Fluid shear stress pre-conditioning promotes endothelial morphogenesis of embryonic stem cells within embryoid bodies

Tissue Engineering - Part A

Volumn 20, Issue 5-6, 2014, Pages 954-965

  Nsiah, Barbara A ^a   Ahsan, Tabassum ^b   Griffiths, Sarah ^b   Cooke, Marissa ^c   Nerem, Robert M ^a,b   Mcdevitt, Todd C ^b,c  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c Emory University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; GENE EXPRESSION; GLYCOPROTEINS; MORPHOLOGY; PHYSIOLOGICAL MODELS; SHEAR FLOW; SHEAR STRESS; STEM CELLS;

EMBRYONIC STEM CELLS; ENDOTHELIAL MARKER; ENDOTHELIAL MORPHOGENESIS; FLUID SHEAR STRESS; PLURIPOTENT STEM CELLS; STEM CELL DIFFERENTIATION; TISSUE ENGINEERED CONSTRUCTS; VASCULAR DIFFERENTIATION;

ENDOTHELIAL CELLS;

CD31 ANTIGEN; COLLAGEN TYPE 4; VASCULAR ENDOTHELIAL CADHERIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; GENE EXPRESSION; MARKER GENE; MORPHOGENESIS; MOUSE; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SHEAR STRESS;

ANIMALS; ANTIGENS, CD; CADHERINS; CELL DIFFERENTIATION; CULTURE MEDIA, CONDITIONED; EMBRYOID BODIES; ENDOTHELIUM; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HEMATOPOIESIS; MICE; MORPHOGENESIS; SHEAR STRENGTH; STRESS, MECHANICAL; TIME FACTORS; VON WILLEBRAND FACTOR;

EID: 84896893679     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0243     Document Type: Article

References (51)

1. Discher, D.E., Mooney, D.J., and Zandstra, P.W. Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673, 2009
2. Murry, C.E., and Keller, G. Differentiation of embryonic stem cells to clinically relevant populations: Lessons from embryonic development. Cell 132, 661, 2008
3. Adamo, L., Naveiras, O., Wenzel, P.L., McKinney-Freeman, S., Mack, P.J., Gracia-Sancho, J., et al. Biomechanical forces promote embryonic haematopoiesis. Nature 459, 1131, 2009
4. Huang, H., Nakayama, Y., Qin, K., Yamamoto, K., Ando, J., Yamashita, J., et al. Differentiation from embryonic stem cells to vascular wall cells under in vitro pulsatile flow loading. J Artif Organs 8, 110, 2005
5. Zeng, L., Xiao, Q., Margariti, A., Zhang, Z., Zampetaki, A., Patel, S., et al. HDAC3 is crucial in shear- And VEGFinduced stem cell differentiation toward endothelial cells. J Cell Biol 174, 1059, 2006
6. Ahsan, T., and Nerem, R.M. Fluid shear stress promotes an endothelial-like phenotype during the early differentiation of embryonic stem cells. Tissue Eng Part A 16, 3547, 2010
7. Yamamoto, K., Sokabe, T., Watabe, T., Miyazono, K., Yamashita, J.K., Obi, S., et al. 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, H1915, 2005
8. Wang, H., Riha, G.M., Yan, S., Li, M., Chai, H., Yang, H., et al. Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol 25, 1817, 2005
9. Masumura, T., Yamamoto, K., Shimizu, N., Obi, S., and Ando, J. Shear stress increases expression of the arterial endothelial marker ephrinB2 in murine ES cells via the VEGF-Notch signaling pathways. Arterioscler Thromb Vasc Biol 29, 2125, 2009
10. Kinney, M.A., Sargent, C.Y., and McDevitt, T.C. The multiparametric effects of hydrodynamic environments on stem cell culture. Tissue Eng Part B Rev 17, 249, 2011
11. Placzek, M.R., Chung, I.-M., Macedo, H.M., Ismail, S., Mortera Blanco, T., Lim, M., et al. Stem cell bioprocessing: Fundamentals and principles. J R Soc Interface 6, 209, 2009
12. Griffith, L.G., and Swartz, M.A. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 7, 211, 2006
13. Levesque, M.J., Nerem, R.M., and Sprague, E.A. Vascular endottielial cell proliferation in culture and the influence of flow. Biomaterials 11, 702, 1990
14. Levesque, M.J., and Nerem, R.M. The elongation and orientation of cultured endothelial cells in response to shear stress. J Biomech Eng 107, 341, 1985
15. Ji, R.P., Phoon, C.K.L., Aristiza'bal, O., McGrath, K.E., Palis, J., and Turnbull, D.H. Onset of cardiac function during early mouse embryogenesis coincides with entry of primitive erythroblasts into the embryo proper. Circ Res 92, 133, 2003
16. Doetschman, T.C., Eistetter, H., Katz, M., Schmidt, W., and Kemler, R. The in vitro development of blastocystderived embryonic stem cell lines: Formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87, 27, 1985
17. Itskovitz-Eldor, J., Schuldiner, M., Karsenti, D., Eden, A., Yanuka, O., Amit, M., et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med 6, 88, 2000
18. Quinn, G., Ochiya, T., Terada, M., and Yoshida, T. Mouse flt-1 promoter directs endothelial-specific expression in the embyroid body model of embryogenesis. Biochem Biophys Res Commun 276, 1089, 2000
19. Ferreira, L.S., Gerecht, S., Shieh, H.F., Watson, N., Rupnick, M.A., Dallabrida, S.M., et al. Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res 101, 286, 2007
20. Wang, R., Clark, R., and Bautch, V.L. Embryonic stem cell-derived cystic embryoid bodies form vascular channels: An in vitro model of blood vessel development. Development 114, 303, 1992
21. Risau, W., Sariola, H., Zerwes, H.G., Sasse, J., Ekblom, P., Kemler, R., et al. Vasculogenesis and angiogenesis in embryonic-stem-cell-derived embryoid bodies. Development 102, 471, 1988
22. Vittet, D., Prandini, M.H., Berthier, R., Schweitzer, A., Martin-Sisteron, H., Uzan, G., et al. Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood 88, 3424, 1996
23. Niebruegge, S., Bauwens, C.L., Peerani, R., Thavandiran, N., Masse, S., Sevaptisidis, E., et al. Generation of human embryonic stem cell-derived mesoderm and cardiac cells using size-specified aggregates in an oxygen-controlled bioreactor. Biotechnol Bioeng 102, 493, 2009
24. Bauwens, C.L., Peerani, R., Niebruegge, S., Woodhouse, K.A., Kumacheva, E., Husain, M., et al. Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells 26, 2300, 2008
25. Mohr, J.C., de Pablo, J.J., and Palecek, S.P. 3-D microwell culture of human embryonic stem cells. Biomaterials 27, 6032, 2006
26. Kinney, M.A., Saeed, R., and McDevitt, T.C. Systematic analysis of embryonic stem cell differentiation in hydrodynamic environments with controlled embryoid body size. Integr Biol 4, 641, 2012
27. Carpenedo, R.L., Bratt-Leal, A.M., Marklein, R.A., Seaman, S.A., Bowen, N.J., McDonald, J.F., et al. Homogeneous and organized differentiation within embryoid bodies induced by microsphere-mediated delivery of small molecules. Biomaterials 30, 2507, 2009
28. Bratt-Leal, A.M., Carpenedo, R.L., Ungrin, M.D., Zandstra, P.W., and McDevitt, T.C. Incorporation of biomaterials in multicellular aggregates modulates pluripotent stem cell differentiation. Biomaterials 32, 48, 2011
29. Dang, S.M., Gerecht-Nir, S., Chen, J., Itskovitz-Eldor, J., and Zandstra, P.W. Controlled, scalable embryonic stem cell differentiation culture. Stem Cells 22, 275, 2004
30. Li, Z., Wu, J.C., Sheikh, A.Y., Kraft, D., Cao, F., Xie, X., et al. Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation 116, I46, 2007
31. Carpenedo, R.L., Sargent, C.Y., and McDevitt, T.C. Rotary suspension culture enhances the efficiency, yield, and homogeneity of embryoid body differentiation. Stem Cells 25, 2224, 2007
32. McCloskey, K.E., Lyons, I., Rao, R.R., Stice, S.L., and Nerem, R.M. Purified and proliferating endothelial cells derived and expanded in vitro from embryonic stem cells. Endothelium 10, 329, 2003
33. Nishikawa, S.I., Nishikawa, S., Hirashima, M., Matsuyoshi, N., and Kodama, H. Progressive lineage analysis by cell sorting and culture identifies FLK1 + VE-cadherin + cells at a diverging point of endothelial and hemopoietic lineages. Development 125, 1747, 1998
34. Wolfe, R.P., and Ahsan, T. Shear stress during early embryonic stem cell differentiation promotes hematopoietic and endothelial phenotypes. Biotechnol Bioeng 110, 1231, 2013
35. McCloskey, K.E., Smith, D.A., Jo, H., and Nerem, R.M. Embryonic stem cell-derived endothelial cells may lack complete functional maturation in vitro. J Vasc Res 43, 411, 2006
36. Metallo, C.M., Vodyanik, M.A., de Pablo, J.J., Slukvin, II, and Palecek, S.P. The response of human embryonic stem cell-derived endothelial cells to shear stress. Biotechnol Bioeng 100, 830, 2008
37. Krah, K., Mironov, V., Risau, W., and Flamme, I. Induction of vasculogenesis in quail blastodisc-derived embryoid bodies. Dev Biol 164, 123, 1994
38. Kazemi, S., Wenzel, D., Kolossov, E., Lenka, N., Raible, A., Sasse, P., et al. Differential role of bFGF and VEGF for vasculogenesis. Cell Physiol Biochem 12, 55, 2002
39. Zhang, P., Baxter, J., Vinod, K., Tulenko, T.N., and Di Muzio, P.J. Endothelial differentiation of amniotic fluidderived stem cells: Synergism of biochemical and shear force stimuli. Stem Cells Dev 18, 1299, 2009
40. Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J.C., and Keller, G. A common precursor for hematopoietic and endothelial cells. Development 125, 725, 1998
41. Kennedy, M., D'Souza, S.L., Lynch-Kattman, M., Schwantz, S., and Keller, G. Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 109, 2679, 2007
42. Fehling, H.J., Lacaud, G., Kubo, A., Kennedy, M., Robertson, S., Keller, G., et al. Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130, 4217, 2003
43. Sabin, F.R. Studies on the origin of blood-vessels and of red blood-corpuscles as seen in the living blastoderm of chicks during the second day of incubation. Contrib Embryol 9, 215, 1920
44. Medvinsky, A., and Dzierzak, E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897, 1996
45. Palis, J., and Yoder, M.C. Yolk-sac hematopoiesis: The first blood cells of mouse and man. Exp Hematol 29, 927, 2001
46. Vischer, U.M. von Willebrand factor, endothelial dysfunction, and cardiovascular disease. J Thromb Haemost 4, 1186, 2006
47. Halbleib, J.M., and Nelson, W.J. Cadherins in development: Cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20, 3199, 2006
48. Takeichi, M. The cadherins: Cell-cell adhesion molecules controlling animal morphogenesis. Development 102, 639, 1988
49. Lampugnani, M.G., Resnati, M., Raiteri, M., Pigott, R., Pisacane, A., Houen, G., et al. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J Cell Biol 118, 1511, 1992
50. Gory-Faure, S., Prandini, M.H., Pointu, H., Roullot, V., Pignot-Paintrand, I., Vernet, M., et al. Role of vascular endothelial-cadherin in vascular morphogenesis. Development 126, 2093, 1999
51. Breier, G., Breviario, F., Caveda, L., Berthier, R., Schnurch, H., Gotsch, U., et al. Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system. Blood 87, 630, 1996