Engineering blood vessels using stem cells: Innovative approaches to treat vascular disorders

Expert Review of Cardiovascular Therapy

Volumn 8, Issue 10, 2010, Pages 1433-1445

  Kusuma, Sravanti ^a,b   Gerecht, Sharon ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b Johns Hopkins University   (United States)

Author keywords

biomimetic scaffolds; cellular therapies; stem cells; tissue engineering; vascular cells; vascular disease

Indexed keywords

ADULT STEM CELL; BIOMIMETICS; BLOOD VESSEL; CELL DIFFERENTIATION; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; HUMAN; IN VITRO STUDY; MESENCHYMAL STEM CELL; PLURIPOTENT STEM CELL; REGENERATION; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; VASCULAR DISEASE;

ANIMALS; BLOOD VESSEL PROSTHESIS; CELL DIFFERENTIATION; CLINICAL TRIALS AS TOPIC; HUMANS; REGENERATION; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TISSUE SCAFFOLDS; VASCULAR DISEASES;

EID: 77958109974     PISSN: 14779072     EISSN: 17448344     Source Type: Journal    
DOI: 10.1586/erc.10.121     Document Type: Review

References (114)

1. Sun GM, Gerecht S. Vascular regeneration: engineering the stem cell microenvironment. Regen. Med. 4(3), 435-447 (2009).
2. Asahara T, Masuda H, Takahashi T et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 85(3), 221-228 (1999).
3. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res. 87(10), 840-844 (2000).
4. Ross R. Atherosclerosis-an infammatory disease. N. Engl. J. Med. 340(2), 115-126 (1999).
5. Devanesan AJ, Laughlan KA, Girn HRS, Homer-Vanniasinkam S. Endothelial progenitor cells as a therapeutic option in peripheral arterial disease. Eur. J. Vasc. Endovasc. Surg. 38(4), 475-481 (2009).
6. Al Mheid I, Quyyumi AA. Cell therapy in peripheral arterial disease. Angiology 59(6), 705-716 (2009).
7. Pacilli A, Faggioli G, Stella A, Pasquinelli G. An update on therapeutic angiogenesis for peripheral vascular disease. Ann. Vasc. Surg. 24(2), 258-268 (2010).
8. Korbling M, Estrov Z. Adult stem cells for tissue repair-a new therapeutic concept? N. Engl. J. Med. 349(6), 570-582 (2003).
9. Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19(3), 180-192 (2001).
10. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 284(5411), 143-147 (1999).
11. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ. Res. 95(1), 9-20 (2004).
12. Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 6(2), 230-247 (1968).
13. Caplan AI. Why are MSCs therapeutic? New data: new insight. J. Pathol. 217(2), 318-324 (2009).
14. Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative ana lysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24(5), 1294-1301 (2006).
15. Pasquinelli G, Tazzari PL, Vaselli C et al. Thoracic aortas from multiorgan donors are suitable for obtaining resident angiogenic mesenchymal stromal cells. Stem Cells 25(7), 1627-1634 (2007).
16. Pasquinelli G, Pacilli A, Alviano F et al. Multidistrict human mesenchymal vascular cells: pluripotency and stemness characteristics. Cytotherapy 12(3), 275-287 (2010).
17. Parolini O, Alviano F, Bagnara GP et al. Concise review: isolation and characterization of cells from human term placenta: outcome of the First International Workshop on Placenta Derived Stem Cells. Stem Cells 26(2), 300-311 (2008).
18. Nan W, Linlin M, Zhen Z et al. Regeneration of smooth muscle cells from bone marrow: use of mesenchymal stem cells for tissue engineering and cellular therapeutics. Presented at: 3rd International Conference on Bioinformatics and Biomedical Engineering, iCBBE. Beijing, China, 11-13 June 2009.
19. Kinner B, Zaleskas JM, Spector M. Regulation of smooth muscle actin expression and contraction in adult human mesenchymal stem cells. Exp. Cell Res. 278(1), 72-83 (2002).
20. Hirschi KK, Rohovsky SA, D'Amore PA. PDGF, TGF-β, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J. Cell Biol. 141(3), 805-814 (1998).
21. Ball SG, Shuttleworth AC, Kielty CM. Direct cell contact infuences bone marrow mesenchymal stem cell fate. Int. J. Biochem. Cell Biol. 36(4), 714-727 (2004).
22. Dong JD, Gu YQ, Li CM et al. Response of mesenchymal stem cells to shear stress in tissue-engineered vascular grafts. Acta Pharmacol. Sinica 30(5), 530-536 (2009).
23. Joachim O, Sabine B, Birgitte J et al Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22(3), 377-384 (2004).
24. Matsumoto R, Omura T, Yoshiyama M et al. Vascular endothelial growth factor-expressing mesenchymal stem cell transplantation for the treatment of acute myocardial infarction. Arterioscler. Thromb. Vasc. Biol. 25(6), 1168-1173 (2005).
25. Kurpinski K, Lam H, Chu J et al. Transforming growth factor-β and notch signaling mediate stem cell differentiation into smooth muscle cells. Stem Cells 28(4), 734-742 (2010).
26. Asahara T, Murohara T, Sullivan A et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302), 964-966 (1997).
27. Takahashi T, Kalka C, Masuda H et al. Ischemia-and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 5(4), 434-438 (1999).
28. Hill JM, Zalos G, Halcox JPJ et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N. Engl. J. Med. 348(7), 593-600 (2003).
29. Mead LE, Prater D, Yoder MC, Ingram DA. Isolation and characterization of endothelial progenitor cells from human blood. Curr. Protoc. Stem Cell Biol. Chapter 2, Unit 2C.1 (2008).
30. Broxmeyer HE, Srour E, Orschell C et al. Cord blood stem and progenitor cells. Methods Enzymol. 439-473 (2006).
31. Javed MJ, Mead LE, Prater D et al. Endothelial colony forming cells and mesenchymal stem cells are enriched at different gestational ages in human umbilical cord blood. Pediatr. Res. 64(1), 68-73 (2008).
32. Xue S, Zhang HT, Zhang P et al. Functional endothelial progenitor cells derived from adipose tissue show benefcial effect on cell therapy of traumatic brain injury Neurosci. Lett. 473(3), 186-191 (2010).
33. Ingram DA, Mead LE, Moore DB, Woodard W, Fenoglio A, Yoder MC. Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 105(7), 2783-2786 (2005).
34. Pacilli A, Pasquinelli G. Vascular wall resident progenitor cells: a review. Exp. Cell Res. 315(6), 901-914 (2009).
35. Yoder MC, Ingram DA. Endothelial progenitor cell: ongoing controversy for defning these cells and their role in neoangiogenesis in the murine system. Curr. Opin. Hematol. 16(4), 269-273 (2009).
36. + endothelial progenitor cell subpopulation with potent vasoregenerative capacities. Circ. Res. 98(3), e20-e25 (2006).
37. + cells identifes a population of functional endothelial precursors. Blood 95(3), 952-958 (2000).
38. Gehling UM, Ergün S, Schumacher U et al. In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95(10), 3106-3112 (2000).
39. + cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp. Hematol. 35(7), 1109-1118 (2007).
40. + hematopoietic precursors. Arterioscler. Thromb. Vasc. Biol. 27(7), 1572-1579 (2007).
41. + monocytic cells into endothelial cells on degradable biomaterials. Biomaterials 28(8), 1470-1479 (2007).
42. Fernandez Pujol B, Lucibello FC, Gehling UM et al. Endothelial-like cells derived from human CD14 positive monocytes. Differentiation 65(5), 287-300 (2000).
43. Harraz M, Jiao C, Hanlon HD, Hartley RS, Schatteman GC. Cd34-blood-derived human endothelial cell progenitors. Stem Cells 19(4), 304-312 (2001).
44. + monocytes in vitro. Exp. Hematol. 33(12), 1554-1563 (2005).
45. Ziegelhoeffer T, Fernandez B, Kostin S et al. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ. Res. 94(2), 230-238 (2004).
46. Hur J, Yoon CH, Kim HS et al. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler. Thromb. Vasc. Biol. 24(2), 288-293 (2004).
47. Yoder MC, Mead LE, Prater D et al. Redefning endothelial progenitor cells via clonal ana lysis and hematopoietic stem/progenitor cell principals. Blood 109(5), 1801-1809 (2007).
48. Yoder MC. Defning human endothelial progenitor cells. J. Thromb. Haemost. 7(Suppl. 1), 49-52 (2009).
49. Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler. Thromb. Vasc. Biol. 28(9), 1584-1595 (2008).
50. Thomson JA. Embryonic stem cell lines derived from human blastocysts. Science 282(5391), 1145-1147 (1998).
51. Takahashi K, Tanabe K, Ohnuki M et al. Induction of pluripotent stem cells from adult human fbroblasts by defned factors. Cell 131(5), 861-872 (2007).
52. Amabile G, Meissner A. Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol. Med. 15(2), 59-68 (2009).
53. Feng Q, Lu SJ, Klimanskaya I et al. Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells 28(4), 704-712 (2010).
54. Celermajer DS, Sorensen KE, Gooch VM et al. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 340(8828), 1111-1115 (1992).
55. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84(3), 767-801 (2004).
56. Levenberg S, Zoldan J, Basevitch Y, Langer R. Endothelial potential of human embryonic stem cells. Blood 110(3), 806-814 (2007).
57. Ferreira LS, Gerecht S, Shieh HF 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(3), 286-294 (2007).
58. Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R. Endothelial cells derived from human embryonic stem cells. Proc. Natl Acad. Sci. USA 99(7), 4391-4396 (2002).
59. Wang L, Li L, Shojaei F et al. Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity 21(1), 31-41 (2004).
60. Cho SW, Moon SH, Lee SH et al. Improvement of postnatal neovascularization by human embryonic stem cell-derived endothelial-like cell transplantation in a mouse model of hindlimb ischemia. Circulation 116(21), 2409-2419 (2007).
61. Lu SJ, Ivanova Y, Feng Q, Luo C, Lanza R. Hemangioblasts from human embryonic stem cells generate multilayered blood vessels with functional smooth muscle cells. Regen. Med. 4(1), 37-47 (2009).
62. Nourse MB, Halpin DE, Scatena M et al. VEGF induces differentiation of functional endothelium from human embryonic stem cells: implications for tissue engineering. Arterioscler. Thromb. Vasc. Biol. 30(1), 80-89 (2010).
63. James D, Nam HS, Seandel M, Nolan D, Janovitz T, Tomishima M et al. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFβ inhibition is Id1 dependent. Nat Biotechnol. 28(2), 161-166 (2010).
64. Hwang YS, Bong GC, Ortmann D, Hattori N, Moeller HC, Khademhosseinia A. Microwell-mediated control of embryoid body size regulates embryonic stem cell fate via differential expression of WNT5a and WNT11. Proc. Natl Acad. Sci. USA 106(40), 16978-16983 (2009).
65. Vodyanik MA, Slukvin II. Hematoendothelial differentiation of human embryonic stem cells. Curr. Protoc. Cell Biol. Chapter 23, Unit 23.6 (2007).
66. Choi K-D, Junying Y, Kim S-O et al. Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 27(3), 559-567 (2009).
67. + cells: effcient production in the coculture with OP9 stromal cells and ana lysis of lymphohematopoietic potential. Blood 105(2), 617-626 (2005).
68. Sone M, Itoh H, Yamahara K et al. Pathway for differentiation of human embryonic stem cells to vascular cell components and their potential for vascular regeneration. Arterioscler. Thromb. Vasc. Biol. 27(10), 2127-2134 (2007).
69. Taura D, Sone M, Homma K et al. Induction and isolation of vascular cells from human induced pluripotent stem cells-brief report. Arterioscler. Thromb. Vasc. Biol. 29(7), 1100-1103 (2009).
70. Hill KL, Obrtlikova P, Alvarez DF et al. Human embryonic stem cell-derived vascular progenitor cells capable of endothelial and smooth muscle cell function. Exp. Hematol. 38(3), 246-257.e241 (2010).
71. Bai H, Gao Y, Arzigian M, Wojchowski DM, Wu W-S, Wang ZZ. BMP4 regulates vascular progenitor development in human embryonic stem cells through a smad-dependent pathway. J. Cell. Biochem. 109(2), 363-374 (2010).
72. Wang ZZ, Au P, Chen T et al. Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat Biotechnol. 25(3), 317-318 (2007).
73. 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. 83(12), 1811-1820 (2003).
74. Kaufman DS, Lewis RL, Hanson ET, Auerbach R, Plendl J, Thomson JA. Functional endothelial cells derived from rhesus monkey embryonic stem cells. Blood 103(4), 1325-1332 (2004).
75. Xie CQ, Zhang J, Villacorta L, Cui T, Huang H, Chen YE. A highly effcient method to differentiate smooth muscle cells from human embryonic stem cells. Arterioscler. Thromb. Vasc. Biol. 27(12), e311 (2007).
76. Vo E, Hanjaya-Putra D, Zha Y, Kusuma S, Gerecht S. Smooth-muscle-like cells derived from human embryonic stem cells support and augment cord-like structures in vitro. Stem Cell Rev. Rep. 6(2), 237-247 (2010).
77. Huang H, Zhao X, Chen L et al. Differentiation of human embryonic stem cells into smooth muscle cells in adherent monolayer culture. Biochem. Biophys. Res. Commun. 351(2), 321-327 (2006).
78. Narazaki G, Uosaki H, Teranishi M S et al. Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation 118(5), 498-506 (2008).
79. Cleaver O, Melton DA. Endothelial signaling during development. Nat Med. 9(6), 661-668 (2003).
80. Cimato T, Beers J, Ding S et al. Neuropilin-1 identifes endothelial precursors in human and murine embryonic stem cells before CD34 expression. Circulation 119(16), 2170-2178 (2009).
81. Goldman O, Feraud O, Ponio JBD et al. A boost of BMP4 accelerates the commitment of human embryonic stem cells to the endothelial lineage. Stem Cells 27(8), 1750-1759 (2009).
82. Marchetti S, Gimond C, Iljin K et al. Endothelial cells genetically selected from differentiating mouse embryonic stem cells incorporate at sites of neovascularization in vivo. J. Cell Sci. 115(10), 2075-2085 (2002).
83. Weinberg CB, Bell E. A blood vessel model constructed from collagen and cultured vascular cells. Science 231(4736), 397-400 (1986).
84. Zilla P. Endothelialization of vascular grafts. Curr. Opin. Cardiol. 6(6), 877-886 (1991).
85. Song Y, Kamphuis MMJ, Zhang Z et al. Flexible and elastic porous poly(trimethylene carbonate) structures for use in vascular tissue engineering. Acta Biomater. 6(4), 1269-1277 (2010).
86. Allen JB, Khan S, Lapidos KA, Ameer GA. Toward engineering a human neoendothelium with circulating progenitor cells. Stem Cells 28(2), 318-328 (2010).
87. + bone marrow cells. Blood 95(2), 581-585 (2000).
88. Gong Z, Niklason LE. Small-diameter human vessel wall engineered from bone marrow-derived mesenchymal stem cells (hMSCs). FASEB J. 22(6), 1635-1648 (2008).
89. Griese DP, Ehsan A, Melo LG et al. Isolation and transplantation of autologous circulating endothelial cells into denuded vessels and prosthetic grafts: implications for cell-based vascular therapy Circulation 108(21), 2710-2715 (2003).
90. Ranjan AK, Kumar U, Hardikar AA, Poddar P, Nair PD. Human blood vessel-derived endothelial progenitors for endothelialization of small diameter vascular prosthesis. PLoS ONE 4(11), e7718 (2009).
91. 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. 9(1), 127-136 (2003).
92. Kaushal S, Amiel GE, Guleserian KJ et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med. 7(9), 1035-1040 (2001).
93. Cho SW, Lim SH, Kim IK et al. Small-diameter blood vessels engineered with bone marrow-derived cells. Ann. Surg. 241(3), 506-515 (2005).
94. Wu X, Rabkin-Aikawa E, Guleserian KJ et al. Tissue-engineered microvessels on three-dimensional biodegradable scaffolds using human endothelial progenitor cells. Am. J. Physiol. Heart Circ. Physiol. 287(2), H480-H487 (2004).
95. Hanjaya-Putra D, Yee J, Ceci D, Truitt R, Yee D, Gerecht S. Vascular endothelial growth factor and substrate mechanics regulate in vitro tubulogenesis of endothelial progenitor cells. J. Cell. Mol. Med. DOI: 10.1111/j.1582-4934.2009.00981.x (2009) (Epub ahead of print).
96. Saunders RL, Hammer DA. Assembly of human umbilical vein endothelial cells on compliant hydrogels. Cell. Mol. Bioeng. 3(1), 60-67 (2010).
97. Moon JJ, Saik JE, Poché RA et al. Biomimetic hydrogels with pro-angiogenic properties. Biomaterials 31(14), 3840-3847 (2010).
98. Levenberg S, Rouwkema J, Macdonald M et al. Engineering vascularized skeletal muscle tissue. Nat Biotech. 23(7), 879-884 (2005).
99. Caspi O, Lesman A, Basevitch Y et al. Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ. Res. 100(2), 263-272 (2007).
100. Lesman A, Habib M, Caspi O et al. Transplantation of a tissue-engineered human vascularized cardiac muscle. Tissue Eng. Part A 16(1), 115-125 (2010).
101. Koike N, Fukumura D, Gralla O, Au P, Schechner JS, Jain RK. Tissue engineering: creation of long-lasting blood vessels. Nature 428(6979), 138-139 (2004).
102. Au P, Daheron LM, Duda DG et al. Differential in vivo potential of endothelial progenitor cells from human umbilical cord blood and adult peripheral blood to form functional long-lasting vessels. Blood 111(3), 1302-1305 (2008).
103. Melero-Martin JM, De Obaldia ME, Kang S-Y et al. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ. Res. 103(2), 194-202 (2008).
104. Traktuev DO, Prater DN, Merfeld-Clauss S et al. Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ. Res. 104(12), 1410-1420 (2009).
105. Au P, Tam J, Fukumura D, Jain RK. Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111(9), 4551-4558 (2008).
106. Silva EA, Kim ES, Hyun JK, Mooney DJ. Material-based deployment enhances effcacy of endothelial progenitor cells. Proc. Natl Acad. Sci. USA 105(38), 14347-14352 (2008).
107. Pasquinelli G, Vinci MC, Gamberini C et al. Architectural organization and functional features of early endothelial progenitor cells cultured in a hyaluronan-based polymer scaffold. Tissue Eng. Part A 15(9), 2751-2762 (2009).
108. Mali P, Chou B-K, Yen J et al. Butyrate greatly enhances derivation of human induced pluripotent stem cells by promoting epigenetic remodeling and the expression of pluripotency-associated genes. Stem Cells 28(4), 713-720 (2010).
109. Ye Z, Zhan H, Mali P et al. Human-induced pluripotent stem cells from blood cells of healthy donors and patients with acquired blood disorders. Blood 114(27), 5473-5480 (2009).
110. Mali P, Ye Z, Hommond HH et al. Improved effciency and pace of generating induced pluripotent stem cells from human adult and fetal fbroblasts. Stem Cells 26(8), 1998-2005 (2008).
111. Jia F, Wilson KD, Sun N et al. A nonviral minicircle vector for deriving human iPS cells. Nat Meth. 7(3), 197-199 (2010).
112. Kim K, Doi A, Wen B et al. Epigenetic memory in induced pluripotent stem cells. Nature 467(7313), 285-290 (2010).
113. Polo JM, Liu S, Figueroa ME et al. Cell type of origin infuences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol. 28(8), 848-855 (2010).
114. Soldner F, Hockemeyer D, Beard C et al. Parkinsons disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136(5), 964-977 (2009).