Effects of shear stress on endothelial progenitor cells

Journal of Biomedical Nanotechnology

Volumn 10, Issue 10, 2014, Pages 2586-2597

  Obi, Syotaro ^a   Yamamoto, Kimiko ^b   Ando, Joji ^c  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c DOKKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Differentiation; Endothelial progenitor cells; Mechanical force; Mechanotransduction

Indexed keywords

BLOOD VESSELS; CELL DEATH; DIFFERENTIATION (CALCULUS); ENDOTHELIAL CELLS; GENE EXPRESSION; PHYSIOLOGICAL MODELS; SHEAR STRESS; STEM CELLS; TISSUE;

ANGIOGENESIS; BIOACTIVE SUBSTANCES; ENDOTHELIAL PROGENITOR CELLS; ENDOTHELIAL PROGENITOR CELLS (EPCS); MECHANICAL FORCE; MECHANOTRANSDUCTION; NEO-VASCULARIZATION; REGENERATIVE MEDICINE;

LOADING;

ANTICOAGULANT AGENT; CD133 ANTIGEN; CD34 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR SP1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; APOPTOSIS; ARTIFICIAL ORGAN; BLOOD VESSEL; CELL ADHESION; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL TRIAL (TOPIC); DNA FLANKING REGION; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; FLUID FLOW; FORCE; HEMATOPOIETIC STEM CELL; HUMAN; MECHANOTRANSDUCTION; MONOCYTE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PROMOTER REGION; REGENERATIVE MEDICINE; REVIEW; SHEAR STRESS; STEM CELL TRANSPLANTATION; STENT; TISSUE REGENERATION; TRANSCRIPTION INITIATION SITE; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; MECHANICAL STRESS; PHYSIOLOGY; SHEAR STRENGTH;

ANIMALS; CLINICAL TRIALS AS TOPIC; ENDOTHELIAL PROGENITOR CELLS; GENE EXPRESSION REGULATION; HUMANS; MECHANOTRANSDUCTION, CELLULAR; SHEAR STRENGTH; STRESS, MECHANICAL;

EID: 84905653351     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2014.2014     Document Type: Review

References (79)

1. J. Ando and K. Yamamoto, Flow detection and calcium signalling in vascular endothelial cells. Cardiovasc. Res. 99, 260 (2013).
2. A. M. Nixon, M. Gunel, and B. E. Sumpio, The critical role of hemodynamics in the development of cerebral vascular disease. J. Neurosurg. 112, 1240 (2010).
3. F. Gijsen, A. van der Giessen, A. van der Steen, and J. Wentzel, Shear stress and advanced atherosclerosis in human coronary arteries. J. Biomech. 46, 240 (2013).
4. T. Asahara, T. Murohara, A. Sullivan, M. Silver, R. Zee, T. Li, B. Witzenbichler, G. Schatteman, and J. M. Isner, Isolation of putative progenitor endothelial cells for angiogenesis. Science 275, 964 (1997).
5. K. Jujo, M. Ii, and D. W. Losordo, Endothelial progenitor cells in neovascularization of infarcted myocardium. J. Mol. Cell. Cardiol. 45, 530 (2008).
6. T. Asahara, H. Masuda, T. Takahashi, C. Kalka, C. Pastore, M. Silver, M. Kearne, M. Magner, and J. M. Isner, Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 85, 221 (1999).
7. T. Asahara, A. Kawamoto, and H. Masuda, Circulating endothelial progenitor cells for vascular medicine. Stem Cells 29, 1650 (2011).
8. M. B. Grant, W. S. May, S. Caballero, G. A. Brown, S. M. Guthrie, R. N. Mames, B. J. Byrne, T. Vaught, P. E. Spoerri, A. B. Peck, and E. W. Scott, Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat. Med. 8, 607 (2002).
9. R. Gulati, D. Jevremovic, T. E. Peterson, S. Chatterjee, V. Shah, R. G. Vile, and R. D. Simari, Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circ. Res. 93, 1023(2003).
10. Y. Lin, D. J. Weisdorf, A. Solovery, and R. P. Hebbel, Origins of circulating endothelial cells and endothelial outgrowth from blood. J. Clin. Invest. 105, 71 (2000).
11. A. Aicher, M. Rentsch, K. Sasaki, J. W. Ellwart, F. Fändrich, R. Siebert, J. P. Cooke, S. Dimmeler, and C. Heeschen, Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circ. Res. 100, 581 (2007).
12. W. His, Lecithoblast und angioblast der wirbelthiere, BG Teubner, Leipzig (1900).
13. P. Murray, The development in vitro of the blood of the early chick embryo. Proc. Royal Soc. London 111, 497 (1932).
14. M. C. Yoder, Defining human endothelial progenitor cells. J. Thromb. Haemost. Suppl. 1, 49 (2009).
15. F. Timmermans, J. Plum, M. C. Yoder, D. A. Ingram, B. Vandekerckhove, and J. Case, Endothelial progenitor cells: Identity defined? J. Cell. Mol. Med. 13, 87 (2009).
16. H. Masuda, C. Alev, H. Akimaru, R. Ito, T. Shizuno, M. Kobori, M. Horii, T. Ishihara, K. Isobe, M. Isozaki, J. Itoh, Y. Itoh, Y. Okada, B. A. McIntyre, S. Kato, and T. Asahara, Methodological development of a clonogenic assay to determine endothelial progenitor cell potential. Circ. Res. 109, 20 (2011).
17. D. A. Ingram, L. E. Mead, H. Tanaka, V. Meade, A. Fenoglio, K. Mortell, K. Pollok, M. J. Ferkowicz, D. Gilley, and M. C. Yoder, Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104, 2752 (2004).
18. J. Hur, C. H. Yoon, H. S. Kim, J. H. Choi, H. J. Kang, K. K. Hwang, B. H. Oh, M. M. Lee, and Y. B. Park, Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler. Thromb. Vasc. Biol. 24, 288 (2004).
19. C. Kalka, H. Masuda, T. Takahashi, W. M. Kalka-Moll, M. Silver, M. Kearney, T. Li, J. M. Isner, and T. Asahara, Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc. Natl. Acad. Sci. USA 97, 3422 (2000).
20. A. Kawamoto, H. C. Gwon, H. Iwaguro, J. I. Yamaguchi, S. Uchida, H. Masuda, M. Silver, H. Ma, M. Kearney, J. M. Isner, and T. Asahara, Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103, 634 (2001).
21. T. Murohara, H. Ikeda, J. Duan, S. Shintani, K. Sasaki, H. Eguchi, I. Onitsuka, K. Matsui, and T. Imaizumi, Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J. Clin. Invest. 105, 1527 (2000).
22. G. C. Schatterman, H. D. Hanlon, C. Jiao, S. G. Dodds, and B. A. Christy, Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J. Clin. Invest. 106, 571 (2000).
23. A. A. Kocher, M. D. Schuster, M. J. Szabolcs, S. Takuma, D. Burkhoff, J. Wang, S. Homma, N. M. Edwards, and S. Itescu, Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat. Med. 7, 430 (2001).
24. R. K. Burt, A. Testori, Y. Oyama, H. E. Rodriguez, K. Yaung, M. Villa, J. M. Bucha, F. Milanetti, J. Sheehan, N. Rajamannan, and W. H. Y. Pearce, Autologous peripheral blood CD133+ cell implantation for limb salvage in patients with critical limb ischemia. Bone Marrow Transplant. 45, 111 (2010).
25. A. Kawamoto, M. Katayama, N. Handa, M. Kinoshita, H. Takano, M. Horii, K. Sadamoto, A. Yokoyama, T. Yamanaka, R. Onodera, A. Kuroda, R. Baba, Y. Kaneko, T. Tsukie, Y. Kurimoto, Y. Okada, Y. Kihara, S. Morioka, M. Fukushima, and T. Asahara, Intramuscular transplantation of G-CSF-mobilized CD34(+) cells in patients with critical limb ischemia: a phase I/IIa, multicenter, single-blinded, dose-escalation clinical trial. Stem Cells 27, 2857 (2009).
26. J. Bartunek, M. Vanderheyden, B. Vandekerckhove, S. Mansour, B. De Bruyne, P. De Bondt, I. Van Haute, N. Lootens, G. Heyndrickx, and W. Wijns, Intracoronary injection of CD133-positive enriched bone marrow progenitor cells promotes cardiac recovery after recent myocardial infarction: Feasibility and safety. Circulation 112, 178 (2005).
27. Z. Q. Li, M. Zhang, Y. Z. Jing, W. W. Zhang, Y. Liu, L. J. Cui, L. Yuan, X. Z. Liu, X. Yu, and T. S. Hu, The clinical study of autologous peripheral blood stem cell transplantation by intracoronary infusion in patients with acute myocardial infarction (AMI). Int. J. Cardiol. 115, 52 (2007).
28. C. Stamm, B. Westphal, H. D. Kleine, M. Petzsch, C. Kittner, H. Klinge, C. Schümichen, C. A. Nienaber, M. Freund, and G. Steinhoff, Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 361, 45 (2003).
29. D. W. Losordo, R. A. Schatz, C. J. White, J. E. Udelson, V. Veereshwarayya, M. Durgin, K. K. Poh, R. Weinstein, M. Kearney, M. Chaudhry, A. Burg, L. Eaton, L. Heyd, T. Thorne, L. Shturman, P. Hoffmeister, K. Story, V. Zak, D. Dowling, J. H. Traverse, R. E. Olson, J. Flanagan, D. Sodano, T. Murayama, A. Kawamoto, K. F. Kusano, J. Wollins, F. Welt, P. Shah, P. Soukas, T. Asahara, and T. D. Henry, Intramyocardial transplantation of autologous CD34+ stem cells for intractable angina: A phase I/IIa double-blind, randomized controlled trial. Circulation 115, 3165 (2007).
30. P. F. Davis, Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75, 519 (1995).
31. A. Kamiya, R. Bukhari, and T. Togawa, Adaptive regulation of wall shear stress optimizing vascular tree function. Bull. Math. Biol. 46, 127 (1984).
32. D. M. Wang and J. M. Tarbell, Modeling interstitial flow in an artery wall allows estimation of wall shear stress on smooth muscle cells. J. Biomech. Eng. 117, 358 (1995).
33. M. H. Kroll, J. D. Hellums, L. V. McIntire, A. I. Schafer, and J. L. Moake, Platelets and shear stress. Blood 88, 1525 (1996).
34. S. R. Bussolari, C. F. Dewey Jr, and M. A. Gimbrone Jr, Apparatus for subjecting living cells to fluid shear stress. Rev. Sci. Instrum. 53, 1851 (1982).
35. B. N. Nanjappa, H. K. Chang, and C. A. Glomski, Trauma of the erythrocyte membrane associated with low shear stress. Biophys. J. 13, 1212 (1973).
36. N. A. Stathopoulos, and J. D. Hellums, Shear stress effects on human embryonic kidney cells in Vitro. Biotechnol. Bioeng. 27, 1021 (1985).
37. J. E. Jr. Moore, E. Bürki, A. Suciu, S. Zhao, M. Burnier, H. R. Brunner, and J. J. Meister, A device for subjecting vascular endothelial cells to both fluid shear stress and circumferential cyclic stretch. Ann. Biomed. Eng. 22, 416 (1994).
38. S. Takayama, E. Ostuni, P. LeDuc, K. Naruse, D. E. Ingber, and G. M. Whitesides, Subcellular positioning of small molecules. Nature 411, 1016 (2001).
39. K. Yamamoto, T. Takahashi, T. Asahara, N. Ohura, T. Sokabe, A. Kamiya, and J. Ando, Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J. Appl. Physiol. 95, 2081 (2003).
40. K. A. Ahmann, S. L. Johnson, R. P. Hebbel, and R. T. Tranquillo, Shear stress responses of adult blood outgrowth endothelial cells seeded on bioartificial tissue. Tissue Eng. Part A 17, 2511 (2011).
41. M. Koga, R. Sudo, Y. Abe, K. Yamomoto, J. Ando, M. Ikeda, and K. Tanishita, Contribution of rat endothelial progenitor cells on three-dementional network formation in vitro. Tissue Eng. 15, 2727 (2009).
42. S. Obi, H. Masuda, T. Shizuno, A. Sato, K. Yamamoto, J. Ando, Y. Abe, and T. Asahara, Fluid shear stress induces differentiation of circulating phenotype endothelial progenitor cells. Am. J. Physiol. Cell Physiol. 303, 595 (2012).
43. J. Tao, Z. Yang, J. M. Wang, L. C. Wang, C. F. Luo, A. L. Tang, Y. G. Dong, and H. Ma, Shear stress increases Cu/Zn SOD activity and mRNA expression in human endothelial progenitor cells. J. Hum. Hypertens. 21, 353 (2007).
44. M. G. Angelos, M. A. Brown, L. L. Satterwhite, V. W. Levering, N. T. Shaked, and G. A. Truskey, Dynamic adhesion of umbilical cord blood endothelial progenitor cells under laminar shear stress. Biophy., J 99, 3545 (2010).
45. A. Peled, V. Grabovsky, L. Habler, J. Sandbank, F. Arenzana-Seisdedos, I. Petit, H. Ben-Hur, T. Lapidot, and R. Alon, The chemokine SDF stimulates integrin-mediated arrest of CD34+ cells on vascular endothelium under shear flow. J. Clin. Invest. 104, 1199 (1999).
46. K. D. Puri, S. Chen, and T. A. Springer, Modifying the mechanical property and shear threshold of L-selectin adhesion independently of equilibrium properties. Nature 392, 930 (1998).
47. Z. Yang, W. H. Xia, Y. Y. Zhang, S. Y. Xu, X. Liu, X. Y. Zhang, B. B. Yu, Y. X. Qiu, and J. Tao, Shear stress-induced activation of Tie2-dependent signaling pathway enhances reendothelialization capacity of early endothelial progenitor cells. J. Mol. Cell Cardiol. 52, 1155 (2012).
48. J. Tao, Z. Yang, J. M. Wang, C. Tu, and S. R. Pan, Effects of fluid shear stress on eNOS mRNA expression and NO production in human endothelial progenitor cells. Cardiology 106, 82 (2006).
49. M. A. Brown, C. S. Wallace, M. Angelos, and G. A. Truskey, Characterization of umbilical cord blood-derived late outgrowth endothelial progenitor cells exposed to laminar shear stress. Tissue Eng. Part A 15, 3575 (2009).
50. Z. Yang, J. M. Wang, L. C. Wang, L. Chen, C. Tu, C. F. Luo, A. L. Tang, S. M. Wang, and J. Tao, In vitro shear stress modulates antithrombogenic potentials of human endothelial progenitor cells. J. Thromb. Thrombolysis 23, 121 (2007).
51. A. D. Egorova, M. C. DeRuiter, H. C. de Boer, S. van de Pas, A. C. Gittenberger-de Groot, A. J. van Zonneveld, R. E. Poelmann, and B. P. Hierck, Endothelial colony-forming cells show a mature transcriptional response to shear stress. In Vitro Cell Dev. Biol. Anim. 48, 21 (2012).
52. T. Lund, S. E. Hermansen, T. V. Andreasen, J. O. Olsen, B. Østerud, T. Myrmel, and K. Ytrehus, Shear stress regulates inflammatory and thrombogenic gene transcripts in cultured human endothelial progenitor cells. Thromb. Haemost. 104, 582 (2010).
53. Z. Yang, J. Tao, J. M. Wang, C. Tu, M. G. Xu, Y. Wang, and S. R. Pan, Shear stress contributes to t-PA mRNA expression in human endothelial progenitor cells and nonthrombogenic potential of small diameter artificial vessels. Biochem. Biophys. Res. Commun. 342, 577 (2006).
54. L. Rössig, C. Urbich, T. Brühl, E. Dernbach, C. Heeschen, E. Chavakis, K. Sasaki, D. Aicher, F. Diehl, F. Seeger, M. Potente, A. Aicher, L. Zanetta, E. Dejana, A. M. Zeiher, and S. Dimmeler, Histone deacetylase activity is essential for the expression of HoxA9 and for endothelial commitment of progenitor cells. J. Exp. Med. 201, 1825 (2005).
55. B. B. Cheng, Z. Q. Yan, Q. P. Yao, B. R. Shen, J. Y. Wang, L. Z. Gao, Y. Q. Li, H. T. Yuan, Y. X. Qi, and Z. L. Jiang, Association of SIRT1 expression with shear stress induced endothelial progenitor cell differentiation. J. Cell. Biochem. 113, 3663 (2012).
56. S. Obi, K. Yamamoto, N. Shimizu, S. Kumagaya, T. Masumura, T. Sokabe, T. Asahara, and J. Ando, Fluid shear stress induces arterial differentiation of endothelial progenitor cells. J. Appl. Physiol. 106, 203 (2009).
57. W. H. Xia, Z. Yang, S. Y. Xu, L. Chen, X. Y. Zhang, J. Li, X. Liu, Y. X. Qiu, X. T. Shuai, and J. Tao, Age-related decline in reendothelialization capacity of human endothelial progenitor cells is restored by shear stress. Hypertension 59, 1225 (2012).
58. R. Daculsi, M. Grellier, M. Rémy, R. Bareille, D. Pierron, P. Fernandez, and L. Bordenave, Unusual transduction response of progenitor-derived and mature endothelial cells exposed to laminar pulsatile shear stress. J. Biomech. 41, 2781 (2008).
59. R. A. Boon, C. Urbich, A. Fischer, R. D. Fontijn, F. H. Seeger, M. Koyanagi, A. J. Horrevoets, and S. Dimmeler, Kruppel-like factor 2 improves neovascularization capacity of aged proangiogenic cells. Eur. Heart J. 32, 371 (2011).
60. M. Cheng, X. Guan, H. Li, X. Cui, X. Zhang, X. Li, X. Jing, H. Wu, and E. Avsar, Shear stress regulates late EPC differentiation via mechanosensitive molecule-mediated cytoskeletal rearrangement. PLoS One 8, e67675 (2013).
61. L. Zeng, Q. Xiao, A. Margariti, Z. Zhang, A. Zampetaki, S. Patel, M. C. Capogrossi, Y. Hu, and Q. Xu, HDAC3 is crucial in shearand VEGF-induced stem cell differentiation toward endothelial cells. J. Cell. Biol. 174, 1059 (2006).
62. C. Ye, L. Bai, Y Z. Q. An, Y. H. Wang, and Z. L. Jiang, Shear stress and vascular smooth muscle cells promote endothelial differentiation of endothelial progenitor cells via activation of Akt. Clin. Biomech. 23, 118 (2008).
63. Y. Suzuki, K. Yamamoto, J. Ando, K. Matsumoto, and T. Matsuda, Arterial shear stress augments the differentiation of endothelial progenitor cells adhered to VEGF-bound surfaces. Biochem. Biophys. Res. Commun. 423, 91 (2012).
64. M. Avci-Adali, N. Perle, G. Ziemer, and H. P. Wendel, Current concepts and new developments for autologous in vivo endothelialisation of biomaterials for intravascular applications. Eur. Cell Mater. 21, 157 (2011).
65. J. Aoki, P. W. Serruys, H. van Beusekom, A. T. Ong, E. P. McFadden, G. Sianos, W. J. van der Giessen, E. Regar, P. J. de Feyter, H. R. Davis, S. Rowland, and M. J. Kutryk, 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. 45, 1574 (2005).
66. H. F. Langer, J. W. von der Ruhr, K. Daub, T. Schoenberger, K. Stellos, A. E. May, H. Schnell, A. Gauss, R. Hafner, P. Lang, M. Schumm, H. J. Buhring, K. Klingel, S. Conrad, M. Schaller, M. van Zandvoort, G. Jung, S. Dimmeler, T. Skutella, and M. Gawaz, Capture of endothelial progenitor cells by a bispecific protein/monoclonal antibody molecule induces reendothelialization of vascular lesions. J. Mol. Med. 88, 687 (2010).
67. W. H. Lim, W. W. Seo, W. Choe, C. K. Kang, J. Park, H. J. Cho, S. Kyeong, J. Hur, H. M. Yang, H. J. Cho, Y. S. Lee, and H. S. Kim, Stent coated with antibody against vascular endothelial-cadherin captures endothelial progenitor cells, accelerates re-endothelialization, and reduces neointimal formation. Arterioscler. Thromb. Vasc. Biol. 31, 2798 (2011).
68. J. Hoffmann, A. Paul, M. Harwardt, J. Groll, T. Reeswinkel, D. Klee, M. Moeller, H. Fischer, T. Walker, T. Greiner, G. Ziemer, and H. P. Wendel, Immobilized DNA aptamers used as potent attractors for porcine endothelial precursor cells. J. Biomed. Mater. Res. A 84, 614 (2008).
69. R. Blindt, F. Vogt, I. Astafieva, C. Fach, M. Hristov, N. Krott, B. Seitz, A. Kapurniotu, C. Kwok, M. Dewor, A. K. Bosserhoff, J. Bernhagen, P. Hanrath, R. Hoffmann, and C. Weber, A novel drug-eluting stent coated with an integrin-binding cyclic Arg-Gly-Asp peptide inhibits neointimal hyperplasia by recruiting endothelial progenitor cells. J. Am. Coll. Cardiol. 47, 1786 (2006).
70. N. Swanson, K. Hogrefe, Q. Javed, N. Malik, and A. H. Gershlick, Vascular endothelial growth factor (VEGF)-eluting stents: In vivo effects on thrombosis, endothelialization and intimal hyperplasia. J. Invasive Cardiol. 15, 688 (2003).
71. J. C. Wojciechowski, S. D. Narasipura, N. Charles, D. Mickelsen, K. Rana, M. L. Blair, and M. R. King, Capture and enrichment of CD34-positive haematopoietic stem and progenitor cells from blood circulation using P-selectin in an implantable device. Br. J. Haematol. 140, 673 (2008).
72. E. J. Suuronen, P. Zhang, D. Kuraitis, X. Cao, A. Melhuish, D. McKee, F. Li, T. G. Mesana, J. P. Veinot, and M. Ruel, An acellular matrix-bound ligand enhances the mobilization, recruitment and therapeutic effects of circulating progenitor cells in a hindlimb ischemia model. FASEB J. 23, 1447 (2009).
73. P. M. Consigny, D. A. Silverberg, and N. J. Vitali, Use of endothelial cells containing superparamagnetic microspheres to improve endothelial cell delivery to arterial surfaces after angioplasty. J. Vasc. Interv. Radiol. 10, 155 (1999).
74. T. Shirota, H. He, H. Yasui, and T. Matsuda, Human endothelial progenitor cell-seeded hybrid graft: proliferative and antithrombogenic potentials in vitro and fabrication processing. Tissue Eng. 9, 127 (2003).
75. H. E. Achneck, R. M. Jamiolkowski, A. E. Jantzen, J. M. Haseltine, W. O. Lane, J. K. Huang, L. J. Galinat, M. J. Serpe, F. H. Lin, M. Li, A. Parikh, L. Ma, T. Chen, B. Sileshi, C. A. Milano, C. S. Wallace, T. V. Stabler, J. D. Allen, G. A. Truskey, and J. H. Lawson, The biocompatibility of titanium cardiovascular devices seeded with autologous blood-derived endothelial progenitor cells: EPC-seeded antithrombotic Ti implants. Biomaterials 32, 10 (2011).
76. D. Kawahara and T. Matsuda, Hydrodynamic shear-stress-dependent retention of endothelial and endothelial progenitor cells adhered to vascular endothelial growth factor-fixed surfaces. J. Biomed. Mater. Res. B Appl. Biomater. 100, 1218 (2012).
77. W. J. Seeto, Y. Tian, and E. A. Lipke, Peptide-grafted poly(ethylene glycol) hydrogels support dynamic adhesion of endothelial progenitor cells. Acta. Biomater. 9, 8279 (2013).
78. B. D. Plouffe, T. Kniazeva, J. E. Jr. Mayer, S. K. Murthy, and V. L. Sales, Development of microfluidics as endothelial progenitor cell capture technology for cardiovascular tissue engineering and diagnostic medicine. FASEB J. 23, 3309 (2009).
79. A. M. Leone, M. Valgimigli, M. B. Giannico, V. Zaccone, M. Perfetti, D. D'Amario, A. G. Rebuzzi, and F. Crea, From bone marrow to the arterial wall: The ongoing tale of endothelial progenitor cells. Eur. Heart J. 30, 890 (2009).