Blood flow and stem cells in vascular disease

Cardiovascular Research

Volumn 99, Issue 2, 2013, Pages 251-259

  Zhang, Cheng ^a   Zeng, Lingfang ^b   Emanueli, Costanza ^c   Xu, Qingbo ^b  

^a SHANDONG UNIVERSITY   (China)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Restenosis; Shear stress; Stem cells; Vascular progenitors; Vascular tissue engineering

Indexed keywords

BLOOD FLOW; BLOOD VESSEL WALL; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYONIC STEM CELL; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; HEMATOPOIETIC STEM CELL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MECHANICAL STRESS; OSTEOBLAST; PRIORITY JOURNAL; PROTEOMICS; RESTENOSIS; REVIEW; SHEAR STRESS; STEM CELL; TISSUE ENGINEERING; VASCULAR DISEASE;

RESTENOSIS; SHEAR STRESS; STEM CELLS; VASCULAR PROGENITORS; VASCULAR TISSUE ENGINEERING;

ANIMALS; BIOMECHANICAL PHENOMENA; BLOOD VESSELS; CELL DIFFERENTIATION; CELL LINEAGE; CONSTRICTION, PATHOLOGIC; ENDOTHELIAL CELLS; HEMODYNAMICS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; REGIONAL BLOOD FLOW; STEM CELLS; STRESS, MECHANICAL; VASCULAR DISEASES;

EID: 84879915152     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt061     Document Type: Review

References (98)

1. Davies PF. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med 2009;6:16-26
2. Li YS, Haga JH, Chien S. Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 2005;38:1949-1971 (Pubitemid 41111740)
3. Lehoux S, Tedgui A. Signal transduction of mechanical stresses in the vascular wall. Hypertension 1998;32:338-345 (Pubitemid 28376494)
4. Li C, Xu Q. Mechanical stress-initiated signal transductions in vascular smooth muscle cells. Cell Signal 2000;12:435-445
5. Xu Q. Stem cells and transplant arteriosclerosis. Circ Res 2008;102:1011-1024 (Pubitemid 351667855)
6. Urbich C, Dimmeler S. Endothelial progenitor cells functional characterization. Trends Cardiovasc Med 2004;14:318-322 (Pubitemid 41110611)
7. Hirschi KK, Majesky MW. Smooth muscle stem cells. Anat Rec A Discov Mol Cell Evol Biol 2004;276:22-33 (Pubitemid 38063875)
8. Abedin M, Tintut Y, Demer LL. Mesenchymal stem cells and the artery wall. Circ Res 2004;95:671-676 (Pubitemid 39331926)
9. Aicher A, Zeiher AM, Dimmeler S. Mobilizing endothelial progenitor cells. Hypertension 2005;45:321-325 (Pubitemid 40315795)
10. Xu Q. Progenitor cells in vascular repair. Curr Opin Lipidol 2007;18:534-539 (Pubitemid 47462206)
11. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B et al. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-Deficient mice. J Clin Invest 2004;113:1258-1265 (Pubitemid 39069924)
12. Ergun S, Tilki D, Klein D. Vascular wall as a reservoir for different types of stem and progenitor cells. Antioxid Redox Signal 2011;15:981-985
13. Klein D, Weisshardt P, Kleff V, Jastrow H, Jakob HG, Ergun S. Vascular wall-resident CD44+ multipotent stem cells give rise to pericytes and smooth muscle cells and contribute to new vessel maturation. PLoS One 2011;6:e20540
14. Majesky MW, Dong XR, Hoglund V, Mahoney WM Jr, Daum G. The adventitia: A dynamic interface containing resident progenitor cells. Arterioscler Thromb Vasc Biol 2011;31:1530-1539
15. Zampetaki A, Kirton JP, Xu Q. Vascular repair by endothelial progenitor cells. Cardiovasc Res 2008;78:413-421 (Pubitemid 351769775)
16. Stary HC. Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. Arteriosclerosis 1989;9:I19-I32 (Pubitemid 19046963)
17. Ross R, Glomset JA. The pathogenesis of atherosclerosis (second of two parts). N Engl J Med 1976;295:420-425
18. Ross R, Glomset JA. The pathogenesis of atherosclerosis (first of two parts). N Engl J Med 1976;295:369-377
19. Ross R. Atherosclerosis -An inflammatory disease. N Engl J Med 1999;340:115-126
20. Ross R. The pathogenesis of atherosclerosis: A perspective for the 1990s. Nature 1993;362:801-809 (Pubitemid 23132154)
21. Sata M. Circulating vascular progenitor cells contribute to vascular repair, remodeling, and lesion formation. Trends Cardiovasc Med 2003;13:249-253 (Pubitemid 36960173)
22. Yokote K, Take A, Nakaseko C, Kobayashi K, Fujimoto M, Kawamura H et al. Bone marrow-Derived vascular cells in response to injury. J Atheroscler Thromb 2003;10: 205-210
23. Dimmeler S, Zeiher AM. Vascular repair by circulating endothelial progenitor cells: The missing link in atherosclerosis? J Mol Med 2004;82:671-677 (Pubitemid 39468491)
24. Hibbert B, Chen YX, O'Brien ER. c-kit-immunopositive vascular progenitor cells populate human coronary in-stent restenosis but not primary atherosclerotic lesions. Am J Physiol Heart Circ Physiol 2004;287:H518-H524 (Pubitemid 38955279)
25. Wassmann S, Werner N, Czech T, Nickenig G. Improvement of endothelial function by systemic transfusion of vascular progenitor cells. Circ Res 2006;99:e74-e83 (Pubitemid 44556373)
26. 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 (Pubitemid 351507474)
27. Ross R. The pathogenesis of atherosclerosis -An update. N Engl J Med 1986;314: 488-500
28. Hu Y, Davison F, Zhang Z, Xu Q. Endothelial replacement and angiogenesis in arteriosclerotic lesions of allografts are contributed by circulating progenitor cells. Circulation 2003;108:3122-3127 (Pubitemid 38031802)
29. Hu Y, Mayr M, Metzler B, Erdel M, Davison F, Xu Q. Both donor and recipient origins of smooth muscle cells in vein graft atherosclerotic lesions. Circ Res 2002;91:e13-e20
30. Invernici G, Emanueli C, Madeddu P, Cristini S, Gadau S, Benetti A et al. Human fetal aorta contains vascular progenitor cells capable of inducing vasculogenesis, angiogenesis, and myogenesis in vitro and in a murine model of peripheral ischemia. Am J Pathol 2007;170:1879-1892 (Pubitemid 47339262)
31. Sainz J, Al Haj Zen A, Caligiuri G, Demerens C, Urbain D, Lemitre M et al. Isolation of" side population" progenitor cells from healthy arteries of adult mice. Arterioscler Thromb Vasc Biol 2006;26:281-286 (Pubitemid 43732188)
32. Ingram DA, Mead LE, Moore DB, Woodard W, Fenoglio A, Yoder MC. Vessel wallderived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 2005;105:2783-2786 (Pubitemid 40446270)
33. 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 2011;31:842-855
34. Covas DT, Piccinato CE, Orellana MD, Siufi JLC, Silva JWA, Proto-Siqueira R et al. Mesenchymal stem cells can be obtained from the human saphena vein. Exp Cell Res 2005;309:340-344 (Pubitemid 41317357)
35. Pasquinelli G, Tazzari PL, Vaselli C, Foroni L, Buzzi M, Storci G et al. Thoracic aortas from multiorgan donors are suitable for obtaining resident angiogenic mesenchymal stromal cells. Stem Cells 2007;25:1627-1634 (Pubitemid 47121839)
36. Campagnolo P, Cesselli D, Al Haj Zen A, Beltrami AP, Krankel N, Katare R et al. Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation 2010;121:1735-1745
37. Tang Z, Wang A, Yuan F, Yan Z, Liu B, Chu JS et al. Differentiation of multipotent vascular stem cells contributes to vascular diseases. Nat Commun 2012;3:875
38. Nguyen AT, Gomez D, Bell RD, Campbell JH, Clowes AW, Gabbiani G et al. Smooth muscle cell plasticity: Fact or fiction? Circ Res 2013;112:17-22
39. Tang Z,Wang A,Wang D, Li S. Smooth muscle cells: To be or not to be? Response to Nguyen et al. Circ Res 2013;112:23-26
40. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008;3:301-313
41. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999;85:221-228 (Pubitemid 29377293)
42. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275:964-967 (Pubitemid 27087709)
43. Prokopi M, Pula G, Mayr U, Devue C, Gallagher J, Xiao Q et al. Proteomic analysis reveals presence of platelet microparticles in endothelial progenitor cell cultures. Blood 2009;114:723-732
44. Hirschi KK. Vascular precursors: Origin, regulation and function. Arterioscler Thromb Vasc Biol 2010;30:1078-1079
45. Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2008;28:1584-1595
46. Simper D, Stalboerger PG, Panetta CJ, Wang S, Caplice NM. Smooth muscle progenitor cells in human blood. Circulation 2002;106:1199-1204 (Pubitemid 34988636)
47. Sugiyama S, Kugiyama K, Nakamura S, Kataoka K, Aikawa M, Shimizu K et al. Characterization of smooth muscle-like cells in circulating human peripheral blood. Atherosclerosis 2006;187:351-362 (Pubitemid 43963015)
48. Deb A, Skelding KA,Wang S, Reeder M, Simper D, Caplice NM. Integrin profile and in vivo homing of human smooth muscle progenitor cells. Circulation 2004;110: 2673-2677 (Pubitemid 39453018)
49. Simper D, Mayr U, Urbich C, Zampetaki A, Prokopi M, Didangelos A et al. Comparative proteomics profiling reveals role of smooth muscle progenitors in extracellular matrix production. Arterioscler Thromb Vasc Biol 2010;30:1325-1332
50. Schwartz SM, Benditt EP. Aortic endothelial cell replication. I. Effects of age and hypertension in the rat. Circ Res 1977;41:248-255 (Pubitemid 8138734)
51. Xu Q. Biomechanical-stress-induced signaling and gene expression in the development of arteriosclerosis. Trends Cardiovasc Med 2000;10:35-41 (Pubitemid 32012679)
52. Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen MJ et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 2006;113:2744-2753 (Pubitemid 43947992)
53. Zeng L, Zampetaki A, Margariti A, Pepe AE, Alam S, Martin D et al. Sustained activation of XBP1 splicing leads to endothelial apoptosis and atherosclerosis development in response to disturbed flow. Proc Natl Acad Sci USA 2009;106:8326-8331
54. Xu Q. Disturbed flow-enhanced endothelial turnover in atherosclerosis. Trends Cardiovasc Med 2009;19:191-195
55. Sholley MM, Gimbrone MA Jr, Cotran RS. Cellular migration and replication in endothelial regeneration: A study using irradiated endothelial cultures. Lab Invest 1977;36: 18-25 (Pubitemid 8021267)
56. Torsney E, Xu Q. Resident vascular progenitor cells. J Mol Cell Cardiol 2011;50: 304-311
57. Pacilli A, Pasquinelli G. Vascular wall resident progenitor cells: A review. Exp Cell Res 2009;315:901-914
58. Zeng L, Xiao Q, Margariti A, Zhang Z, Zampetaki A, Patel S et al. HDAC3 is crucial in shear-And VEGF-induced stem cell differentiation toward endothelial cells. J Cell Biol 2006;174:1059-1069 (Pubitemid 44455193)
59. 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 2005;8:110-118 (Pubitemid 41139592)
60. Illi B, Scopece A, Nanni S, Farsetti A, Morgante L, Biglioli P et al. Epigenetic histone modification and cardiovascular lineage programming in mouse embryonic stem cells exposed to laminar shear stress. Circ Res 2005;96:501-508 (Pubitemid 40463458)
61. 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; 100:830-837 (Pubitemid 351914010)
62. Xiao Q, Zeng L, Zhang Z, Margariti A, Ali ZA, Channon KM et al. Sca-1+ progenitors derived from embryonic stem cells differentiate into endothelial cells capable of vascular repair after arterial injury. Arterioscler Thromb Vasc Biol 2006;26:2244-2251 (Pubitemid 44465718)
63. Yamamoto K, Sokabe T, Watabe T, Miyazono K, Yamashita JK, 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 2005;288:H1915-H1924 (Pubitemid 40418021)
64. Dong JD, Gu YQ, Li CM, Wang CR, Feng ZG, Qiu RX et al. Response of mesenchymal stem cells to shear stress in tissue-engineered vascular grafts. Acta Pharmacol Sin 2009;30:530-536
65. Kreke MR, Sharp LA, Lee YW, Goldstein AS. Effect of intermittent shear stress on mechanotransductive signaling and osteoblastic differentiation of bone marrow stromal cells. Tissue Eng Part A 2008;14:529-537 (Pubitemid 351520460)
66. Wang H, Riha GM, 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 2005;25:1817-1823 (Pubitemid 41243448)
67. Wang H, Li M, Lin PH, Yao Q, Chen C. Fluid shear stress regulates the expression of TGF-beta1 and its signaling molecules in mouse embryo mesenchymal progenitor cells. J Surg Res 2008;150:266-270
68. Obi S, Yamamoto K, Shimizu N, Kumagaya S, Masumura T, Sokabe T et al. Fluid shear stress induces arterial differentiation of endothelial progenitor cells. J Appl Physiol 2009;106:203-211
69. Daculsi R, Grellier M, Remy M, Bareille R, Pierron D, Fernandez P et al. Unusual transduction response of progenitor-Derived and mature endothelial cells exposed to laminar pulsatile shear stress. J Biomech 2008;41:2781-2785
70. 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
71. Sreerekha PR, Krishnan LK. Cultivation of endothelial progenitor cells on fibrin matrix and layering on dacron/polytetrafluoroethylene vascular grafts. Artif Organs 2006;30: 242-249
72. Rossig L, Urbich C, Bruhl T, Dernbach E, Heeschen C, Chavakis E 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 (Pubitemid 41002901)
73. Sho E, Sho M, Nanjo H, Kawamura K, Masuda H, Dalman RL. Hemodynamic regulation of CD34+ cell localization and differentiation in experimental aneurysms. Arterioscler Thromb Vasc Biol 2004;24:1916-1921 (Pubitemid 39350313)
74. Yamamoto K, Takahashi T, Asahara T, Ohura N, Sokabe T, Kamiya A et al. Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J Appl Physiol 2003;95:2081-2088 (Pubitemid 37310394)
75. DiMuzio P, Tulenko T. Tissue engineering applications to vascular bypass graft development: The use of adipose-Derived stem cells. J Vasc Surg 2007;45(Suppl. A): A99-103
76. Wu CC, Chao YC, Chen CN, Chien S, Chen YC, Chien CC et al. Synergism of biochemical and mechanical stimuli in the differentiation of human placenta-Derived multipotent cells into endothelial cells. J Biomech 2008;41:813-821
77. Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T et al. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 2000; 408:92-96
78. Gerecht-Nir S, Ziskind A, Cohen S, Itskovitz-Eldor J. Human embryonic stem cells as an in vitro model for human vascular development and the induction of vascular differentiation. Lab Invest 2003;83:1811-1820 (Pubitemid 38018544)
79. Liu LT, Chang HC, Chiang LC, Hung WC. Histone deacetylase inhibitor up-regulates RECK to inhibit MMP-2 activation and cancer cell invasion. Cancer Res 2003;63: 3069-3072
80. Sawa H, Murakami H, Ohshima Y, Murakami M, Yamazaki I, Tamura Y et al. Histone deacetylase inhibitors such as sodium butyrate and trichostatin A inhibit vascular endothelial growth factor (VEGF) secretion from human glioblastoma cells. Brain Tumor Pathol 2002;19:77-81 (Pubitemid 36356314)
81. 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 (Pubitemid 46436444)
82. Riha GM,Wang X,Wang H, Chai H, Mu H, Lin PH et al. Cyclic strain induces vascular smooth muscle cell differentiation from murine embryonic mesenchymal progenitor cells. Surgery 2007;141:394-402 (Pubitemid 46356436)
83. Shimizu N, Yamamoto K, Obi S, Kumagaya S, Masumura T, Shimano Y et al. Cyclic strain induces mouse embryonic stem cell differentiation into vascular smooth muscle cells by activating PDGF receptor beta. J Appl Physiol 2008;104:766-772 (Pubitemid 351468806)
84. Gwak SJ, Bhang SH, Kim IK, Kim SS, Cho SW, Jeon O et al. The effect of cyclic strain on embryonic stem cell-Derived cardiomyocytes. Biomaterials 2008;29:844-856 (Pubitemid 350266049)
85. Tsai TN, Kirton JP, Campagnolo P, Zhang L, Xiao Q, Zhang Z et al. Contribution of stem cells to neointimal formation of decellularized vessel grafts in a novel mouse model. Am J Pathol 2012;181:362-373
86. Margariti A, Winkler B, Karamariti E, Zampetaki A, Tsai TN, Baban D et al. Direct reprogramming of fibroblasts into endothelial cells capable of angiogenesis and reendothelialization in tissue-engineered vessels. Proc Natl Acad Sci USA 2012;109: 13793-13798
87. Rajagopal V, Rockson SG. Coronary restenosis: A review of mechanisms and management. Am J Med 2003;115:547-553 (Pubitemid 37352801)
88. Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci 2000;902: 230-239. Discussion 239-240
89. Rotmans JI, Heyligers JM, Verhagen HJ, Velema E, Nagtegaal MM, de Kleijn DP et al. In vivo cell seeding with anti-CD34 antibodies successfully accelerates endothelialization but stimulates intimal hyperplasia in porcine arteriovenous expanded polytetrafluoroethylene grafts. Circulation 2005;112:12-18 (Pubitemid 40962563)
90. Aoki J, Serruys PW, van Beusekom H, Ong AT, McFadden EP, Sianos G et al. Endothelial progenitor cell capture by stents coated with antibody against CD34: The HEALING-FIM (Healthy Endothelial Accelerated Lining Inhibits Neointimal Growth-First in Man) Registry. J Am Coll Cardiol 2005;45:1574-1579 (Pubitemid 40704488)
91. Kang HJ, Kim HS, Zhang SY, Park KW, Cho HJ, Koo BK et al. Effects of intracoronary infusion of peripheral blood stem-cells mobilised with granulocyte-colony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: The MAGIC cell randomised clinical trial. Lancet 2004;363: 751-756
92. Alessandri G, Girelli M, Taccagni G, Colombo A, Nicosia R, Caruso A et al. Human vasculogenesis ex vivo: Embryonal aorta as a tool for isolation of endothelial cell progenitors. Lab Invest 2001;81:875-885 (Pubitemid 32553408)
93. Howson KM, Aplin AC, Gelati M, Alessandri G, Parati EA, Nicosia RF. The postnatal rat aorta contains pericyte progenitor cells that form spheroidal colonies in suspension culture. Am J Physiol Cell Physiol 2005;289:C1396-C1407 (Pubitemid 41636345)
94. Zengin E, Chalajour F, Gehling UM, Ito WD, Treede H, Lauke H et al. Vascular wall resident progenitor cells: A source for postnatal vasculogenesis. Development 2006; 133:1543-1551 (Pubitemid 43732967)
95. Hoshino A, Chiba H, Nagai K, Ishii G, Ochiai A. Human vascular adventitial fibroblasts contain mesenchymal stem/progenitor cells. Biochem Biophys Res Commun 2008;368: 305-310
96. Passman JN, Dong XR, Wu SP, Maguire CT, Hogan KA, Bautch VL et al. A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proc Natl Acad Sci USA 2008;105:9349-9354
97. Liu C, Wang S, Metharom P, Caplice NM. Myeloid lineage of human endothelial outgrowth cells circulating in blood and vasculogenic endothelial-like cells in the diseased vessel wall. J Vasc Res 2009;46:581-591
98. Fang B, Li Y, Song Y, Li N. Isolation and characterization of multipotent progenitor cells from the human fetal aorta wall. Exp Biol Med 2010;235:130-138