow synergistically accelerate mesenchymal stem cell-mediated engineered tissue formation: Implications for engineered heart valve tissues. , 2006, Biomaterials.

[29]  James M. Harris,et al.  Hematopoietic Stem Cell Development Is Dependent on Blood Flow , 2009, Cell.

[30]  P. Lin,et al.  Fluid shear stress regulates the expression of TGF-beta1 and its signaling molecules in mouse embryo mesenchymal progenitor cells. , 2008, The Journal of surgical research.

[31]  Kimiko Yamamoto,et al.  Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. , 2005, American journal of physiology. Heart and circulatory physiology.

[32]  G. Garcı́a-Cardeña,et al.  Biomechanical activation of vascular endothelium as a determinant of its functional phenotype , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[33]  T. Gu,et al.  Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. , 1999, Development.

[34]  Sean P. Palecek,et al.  The response of human embryonic stem cell-derived endothelial cells to shear stress. , 2008, Biotechnology and bioengineering.

[35]  S. Rafii,et al.  Emerging biology of vascular wall progenitor cells in health and disease. , 2009, Trends in molecular medicine.

[36]  A. Ullrich,et al.  Flk-1 expression defines a population of early embryonic hematopoietic precursors. , 1997, Development.

[37]  Ian A. Coe,et al.  Oscillatory fluid flow affects human marrow stromal cell proliferation and differentiation , 2004, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[38]  F. Locatelli,et al.  Mesenchymal Stromal Cells , 2009, Annals of the New York Academy of Sciences.

[39]  Jun Yamashita,et al.  Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors , 2000, Nature.

[40]  A. Atala,et al.  Sources of Stem Cells for Regenerative Medicine , 2008, Stem Cell Reviews.

[41]  Mia M. Thi,et al.  Fluid Shear Stress Upregulates Vascular Endothelial Growth Factor Gene Expression in Osteoblasts , 2007, Annals of the New York Academy of Sciences.

[42]  J. Ando,et al.  Differentiation from embryonic stem cells to vascular wall cells under in vitro pulsatile flow loading , 2005, Journal of Artificial Organs.

[43]  L. Bonewald.  Osteocytes as Dynamic Multifunctional Cells , 2007, Annals of the New York Academy of Sciences.

[44]  Shinichiro Kumagaya,et al.  Fluid shear stress induces arterial differentiation of endothelial progenitor cells. , 2009, Journal of applied physiology.

[45]  Yong Woo Lee,et al.  Effect of intermittent shear stress on mechanotransductive signaling and osteoblastic differentiation of bone marrow stromal cells. , 2008, Tissue engineering. Part A.

[46]  J. Gimble,et al.  Adipose-derived stem cells for regenerative medicine. , 2007, Circulation research.

[47]  Y. Amagai,et al.  In vitro differentiation and calcification in a new clonal osteogenic cell line derived from newborn mouse calvaria , 1983, The Journal of cell biology.

[48]  Qingbo Xu,et al.  HDAC3 is crucial in shear- and VEGF-induced stem cell differentiation toward endothelial cells , 2006, The Journal of cell biology.

[49]  G. Daley.  Stem cells: roadmap to the clinic. , 2010, The Journal of clinical investigation.

[50]  Yi Duan,et al.  Shear-induced reorganization of renal proximal tubule cell actin cytoskeleton and apical junctional complexes , 2008, Proceedings of the National Academy of Sciences.

[51]  朝倉 利久,et al.  Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries , 1989 .

[52]  L V McIntire,et al.  Flow effects on prostacyclin production by cultured human endothelial cells. , 1985, Science.

[53]  L. Xiang,et al.  Mesenchymal stem cells: a promising candidate in regenerative medicine. , 2008, The international journal of biochemistry & cell biology.

[54]  Anthony Atala,et al.  Isolation of amniotic stem cell lines with potential for therapy , 2007, Nature Biotechnology.

[55]  R. Franke,et al.  Induction of human vascular endothelial stress fibres by fluid shear stress , 1984, Nature.

[56]  David J. Mooney,et al.  Growth Factors, Matrices, and Forces Combine and Control Stem Cells , 2009, Science.

[57]  I. Shapiro,et al.  Endothelial differentiation of adipose-derived stem cells: effects of endothelial cell growth supplement and shear force. , 2009, The Journal of surgical research.

[58]  Z. Yang,et al.  Arterial elasticity identified by pulse wave analysis and its relation to endothelial function in patients with coronary artery disease , 2007, Journal of Human Hypertension.

[59]  Melissa L Knothe Tate,et al.  Modulation of stem cell shape and fate B: mechanical modulation of cell shape and gene expression. , 2008, Tissue engineering. Part A.

[60]  A. Goldstein,et al.  Fluid flow stimulates expression of osteopontin and bone sialoprotein by bone marrow stromal cells in a temporally dependent manner. , 2005, Bone.

[61]  George Q. Daley,et al.  Biomechanical forces promote embryonic haematopoiesis , 2009, Nature.

[62]  KimikoYamamoto,et al.  Shear Stress Increases Expression of the Arterial Endothelial Marker EphrinB2 in Murine ES Cells via the VEGF-Notch Signaling Pathways , 2009 .

[63]  Jiemei Wang,et al.  In vitro shear stress modulates antithrombogenic potentials of human endothelial progenitor cells , 2007, Journal of Thrombosis and Thrombolysis.