Differentiation of stem/progenitor cells into vascular cells in response to fluid mechanical forces
Tóm tắt
Vascular functions are regulated not only by chemical mediators, such as hormones, cytokines, and neurotransmitters, but by mechanical hemodynamic forces generated by blood flow and blood pressure. The mechanical force-mediated regulation is based on the ability of vascular cells, including endothelial cells and smooth muscle cells, to recognize fluid mechanical forces, i.e., the shear stress produced by flowing blood and the cyclic strain generated by blood pressure, and to transmit the signals into the cell interior, where they trigger cell responses that involve changes in cell morphology, cell function, and gene expression. Recent studies have revealed that immature cells, such as endothelial progenitor cells (EPCs) and embryonic stem (ES) cells, as well as adult vascular cells, respond to fluid mechanical forces. Shear stress and cyclic strain promote the proliferation and differentiation of EPCs and ES cells into vascular cells and enhance their ability to form new vessels. Even more recently, attempts have been made to apply fluid mechanical forces to EPCs and ES cells cultured on polymer tubes and develop tissue-engineered blood vessel grafts that have a structure and function similar to that of blood vessels in vivo. This review summarizes the current state of knowledge concerning the mechanobiological responses of stem/progenitor cells and its potential applications to tissue engineering.
Tài liệu tham khảo
Ando J, Yamamoto K. Vascular mechanobiology: endothelial cell responses to fluid shear stress. Circ J. 2009;73:1983–92.
Cai Z, Xin J, Pollock DM, Pollock JS. Shear stress-mediated NO production in inner medullary collecting duct cells. Am J Physiol Renal Physiol. 2000;279:F270–4.
Essig M, Terzi F, Burtin M, Friedlander G. Mechanical strains induced by tubular flow affect the phenotype of proximal tubular cells. Am J Physiol Renal Physiol. 2001;281:F751–62.
Sidhaye VK, Schweitzer KS, Caterina MJ, Shimoda L, King LS. Shear stress regulates aquaporin-5 and airway epithelial barrier function. Proc Natl Acad Sci USA. 2008;105:3345–50.
Cooke HJ, Wunderlich J, Christofi FL. “The force be with you”: ATP in gut mechanosensory transduction. News Physiol Sci. 2003;18:43–9.
Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature. 2003;421:172–7.
Nonaka S, Shiratori H, Saijoh Y, Hamada H. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature. 2002;418:96–9.
Kamiya A, Bukhari R, Togawa T. Adaptive regulation of wall shear stress optimizing vascular tree function. Bull Math Biol. 1984;46:127–37.
Dewey CF Jr, Bussolari SR, Gimbrone MA Jr, Davies PF. The dynamic response of vascular endothelial cells to fluid shear stress. J Biomech Eng. 1981;103:177–85.
Frangos JA, Eskin SG, McIntire LV, Ives CL. Flow effects on prostacyclin production by cultured human endothelial cells. Science. 1985;227:1477–9.
Korenaga R, Ando J, Tsuboi H, Yang W, Sakuma I, Toyo-oka T, Kamiya A. Laminar flow stimulates ATP- and shear stress-dependent nitric oxide production in cultured bovine endothelial cells. Biochem Biophys Res Commun. 1994;198:213–9.
Takada Y, Shinkai F, Kondo S, Yamamoto S, Tsuboi H, Korenaga R, Ando J. Fluid shear stress increases the expression of thrombomodulin by cultured human endothelial cells. Biochem Biophys Res Commun. 1994;205:1345–52.
Ohura N, Yamamoto K, Ichioka S, Sokabe T, Nakatsuka H, Baba A, Shibata M, Nakatsuka T, Harii K, Wada Y, Kohro T, Kodama T, Ando J. Global analysis of shear stress-responsive genes in vascular endothelial cells. J Atheroscler Thromb. 2003;10:304–13.
Ando J, Korenaga R, Kamiya A. Flow-induced endothelial gene regulation. In: Lelkes PI, editors. Mechanical forces and the endothelium. London: Harwood Academic Publishers; 1999. pp. 111–26.
Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964–7.
Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999;5:434–8.
Yamamoto K, Takahashi T, Asahara T, Ohura N, Sokabe T, Kamiya A, Ando J. Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J Appl Physiol. 2003;95:2081–8.
Tao J, Yang Z, Wang JM, Tu C, Pan SR. Effects of fluid shear stress on eNOS mRNA expression and NO production in human endothelial progenitor cells. Cardiology. 2006;106:82–8.
Yang Z, Wang JM, Wang LC, Chen L, Tu C, Luo CF, Tang AL, Wang SM, Tao J. In vitro shear stress modulates antithrombogenic potentials of human endothelial progenitor cells. J Thromb Thrombolysis. 2007;23:121–7.
Tao J, Yang Z, Wang JM, Wang LC, Luo CF, Tang AL, Dong YG, Ma H. Shear stress increases Cu/Zn SOD activity and mRNA expression in human endothelial progenitor cells. J Hum Hypertens. 2007;21:353–8.
Ye C, Bai L, Yan ZQ, Wang YH, Jiang ZL. Shear stress and vascular smooth muscle cells promote endothelial differentiation of endothelial progenitor cells via activation of Akt. Clin Biomech. 2008;23(Suppl 1):S118–24.
Wu CC, Chao YC, Chen CN, Chien S, Chen YC, Chien CC, Chiu JJ, Linju Yen B. Synergism of biochemical and mechanical stimuli in the differentiation of human placenta-derived multipotent cells into endothelial cells. J Biomech. 2008;41:813–21.
Fischer LJ, McIlhenny S, Tulenko T, Golesorkhi N, Zhang P, Larson R, Lombardi J, Shapiro I, DiMuzio PJ. Endothelial differentiation of adipose-derived stem cells: effects of endothelial cell growth supplement and shear force. J Surg Res. 2009;152:157–66.
Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154–6.
Bain G, Kitchens D, Yao M, Huettner JE, Gottlieb DI. Embryonic stem cells express neuronal properties in vitro. Dev Biol. 1995;168:342–57.
Rohwedel J, Maltsev V, Bober E, Arnold HH, Hescheler J, Wobus AM. Muscle cell differentiation of embryonic stem cells reflects myogenesis in vivo: developmentally regulated expression of myogenic determination genes and functional expression of ionic currents. Dev Biol. 1994;164:87–101.
Vittet D, Prandini M-H, Berthier R, Schweitzer A, Martin-Sisteron H, Uzan G, Dejana E. Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood. 1996;88:3424–31.
Kramer J, Hegert C, Guan K, Wobus AM, Muller PK, Rohwedel J. Embryonic stem cell-derived chondrogenic differentiation in vitro: activation by BMP-2 and BMP-4. Mech Dev. 2000;92:193–205.
Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T, Naito M, Nakao K. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature. 2000;408:92–6.
Jones EA, Baron MH, Fraser SE, Dickinson ME. Measuring hemodynamic changes during mammalian development. Am J Physiol Heart Circ Physiol. 2004;287:H1561–9.
Yamamoto K, Sokabe T, Watabe T, Miyazono K, Yamashita JK, Obi S, Ohura N, Matsushita A, Kamiya A, Ando J. Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am J Physiol Heart Circ Physiol. 2005;288:H1915–24.
McCloskey KE, Smith DA, Jo H, Nerem RM. Embryonic stem cell-derived endothelial cells may lack complete functional maturation in vitro. J Vasc Res. 2006;43:411–21.
Metallo CM, Vodyanik MA, de Pablo JJ, Slukvin II, Palecek SP. The response of human embryonic stem cell-derived endothelial cells to shear stress. Biotechnol Bioeng. 2008;100:830–7.
Wang H, Riha GM, Yan S, Li M, Chai H, Yang H, Yao Q, Chen C. Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol. 2005;25:1817–23.
Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407:242–8.
le Noble F, Moyon D, Pardanaud L, Yuan L, Djonov V, Matthijsen R, Breant C, Fleury V, Eichmann A. Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development. 2004;131:361–75.
Wang HU, Chen ZF, Anderson DJ. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell. 1998;93:741–53.
Yancopoulos GD, Klagsbrun M, Folkman J. Vasculogenesis, angiogenesis, and growth factors: ephrins enter the fray at the border. Cell. 1998;93:661–4.
Torres-Vazquez J, Kamei M, Weinstein BM. Molecular distinction between arteries and veins. Cell Tissue Res. 2003;314:43–59.
Masumura T, Yamamoto K, Shimizu N, Obi S, 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. 2009;29:2125–31.
Othman-Hassan K, Patel K, Papoutsi M, Rodriguez-Niedenfuhr M, Christ B, Wilting J. Arterial identity of endothelial cells is controlled by local cues. Dev Biol. 2001;237:398–409.
Obi S, Yamamoto K, Shimizu N, Kumagaya S, Masumura T, Sokabe T, Asahara T, Ando J. Fluid shear stress induces arterial differentiation of endothelial progenitor cells. J Appl Physiol. 2009;106:203–11.
Jin ZG, Ueba H, Tanimoto T, Lungu AO, Frame MD, Berk BC. Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ Res. 2003;93:354–63.
Zeng L, Xiao Q, Margariti A, Zhang Z, Zampetaki A, Patel S, Capogrossi MC, Hu Y, Xu Q. HDAC3 is crucial in shear- and VEGF-induced stem cell differentiation toward endothelial cells. J Cell Biol. 2006;174:1059–69.
Illi B, Scopece A, Nanni S, Farsetti A, Morgante L, Biglioli P, Capogrossi MC, Gaetano C. Epigenetic histone modification and cardiovascular lineage programming in mouse embryonic stem cells exposed to laminar shear stress. Circ Res. 2005;96:501–8.
Yamamoto K, Korenaga R, Kamiya A, Ando J. Fluid shear stress activates Ca2+ influx into human endothelial cells via P2X4 purinoceptors. Circ Res. 2000;87:385–91.
Yamamoto K, Sokabe T, Matsumoto T, Yoshimura K, Shibata M, Ohura N, Fukuda T, Sato T, Sekine K, Kato S, Isshiki M, Fujita T, Kobayashi M, Kawamura K, Masuda H, Kamiya A, Ando J. Impaired flow-dependent control of vascular tone and remodeling in P2X4-deficient mice. Nat Med. 2006;12:133–7.
Yamamoto K, Sokabe T, Ohura N, Nakatsuka H, Kamiya A, Ando J. Endogenously released ATP mediates shear stress-induced Ca2+ influx into pulmonary artery endothelial cells. Am J Physiol Heart Circ Physiol. 2003;285:H793–803.
Novak I. ATP as a signaling molecule: the exocrine focus. News Physiol Sci. 2003;18:12–7.
Jakkaraju S, Zhe X, Schuger L. Role of stretch in activation of smooth muscle cell lineage. Trends Cardiovasc Med. 2003;13:330–5.
Hamilton DW, Maul TM, Vorp DA. Characterization of the response of bone marrow-derived progenitor cells to cyclic strain: implications for vascular tissue-engineering applications. Tissue Eng. 2004;10:361–9.
Park JS, Chu JS, Cheng C, Chen F, Chen D, Li S. Differential effects of equiaxial and uniaxial strain on mesenchymal stem cells. Biotechnol Bioeng. 2004;88:359–68.
Schmelter M, Ateghang B, Helmig S, Wartenberg M, Sauer H. Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. Faseb J. 2006;20:1182–4.
Shimizu N, Yamamoto K, Obi S, Kumagaya S, Masumura T, Shimano Y, Naruse K, Yamashita JK, Igarashi T, Ando J. Cyclic strain induces mouse embryonic stem cell differentiation into vascular smooth muscle cells by activating PDGF receptor beta. J Appl Physiol. 2008;104:766–72.
Riha GM, Wang X, Wang H, Chai H, Mu H, Lin PH, Lumsden AB, Yao Q, Chen C. Cyclic strain induces vascular smooth muscle cell differentiation from murine embryonic mesenchymal progenitor cells. Surgery. 2007;141:394–402.
Saha S, Ji L, de Pablo JJ, Palecek SP. Inhibition of human embryonic stem cell differentiation by mechanical strain. J Cell Physiol. 2006;206:126–37.
Weinberg CB, Bell E. A blood vessel model constructed from collagen and cultured vascular cells. Science. 1986;231:397–400.
Niklason LE, Gao J, Abbott WM, Hirschi KK, Houser S, Marini R, Langer R. Functional arteries grown in vitro. Science. 1999;284:489–93.
Isenberg BC, Williams C, Tranquillo RT. Small-diameter artificial arteries engineered in vitro. Circ Res. 2006;98:25–35.
Shirota T, He H, Yasui H, Matsuda T. Human endothelial progenitor cell-seeded hybrid graft: proliferative and antithrombogenic potentials in vitro and fabrication processing. Tissue Eng. 2003;9:127–36.
Kaushal S, Amiel GE, Guleserian KJ, Shapira OM, Perry T, Sutherland FW, Rabkin E, Moran AM, Schoen FJ, Atala A, Soker S, Bischoff J, Mayer JE Jr. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med. 2001;7:1035–40.
Wu X, Rabkin-Aikawa E, Guleserian KJ, Perry TE, Masuda Y, Sutherland FW, Schoen FJ, Mayer JE Jr, Bischoff J. Tissue-engineered microvessels on three-dimensional biodegradable scaffolds using human endothelial progenitor cells. Am J Physiol Heart Circ Physiol. 2004;287:H480–7.
Huang H, Nakayama Y, Qin K, Yamamoto K, Ando J, Yamashita J, Itoh H, Kanda K, Yaku H, Okamoto Y, Nemoto Y. Differentiation from embryonic stem cells to vascular wall cells under in vitro pulsatile flow loading. J Artif Organs. 2005;8:110–8.
Guo XM, Zhao YS, Chang HX, Wang CY, E LL, Zhang XA, Duan CM, Dong LZ, Jiang H, Li J, Song Y, Yang XJ. Creation of engineered cardiac tissue in vitro from mouse embryonic stem cells. Circulation. 2006;113:2229–37.