Role of biomechanical forces in stem cell vascular lineage differentiation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 10, 2014, Pages 2184-2190

  Potter, Claire M F ^a   Lao, Ka Hou ^a   Zeng, Lingfang ^a   Xu, Qingbo ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Adventitia; Atherosclerosis; Cell differentiation; Stem cells

Indexed keywords

ARTICLE; BIOMECHANICS; BLOOD VESSEL WALL; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; FORCE; HUMAN; NONHUMAN; RESTENOSIS; SHEAR STRESS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; STEM CELL; STENT; VASCULAR SURGERY; ANIMAL; ATHEROSCLEROSIS; BLOOD FLOW; BLOOD VESSEL; CELL PROLIFERATION; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; REGENERATION;

ANIMALS; ATHEROSCLEROSIS; BLOOD VESSELS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; HUMANS; MECHANOTRANSDUCTION, CELLULAR; PHENOTYPE; REGENERATION; REGIONAL BLOOD FLOW; STEM CELLS; STRESS, MECHANICAL;

EID: 84914105210     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.303423     Document Type: Article

References (77)

1. Ramalho-Santos M, Willenbring H. On the origin of the term "stem cell". Cell Stem Cell. 2007;1:35-38.
2. Krawiec JT, Vorp DA. Adult stem cell-based tissue engineered blood vessels: a review. Biomaterials. 2012;33:3388-3400.
3. Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol. 2003;23:168-175.
4. Caro CG, Fitz-Gerald JM, Schroter RC. Arterial wall shear and distribution of early atheroma in man. Nature. 1969;223:1159-1160.
5. Zarins CK, Giddens DP, Bharadvaj BK, Sottiurai VS, Mabon RF, Glagov S. Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res. 1983;53:502-514.
6. Haga JH, Li YS, Chien S. Molecular basis of the effects of mechanical stretch on vascular smooth muscle cells. J Biomech. 2007;40:947-960.
7. Stolberg S, McCloskey KE. Can shear stress direct stem cell fate? Biotechnol Prog. 2009;25:10-19.
8. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res. 2007;100:1249-1260.
9. Villaron EM, Almeida J, López-Holgado N, Alcoceba M, Sánchez-Abarca LI, Sanchez-Guijo FM, Alberca M, Pérez-Simon JA, San Miguel JF, Del Cañizo MC. Mesenchymal stem cells are present in peripheral blood and can engraft after allogeneic hematopoietic stem cell transplantation. Haematologica. 2004;89:1421-1427.
10. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001;44:1928-1942.
11. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol. 2008;8:726-736.
12. Tropel P, Platet N, Platel JC, Noël D, Albrieux M, Benabid AL, Berger F. Functional neuronal differentiation of bone marrow-derived mesenchymal stem cells. Stem Cells. 2006;24:2868-2876.
13. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. Bone marrow cells regenerate infarcted myocardium. Nature. 2001;410:701-705.
14. Oswald J, Boxberger S, Jørgensen B, Feldmann S, Ehninger G, Bornhäuser M, Werner C. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells. 2004;22:377-384.
15. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. 2002;8:403-409.
16. Boehm M, Olive M, True AL, Crook MF, San H, Qu X, Nabel EG. Bone marrow-derived immune cells regulate vascular disease through a p27(Kip1)-dependent mechanism. J Clin Invest. 2004;114:419-426.
17. George J, Afek A, Abashidze A, Shmilovich H, Deutsch V, Kopolovich J, Miller H, Keren G. Transfer of endothelial progenitor and bone marrow cells influences atherosclerotic plaque size and composition in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol. 2005;25:2636-2641.
18. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, Pollok K, Ferkowicz MJ, Gilley D, Yoder MC. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104:2752-2760.
19. Critser PJ, Voytik-Harbin SL, Yoder MC. Isolating and defining cells to engineer human blood vessels. Cell Prolif. 2011;44(suppl 1):15-21.
20. Yoder MC. Is endothelium the origin of endothelial progenitor cells? Arterioscler Thromb Vasc Biol. 2010;30:1094-1103.
21. Davies PF, Remuzzi A, Gordon EJ, Dewey CF Jr, Gimbrone MA Jr. Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc Natl Acad Sci U S A. 1986;83:2114-2117.
22. Foteinos G, Hu Y, Xiao Q, Metzler B, Xu Q. Rapid endothelial turnover in atherosclerosis-prone areas coincides with stem cell repair in apolipoprotein E-deficient mice. Circulation. 2008;117:1856-1863.
23. Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2008;28:1584-1595.
24. Naito H, Kidoya H, Sakimoto S, Wakabayashi T, Takakura N. Identification and characterization of a resident vascular stem/progenitor cell population in preexisting blood vessels. EMBO J. 2012;31:842-855.
25. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, Xu Q. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest. 2004;113:1258-1265.
26. Zengin E, Chalajour F, Gehling UM, Ito WD, Treede H, Lauke H, Weil J, Reichenspurner H, Kilic N, Ergün S. Vascular wall resident progenitor cells: a source for postnatal vasculogenesis. Development. 2006;133:1543-1551.
27. Passman JN, Dong XR, Wu SP, Maguire CT, Hogan KA, Bautch VL, Majesky MW. A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proc Natl Acad Sci U S A. 2008;105:9349-9354.
28. Srinivasan S, Baldwin HS, Aristizabal O, Kwee L, Labow M, Artman M, Turnbull DH. Noninvasive, in utero imaging of mouse embryonic heart development with 40-MHz echocardiography. Circulation. 1998;98:912-918.
29. Adamo L, Naveiras O, Wenzel PL, McKinney-Freeman S, Mack PJ, Gracia-Sancho J, Suchy-Dicey A, Yoshimoto M, Lensch MW, Yoder MC, García-Cardeña G, Daley GQ. Biomechanical forces promote embryonic haematopoiesis. Nature. 2009;459:1131-1135.
30. Lucitti JL, Jones EA, Huang C, Chen J, Fraser SE, Dickinson ME. Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development. 2007;134:3317-3326.
31. Udan RS, Vadakkan TJ, Dickinson ME. Dynamic responses of endothelial cells to changes in blood flow during vascular remodeling of the mouse yolk sac. Development. 2013;140:4041-4050.
32. Ingber DE. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 2006;20:811-827.
33. Ingber DE. Tensegrity I. Cell structure and hierarchical systems biology. J Cell Sci. 2003;116(Pt 7):1157-1173.
34. Ingber DE. Tensegrity II. How structural networks influence cellular information processing networks. J Cell Sci. 2003;116(Pt 8):1397-1408.
35. Pahakis MY, Kosky JR, Dull RO, Tarbell JM. The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem Biophys Res Commun. 2007;355:228-233.
36. Barakat AI, Lieu DK, Gojova A. Secrets of the code: do vascular endothelial cells use ion channels to decipher complex flow signals? Biomaterials. 2006;27:671-678.
37. Chachisvilis M, Zhang YL, Frangos JA. G protein-coupled receptors sense fluid shear stress in endothelial cells. Proc Natl Acad Sci U S A. 2006;103:15463-15468.
38. Cohen DM, Chen CS. Mechanical control of stem cell differentiation. In: StemBook. Cambridge, MA: Harvard Stem Cell Institute; 2008.
39. 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-H1924.
40. 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;174:1059-1069.
41. Jin ZG, Ueba H, Tanimoto T, Lungu AO, Frame MD, Berk BC. Ligandindependent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ Res. 2003;93:354-363.
42. Zachary I, Gliki G. Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc Res. 2001;49:568-581.
43. 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 (Bristol, Avon). 2008;23(suppl 1):S118-S124.
44. Cheng BB, Yan ZQ, Yao QP, Shen BR, Wang JY, Gao LZ, Li YQ, Yuan HT, Qi YX, Jiang ZL. Association of SIRT1 expression with shear stress induced endothelial progenitor cell differentiation. J Cell Biochem. 2012;113:3663-3671.
45. Obi S, Masuda H, Shizuno T, Sato A, Yamamoto K, Ando J, Abe Y, Asahara T. Fluid shear stress induces differentiation of circulating phenotype endothelial progenitor cells. Am J Physiol Cell Physiol. 2012;303:C595-C606.
46. Zhang P, Moudgill N, Hager E, Tarola N, Dimatteo C, McIlhenny S, Tulenko T, DiMuzio PJ. Endothelial differentiation of adipose-derived stem cells from elderly patients with cardiovascular disease. Stem Cells Dev. 2011;20:977-988.
47. 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;29:2125-2131.
48. Rössig L, Urbich C, Brühl T, et al. Histone deacetylase activity is essential for the expression of HoxA9 and for endothelial commitment of progenitor cells. J Exp Med. 2005;201:1825-1835.
49. Dunn J, Qiu H, Kim S, Jjingo D, Hoffman R, Kim C, Jang I, Son D, Kim D, Pan C, Fan Y, Jordan IK, Jo H. Flow alters genome wide methylation, regulating endothelial gene expression and atherosclerosis. J Clin Invest. 2014;124:3187-3199.
50. 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 (1985). 2009;106:203-211.
51. Fang F, Wasserman SM, Torres-Vazquez J, Weinstein B, Cao F, Li Z, Wilson KD, Yue W, Wu JC, Xie X, Pei X. The role of Hath6, a newly identified shear-stress-responsive transcription factor, in endothelial cell differentiation and function. J Cell Sci. 2014;127(Pt 7):1428-1440.
52. Cui X, Zhang X, Guan X, Li H, Li X, Lu H, Cheng M. Shear stress augments the endothelial cell differentiation marker expression in late EPCs by upregulating integrins. Biochem Biophys Res Commun. 2012;425:419-425.
53. Cheng M, Guan X, Li H, Cui X, Zhang X, Li X, Jing X, Wu H, Avsar E. Shear stress regulates late EPC differentiation via mechanosensitive molecule- mediated cytoskeletal rearrangement. PLoS One. 2013;8:e67675.
54. Urbich C, Dernbach E, Reissner A, Vasa M, Zeiher AM, Dimmeler S. Shear stress-induced endothelial cell migration involves integrin signaling via the fibronectin receptor subunits alpha(5) and beta(1). Arterioscler Thromb Vasc Biol. 2002;22:69-75.
55. Lee TH, Seng S, Li H, Kennel SJ, Avraham HK, Avraham S. Integrin regulation by vascular endothelial growth factor in human brain microvascular endothelial cells: role of alpha6beta1 integrin in angiogenesis. J Biol Chem. 2006;281:40450-40460.
56. Nikmanesh M, Shi ZD, Tarbell JM. Heparan sulfate proteoglycan mediates shear stress-induced endothelial gene expression in mouse embryonic stem cell-derived endothelial cells. Biotechnol Bioeng. 2012;109:583-594.
57. Zhang X, Nan Y, Wang H, Chen J, Wang N, Xie J, Ma J, Wang Z. Model microgravity enhances endothelium differentiation of mesenchymal stem cells. Naturwissenschaften. 2013;100:125-133.
58. Fang F, Wasserman SM, Torres-Vazquez J, Weinstein B, Cao F, Li Z, Wilson KD, Yue W, Wu JC, Xie X, Pei X. The role of Hath6, a newly identified shear-stress-responsive transcription factor, in endothelial cell differentiation and function. J Cell Sci. 2014;127(Pt 7):1428-1440.
59. Gimbrone MA Jr, Resnick N, Nagel T, Khachigian LM, Collins T, Topper JN. Hemodynamics, endothelial gene expression, and atherogenesis. Ann N Y Acad Sci. 1997;811:1-10.
60. Koskinas KC, Chatzizisis YS, Antoniadis AP, Giannoglou GD. Role of endothelial shear stress in stent restenosis and thrombosis: pathophysiologic mechanisms and implications for clinical translation. J Am Coll Cardiol. 2012;59:1337-1349.
61. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801.
62. Ghazanfari S, Tafazzoli-Shadpour M, Shokrgozar MA. Effects of cyclic stretch on proliferation of mesenchymal stem cells and their differentiation to smooth muscle cells. Biochem Biophys Res Commun. 2009;388:601-605.
63. Maul TM, Chew DW, Nieponice A, Vorp DA. Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation. Biomech Model Mechanobiol. 2011;10:939-953.
64. Nieponice A, Maul TM, Cumer JM, Soletti L, Vorp DA. Mechanical stimulation induces morphological and phenotypic changes in bone marrow-derived progenitor cells within a three-dimensional fibrin matrix. J Biomed Mater Res A. 2007;81:523-530.
65. Nikolovski J, Kim BS, Mooney DJ. Cyclic strain inhibits switching of smooth muscle cells to an osteoblast-like phenotype. FASEB J. 2003;17:455-457.
66. Stegemann JP, Hong H, Nerem RM. Mechanical, biochemical, and extracellular matrix effects on vascular smooth muscle cell phenotype. J Appl Physiol (1985). 2005;98:2321-2327.
67. Shah N, Morsi Y, Manasseh R. From mechanical stimulation to biological pathways in the regulation of stem cell fate. Cell Biochem Funct. 2014;32:309-325.
68. Hu Y, Böck G, Wick G, Xu Q. Activation of PDGF receptor alpha in vascular smooth muscle cells by mechanical stress. FASEB J. 1998;12:1135-1142.
69. Li C, Xu Q. Mechanical stress-initiated signal transduction in vascular smooth muscle cells in vitro and in vivo. Cell Signal. 2007;19:881-891.
70. Kurpinski K, Chu J, Wang D, Li S. Proteomic Profiling of Mesenchymal Stem Cell Responses to Mechanical Strain and TGF-beta1. Cell Mol Bioeng. 2009;2:606-614.
71. Xiao Q, Wang G, Luo Z, Xu Q. The mechanism of stem cell differentiation into smooth muscle cells. Thromb Haemost. 2010;104:440-448.
72. Egusa H, Kobayashi M, Matsumoto T, Sasaki J, Uraguchi S, Yatani H. Application of cyclic strain for accelerated skeletal myogenic differentiation of mouse bone marrow-derived mesenchymal stromal cells with cell alignment. Tissue Eng Part A. 2013;19:770-782.
73. Margariti A, Winkler B, Karamariti E, Zampetaki A, Tsai TN, Baban D, Ragoussis J, Huang Y, Han JD, Zeng L, Hu Y, Xu Q. Direct reprogramming of fibroblasts into endothelial cells capable of angiogenesis and reendothelialization in tissue-engineered vessels. Proc Natl Acad Sci U S A. 2012;109:13793-13798.
74. Kim K, Doi A, Wen B, et al. Epigenetic memory in induced pluripotent stem cells. Nature. 2010;467:285-290.
75. Waugh J, Wagstaff AJ. The paclitaxel (TAXUS)-eluting stent: a review of its use in the management of de novo coronary artery lesions. Am J Cardiovasc Drugs. 2004;4:257-268.
76. Motovska Z, Knot J, Widimsky P. Stent thrombosis-risk assessment and prevention. Cardiovasc Ther. 2010;28:e92-100.
77. Wong MM, Winkler B, Karamariti E, Wang X, Yu B, Simpson R, Chen T, Margariti A, Xu Q. Sirolimus stimulates vascular stem/progenitor cell migration and differentiation into smooth muscle cells via epidermal growth factor receptor/extracellular signal-regulated kinase/β- catenin signaling pathway. Arterioscler Thromb Vasc Biol. 2013; 33:2397-2406.