Skip to main content

Advertisement

Log in

Engineering of arteries in vitro

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

This review will focus on two elements that are essential for functional arterial regeneration in vitro: the mechanical environment and the bioreactors used for tissue growth. The importance of the mechanical environment to embryological development, vascular functionality, and vascular graft regeneration will be discussed. Bioreactors generate mechanical stimuli to simulate biomechanical environment of arterial system. This system has been used to reconstruct arterial grafts with appropriate mechanical strength for implantation by controlling the chemical and mechanical environments in which the grafts are grown. Bioreactors are powerful tools to study the effect of mechanical stimuli on extracellular matrix architecture and mechanical properties of engineered vessels. Hence, biomimetic systems enable us to optimize chemo-biomechanical culture conditions to regenerate engineered vessels with physiological properties similar to those of native arteries. In addition, this article reviews various bioreactors designed especially to apply axial loading to engineered arteries. This review will also introduce and examine different approaches and techniques that have been used to engineer biologically based vascular grafts, including collagen-based grafts, fibrin-gel grafts, cell sheet engineering, biodegradable polymers, and decellularization of native vessels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Dahl SLM et al (2003) Decellularized native and engineered arterial scaffolds for transplantation. Cell Transpl 12(6):659–666

    Google Scholar 

  2. Opitz F et al (2004) Tissue engineering of ovine aortic blood vessel substitutes using applied shear stress and enzymatically derived vascular smooth muscle cells. Ann Biomed Eng 32(2):212–222

    CAS  PubMed  Google Scholar 

  3. Conte MS (1998) The ideal small arterial substitute: a search for the Holy Grail? FASEB J 12(1):43–45

    CAS  PubMed  Google Scholar 

  4. Kannan RY et al (2005) Current status of prosthetic bypass grafts: a review. J Biomed Mater Res Part B Appl Biomater 74B(1):570–581

    CAS  Google Scholar 

  5. Pasic M et al (1995) Seeding with omental cells prevents late neointimal hyperplasia in small-diameter Dacron grafts. Circulation 92(9):2605–2616

    CAS  PubMed  Google Scholar 

  6. Graham LM et al (1989) Effects of thromboxane synthetase inhibition on patency and anastomotic hyperplasia of vascular grafts. J Surg Res 46(6):611–615

    CAS  PubMed  Google Scholar 

  7. Lucitti JL et al (2007) Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134(18):3317–3326

    CAS  PubMed  Google Scholar 

  8. Adamo L et al (2009) Biomechanical forces promote embryonic haematopoiesis. Nature 459(7250):1131–1135

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Jones EAV (2011) Mechanical factors in the development of the vascular bed. Respir Physiol Neurobiol 178(1):59–65

    PubMed  Google Scholar 

  10. Culver JC, Dickinson ME (2010) The effects of hemodynamic force on embryonic development. Microcirculation 17(3):164–178

    PubMed Central  PubMed  Google Scholar 

  11. Obi S et al (2009) Fluid shear stress induces arterial differentiation of endothelial progenitor cells. J Appl Physiol 106(1):203–211

    CAS  PubMed  Google Scholar 

  12. Chapman WB (1918) The effect of the heart-beat upon the development of the vascular system in the chick. Am J Anat 23(1):175–203

    Google Scholar 

  13. Wakimoto K et al (2000) Targeted disruption of Na+/Ca2+ exchanger gene leads to cardiomyocyte apoptosis and defects in heartbeat. J Biol Chem 275(47):36991–36998

    CAS  PubMed  Google Scholar 

  14. Hierck BP et al (2008) Fluid shear stress and inner curvature remodeling of the embryonic heart. Choosing the right lane! ScientificWorldJournal 8:212–222

    PubMed  Google Scholar 

  15. Huang CQ et al (2003) Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis. Development 130(24):6111–6119

    CAS  PubMed  Google Scholar 

  16. Clark ER (1918) Studies on the growth of blood-vessels in the tail of the frog larva—by observation and experiment on the living animal. Am J Anat 23(1):37–88

    Google Scholar 

  17. Wagenseil JE, Mecham RP (2009) Vascular extracellular matrix and arterial mechanics. Physiol Rev 89(3):957–989

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Gerrity RG, Cliff WJ (1975) The aortic tunica media of the developing rat. I. Quantitative stereologic and biochemical analysis. Lab Invest 32(5):585–600

    CAS  PubMed  Google Scholar 

  19. Olivetti G et al (1980) Morphometric study of early postnatal development of the thoracic aorta in the rat. Circ Res 47(3):417–424

    CAS  PubMed  Google Scholar 

  20. Berry CL, Looker T, Germain J (1972) The growth and development of the rat aorta. I. Morphological aspects. J Anat 113(Pt 1):1–16

    CAS  PubMed Central  PubMed  Google Scholar 

  21. Lucitti JL et al (2006) Increased arterial load alters aortic structural and functional properties during embryogenesis. Am J Physiol Heart Circ Physiol 291(4):H1919–H1926

    CAS  PubMed  Google Scholar 

  22. Lucitti JL, Tobita K, Keller BB (2005) Arterial hemodynamics and mechanical properties after circulatory intervention in the chick embryo. J Exp Biol 208(10):1877–1885

    PubMed  Google Scholar 

  23. Freed LE et al (2006) Advanced tools for tissue engineering: scaffolds, bioreactors, and signaling. Tissue Eng 12(12):3285–3305

    CAS  PubMed  Google Scholar 

  24. Valdez-Jasso D et al (2011) Linear and nonlinear viscoelastic modeling of aorta and carotid pressure-area dynamics under in vivo and ex vivo conditions. Ann Biomed Eng 39(5):1438–1456

    PubMed Central  PubMed  Google Scholar 

  25. Cheng J, Wagenseil J (2012) Extracellular matrix and the mechanics of large artery development. Biomech Model Mechanobiol 11(8):1169–1186

    Google Scholar 

  26. Silver FH, Horvath I, Foran DJ (2001) Viscoelasticity of the vessel wall: the role of collagen and elastic fibers. Crit Rev Biomed Eng 29(3):279–301

    CAS  PubMed  Google Scholar 

  27. Barra JG et al (1993) Assessment of smooth muscle contribution to descending thoracic aortic elastic mechanics in conscious dogs. Circ Res 73(6):1040–1050

    CAS  PubMed  Google Scholar 

  28. Dahl SLM, Vaughn ME, Niklason LE (2007) An ultrastructural analysis of collagen in tissue engineered arteries. Ann Biomed Eng 35:1749–1755

    PubMed Central  PubMed  Google Scholar 

  29. Canham PB, Finlay HM, Boughner DR (1997) Contrasting structure of the saphenous vein and internal mammary artery used as coronary bypass vessels. Cardiovasc Res 34(3):557–567

    CAS  PubMed  Google Scholar 

  30. Canham PB et al (1991) Medial collagen organization in human arteries of the heart and brain by polarized light microscopy. Connect Tissue Res 26(1–2):121–134

    CAS  PubMed  Google Scholar 

  31. Bou-Gharios G et al (2004) Extra-cellular matrix in vascular networks. Cell Prolif 37(3):207–220

    CAS  PubMed  Google Scholar 

  32. Shadwick RE (1999) Mechanical design in arteries. J Exp Biol 202(23):3305–3313

    CAS  PubMed  Google Scholar 

  33. Humphrey JD (2008) Vascular adaptation and mechanical homeostasis at tissue, cellular, and sub-cellular levels. Cell Biochem Biophys 50(2):53–78

    CAS  PubMed  Google Scholar 

  34. Gleason RL, Wilson E, Humphrey JD (2007) Biaxial biomechanical adaptations of mouse carotid arteries cultured at altered axial extension. J Biomech 40(4):766–776

    PubMed  Google Scholar 

  35. Jackson ZS, Gotlieb AI, Langille BL (2002) Wall tissue remodeling regulates longitudinal tension in arteries. Circ Res 90(8):918–925

    CAS  PubMed  Google Scholar 

  36. Clerin V et al (2003) Tissue engineering of arteries by directed remodeling of intact arterial segments. Tissue Eng 9(3):461–472

    PubMed  Google Scholar 

  37. Lawrence AR, Gooch KJ (2009) Transmural pressure and axial loading interactively regulate arterial remodeling ex vivo. Am J Physiol Heart Circ Physiol 297(1):22

    Google Scholar 

  38. Cines DB et al (1998) Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 91(10):3527–3561

    CAS  PubMed  Google Scholar 

  39. Davies PF (2009) Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med 6(1):16–26

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Chien S (2007) Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol 292(3):H1209–H1224

    CAS  PubMed  Google Scholar 

  41. Yamamoto K et al (2003) Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J Appl Physiol 95(5):2081–2088

    PubMed  Google Scholar 

  42. Franke RP et al (1984) Induction of human vascular endothelial stress fibres by fluid shear stress. Nature 307(5952):648–649

    CAS  PubMed  Google Scholar 

  43. Wechezak AR, Viggers RF, Sauvage LR (1985) Fibronectin and F-actin redistribution in cultured endothelial cells exposed to shear stress. Lab Invest 53(6):639–647

    CAS  PubMed  Google Scholar 

  44. Traub O, Berk BC (1998) Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arterioscler Thromb Vasc Biol 18(5):677–685

    CAS  PubMed  Google Scholar 

  45. Vanhoutte PM (1989) Endothelium and control of vascular function. State of the art lecture. Hypertension 13(6 Pt 2):658–667

    CAS  PubMed  Google Scholar 

  46. Paszkowiak JJ, Dardik A (2003) Arterial wall shear stress: observations from the bench to the bedside. Vasc Endovascular Surg 37(1):47–57

    PubMed  Google Scholar 

  47. Balligand JL, Feron O, Dessy C (2009) eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev 89(2):481–534

    CAS  PubMed  Google Scholar 

  48. Tzima E et al (2006) A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. FASEB J 20(5):A1378–A1378

    Google Scholar 

  49. Shaw A, Xu Q (2003) Biomechanical stress-induced signaling in smooth muscle cells: an update. Curr Vasc Pharmacol 1(1):41–58

    CAS  PubMed  Google Scholar 

  50. Owens GK (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75(3):487–517

    CAS  PubMed  Google Scholar 

  51. Stegemann JP, Hong H, Nerem RM (2005) Mechanical, biochemical, and extracellular matrix effects on vascular smooth muscle cell phenotype. J Appl Physiol 98(6):2321–2327

    PubMed  Google Scholar 

  52. Gupta V, Grande-Allen KJ (2006) Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells. Cardiovasc Res 72(3):375–383

    CAS  PubMed  Google Scholar 

  53. Tock J et al (2003) Induction of SM-alpha-actin expression by mechanical strain in adult vascular smooth muscle cells is mediated through activation of JNK and p38 MAP kinase. Biochem Biophys Res Commun 301(4):1116–1121

    CAS  PubMed  Google Scholar 

  54. Li X et al (2011) Uniaxial mechanical strain modulates the differentiation of neural crest stem cells into smooth muscle lineage on micropatterned surfaces. Plos One 6(10):7

    Google Scholar 

  55. Reusch P et al (1996) Mechanical strain increases smooth muscle and decreases nonmuscle myosin expression in rat vascular smooth muscle cells. Circ Res 79(5):1046–1053

    CAS  PubMed  Google Scholar 

  56. Leung DY, Glagov S, Mathews MB (1976) Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. Science 191(4226):475–477

    CAS  PubMed  Google Scholar 

  57. Beamish JA et al (2010) Molecular regulation of contractile smooth muscle cell phenotype: implications for vascular tissue engineering. Tissue Eng Part B Rev 16(5):467–491

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Carver W et al (1991) Collagen expression in mechanically stimulated cardiac fibroblasts. Circ Res 69(1):116–122

    CAS  PubMed  Google Scholar 

  59. Sheidaei A et al (2011) Simulation of abdominal aortic aneurysm growth with updating hemodynamic loads using a realistic geometry. Med Eng Phys 33(1):80–88

    CAS  PubMed  Google Scholar 

  60. Rucker RB, Tinker D (1977) Structure and metabolism of arterial elastin. Int Rev Exp Pathol 17:1–47

    CAS  PubMed  Google Scholar 

  61. Lefevre M, Rucker RB (1980) Aorta elastin turnover in normal and hypercholesterolemic Japanese quail. Biochim Biophys Acta 630(4):519–529

    CAS  PubMed  Google Scholar 

  62. Shapiro SD (1998) Matrix metalloproteinase degradation of extracellular matrix: biological consequences. Curr Opin Cell Biol 10(5):602–608

    CAS  PubMed  Google Scholar 

  63. Solan A et al (2003) Effect of pulse rate on collagen deposition in the tissue-engineered blood vessel. Tissue Eng 9(4):579–586

    CAS  PubMed  Google Scholar 

  64. Asanuma K et al (2003) Uniaxial strain upregulates matrix-degrading enzymes produced by human vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 284(5):H1778–H1784

    CAS  PubMed  Google Scholar 

  65. Weinberg CB, Bell E (1986) A blood vessel model constructed from collagen and cultured vascular cells. Science 231(4736):397–400

    CAS  PubMed  Google Scholar 

  66. Clark RA et al (1995) Collagen matrices attenuate the collagen-synthetic response of cultured fibroblasts to TGF-beta. J Cell Sci 108(Pt 3):1251–1261

    CAS  PubMed  Google Scholar 

  67. Thie M et al (1991) Aortic smooth muscle cells in collagen lattice culture: effects on ultrastructure, proliferation and collagen synthesis. Eur J Cell Biol 55(2):295–304

    CAS  PubMed  Google Scholar 

  68. Schmidt CE, Baier JM (2000) Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering. Biomaterials 21(22):2215–2231

    CAS  PubMed  Google Scholar 

  69. Payne JW (1973) Polymerization of proteins with glutaraldehyde. Soluble molecular-weight markers. Biochem J 135(4):867–873

    CAS  PubMed Central  PubMed  Google Scholar 

  70. Charulatha V, Rajaram A (2003) Influence of different crosslinking treatments on the physical properties of collagen membranes. Biomaterials 24(5):759–767

    CAS  PubMed  Google Scholar 

  71. Elbjeirami WM et al (2003) Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity. J Biomed Mater Res Part A 66A(3):513–521

    CAS  Google Scholar 

  72. Orban JM et al (2004) Crosslinking of collagen gels by transglutaminase. J Biomed Mater Res Part A 68A(4):756–762

    CAS  Google Scholar 

  73. Brinkman WT et al (2003) Photo-cross-linking of type I collagen gels in the presence of smooth muscle cells: mechanical properties, cell viability, and function. Biomacromolecules 4(4):890–895

    CAS  PubMed  Google Scholar 

  74. Ibusuki S et al (2007) Photochemically cross-linked collagen gels as three-dimensional scaffolds for tissue engineering. Tissue Eng 13(8):1995–2001

    CAS  PubMed  Google Scholar 

  75. Mi SL et al (2011) Photochemical cross-linking of plastically compressed collagen gel produces an optimal scaffold for corneal tissue engineering. J Biomed Mater Res Part A 99A(1):1–8

    CAS  Google Scholar 

  76. Seliktar D et al (2000) Dynamic mechanical conditioning of collagen-gel blood vessel constructs induces remodeling in vitro. Ann Biomed Eng 28(4):351–362

    CAS  PubMed  Google Scholar 

  77. Dahl SL, Rhim C, Song YC, Niklason LE (2007) Mechanical properties and compositions of tissue engineered and native arteries. Ann Biomed Eng 35(3):348–355

    Google Scholar 

  78. Shaikh FM et al (2008) Fibrin: a natural biodegradable scaffold in vascular tissue engineering. Cells Tissues Organs 188(4):333–346

    CAS  PubMed  Google Scholar 

  79. Grassl ED, Oegema TR, Tranquillo RT (2002) Fibrin as an alternative biopolymer to type-I collagen for the fabrication of a media equivalent. J Biomed Mater Res 60(4):607–612

    CAS  PubMed  Google Scholar 

  80. Long JL, Tranquillo RT (2003) Elastic fiber production in cardiovascular tissue-equivalents. Matrix Biol 22(4):339–350

    CAS  PubMed  Google Scholar 

  81. Grassl ED, Oegema TR, Tranquillo RT (2003) A fibrin-based arterial media equivalent. J Biomed Mater Res Part A 66A(3):550–561

    CAS  Google Scholar 

  82. Swartz DD, Russell JA, Andreadis ST (2005) Engineering of fibrin-based functional and implantable small-diameter blood vessels. Am J Physiol Heart Circ Physiol 288(3):H1451–H1460

    CAS  PubMed  Google Scholar 

  83. L’Heureux N et al (1993) In vitro construction of a human blood vessel from cultured vascular cells: a morphologic study. J Vasc Surg 17(3):499–509

    PubMed  Google Scholar 

  84. Konig G et al (2009) Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery. Biomaterials 30(8):1542–1550

    CAS  PubMed Central  PubMed  Google Scholar 

  85. McAllister TN et al (2009) Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: a multicentre cohort study. Lancet 373(9673):1440–1446

    PubMed  Google Scholar 

  86. Garrido SA et al (2009) Haemodialysis access via tissue-engineered vascular graft Authors’ reply. Lancet 374(9685):201

    Google Scholar 

  87. Wystrychowski W et al (2013) First human use of an allogeneic tissue-engineered vascular graft for hemodialysis access. J Vasc Surg 5(13):01530–01539

    Google Scholar 

  88. Pham QP, Sharma U, Mikos AG (2006) Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng 12(5):1197–1211

    CAS  PubMed  Google Scholar 

  89. Sill TJ, von Recum HA (2008) Electro spinning: applications in drug delivery and tissue engineering. Biomaterials 29(13):1989–2006

    CAS  PubMed  Google Scholar 

  90. Mikos AG et al (1993) Prevascularization of porous biodegradable polymers. Biotechnol Bioeng 42(6):716–723

    CAS  PubMed  Google Scholar 

  91. Kwon IK, Matsuda T (2005) Co-electrospun nanofiber fabrics of poly(l-lactide-co-epsilon-caprolactone) with type I collagen or heparin. Biomacromolecules 6(4):2096–2105

    CAS  PubMed  Google Scholar 

  92. Pham QP, Sharma U, Mikos AG (2006) Electrospun poly(epsilon-caprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration. Biomacromolecules 7(10):2796–2805

    CAS  PubMed  Google Scholar 

  93. Bergmeister H et al (2012) Electrospun small-diameter polyurethane vascular grafts: ingrowth and differentiation of vascular-specific host cells. Artif Organs 36(1):54–61

    CAS  PubMed  Google Scholar 

  94. Shin’oka T et al (2005) Midterm clinical result of tissue-engineered vascular autografts seeded with autologous bone marrow cells. J Thorac Cardiovasc Surg 129(6):1330–1338

    PubMed  Google Scholar 

  95. Hibino N et al (2010) Late-term results of tissue-engineered vascular grafts in humans. J Thorac Cardiovasc Surg 139(2):431–436

    PubMed  Google Scholar 

  96. Roh JD et al (2010) Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc Natl Acad Sci USA 107(10):4669–4674

    CAS  PubMed Central  PubMed  Google Scholar 

  97. Wu W, Allen RA, Wang Y (2012) Fast-degrading elastomer enables rapid remodeling of a cell-free synthetic graft into a neoartery. Nat Med 18(7):1148–1153

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Fiddler GI et al (1983) Calcification of glutaraldehyde-preserved porcine and bovine xenograft valves in young children. Ann Thorac Surg 35(3):257–261

    CAS  PubMed  Google Scholar 

  99. Rose AG, Forman R, Bowen RM (1978) Calcification of glutaraldehyde-fixed porcine xenograft. Thorax 33(1):111–114

    CAS  PubMed Central  PubMed  Google Scholar 

  100. Jernigan TW et al (2004) Small intestinal submucosa for vascular reconstruction in the presence of gastrointestinal contamination. Ann Surg 239(5):733–738

    PubMed Central  PubMed  Google Scholar 

  101. Lantz GC et al (1990) Small intestinal submucosa as a small-diameter arterial graft in the dog. J Invest Surg 3(3):217–227

    CAS  PubMed  Google Scholar 

  102. Kennealey PT et al (2011) A prospective, randomized comparison of bovine carotid artery and expanded polytetrafluoroethylene for permanent hemodialysis vascular access. J Vasc Surg 53(6):1640–1648

    PubMed  Google Scholar 

  103. Crapo PM, Gilbert TW, Badylak SF (2011) An overview of tissue and whole organ decellularization processes. Biomaterials 32(12):3233–3243

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Cho SW et al (2005) Small-diameter blood vessels engineered with bone marrow-derived cells. Ann Surg 241(3):506–515

    PubMed Central  PubMed  Google Scholar 

  105. Brown KE et al (2009) Arterial reconstruction with cryopreserved human allografts in the setting of infection: a single-center experience with midterm follow-up. J Vasc Surg 49(3):660–666

    PubMed  Google Scholar 

  106. Gui L et al (2009) Development of decellularized human umbilical arteries as small-diameter vascular grafts. Tissue Eng Part A 15(9):2665–2676

    CAS  PubMed Central  PubMed  Google Scholar 

  107. Schaner PJ et al (2004) Decellularized vein as a potential scaffold for vascular tissue engineering. J Vasc Surg 40(1):146–153

    PubMed  Google Scholar 

  108. Bonetti PO, Lerman LO, Lerman A (2003) Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol 23(2):168–175

    CAS  PubMed  Google Scholar 

  109. Li S, Henry JJ (2011) Nonthrombogenic approaches to cardiovascular bioengineering. Annu Rev Biomed Eng 13:451–475

    CAS  PubMed  Google Scholar 

  110. Chien S (2008) Effects of disturbed flow on endothelial cells. Ann Biomed Eng 36(4):554–562

    PubMed Central  PubMed  Google Scholar 

  111. Cicha I et al (2008) Endothelial dysfunction and monocyte recruitment in cells exposed to non-uniform shear stress. Clin Hemorheol Microcirc 39(1–4):113–119

    CAS  PubMed  Google Scholar 

  112. Chiu J-J, Usami S, Chien S (2009) Vascular endothelial responses to altered shear stress: pathologic implications for atherosclerosis. Ann Med 41(1):19–28

    CAS  PubMed  Google Scholar 

  113. Stanley JC et al (1982) Enhanced patency of small-diameter, externally supported Dacron iliofemoral grafts seeded with endothelial cells. Surgery 92(6):994–1005

    CAS  PubMed  Google Scholar 

  114. Schneider PA et al (1988) Preformed confluent endothelial cell monolayers prevent early platelet deposition on vascular prostheses in baboons. J Vasc Surg 8(3):229–235

    CAS  PubMed  Google Scholar 

  115. Williams SK et al (1991) Formation of a functional endothelium on vascular grafts. J Electron Microsc Tech 19(4):439–451

    CAS  PubMed  Google Scholar 

  116. Pasic M et al (1993) Long-term results in the dog carotid artery with small lumen vascular prostheses with microvascular endothelial cells. Helv Chir Acta 60(3):381–385

    CAS  PubMed  Google Scholar 

  117. Rosenman JE et al (1985) Kinetics of endothelial cell seeding. J Vasc Surg 2(6):778–784

    CAS  PubMed  Google Scholar 

  118. Miyata T et al (1991) Delayed exposure to pulsatile shear stress improves retention of human saphenous vein endothelial cells on seeded ePTFE grafts. J Surg Res 50(5):485–493

    CAS  PubMed  Google Scholar 

  119. Ott MJ, Ballermann BJ (1995) Shear stress-conditioned, endothelial cell-seeded vascular grafts: improved cell adherence in response to in vitro shear stress. Surgery 117(3):334–339

    CAS  PubMed  Google Scholar 

  120. Inoguchi H et al (2007) The effect of gradually graded shear stress on the morphological integrity of a huvec-seeded compliant small-diameter vascular graft. Biomaterials 28(3):486–495

    CAS  PubMed  Google Scholar 

  121. Ott MJ, Olson JL, Ballermann BJ (1995) Chronic in vitro flow promotes ultrastructural differentiation of endothelial cells. Endothelium 3(1):21–30

    Google Scholar 

  122. Ballermann BJ (1998) Adding endothelium to artificial vascular grafts. News Physiol Sci 13:154

    PubMed  Google Scholar 

  123. Kim BS et al (1999) Cyclic mechanical strain regulates the development of engineered smooth muscle tissue. Nat Biotechnol 17(10):979–983

    CAS  PubMed  Google Scholar 

  124. Niklason LE et al (1999) Functional arteries grown in vitro. Science 284(5413):489–493

    CAS  PubMed  Google Scholar 

  125. Cross KS et al (1994) Long-term human vein graft contractility and morphology: a functional and histopathological study of retrieved coronary vein grafts. Br J Surg 81(5):699–705

    CAS  PubMed  Google Scholar 

  126. Niklason LE et al (2001) Morphologic and mechanical characteristics of engineered bovine arteries. J Vasc Surg 33(3):628–638

    CAS  PubMed  Google Scholar 

  127. L’Heureux N et al (1998) A completely biological tissue-engineered human blood vessel. FASEB J 12(1):47–56

    PubMed  Google Scholar 

  128. Mironov V et al (2003) Perfusion bioreactor for vascular tissue engineering with capacities for longitudinal stretch. J Craniofac Surg 14(3):340–347

    PubMed  Google Scholar 

  129. Zaucha MT et al (2009) A novel cylindrical biaxial computer-controlled bioreactor and biomechanical testing device for vascular tissue engineering. Tissue Eng Part A 15(11):3331–3340

    CAS  PubMed Central  PubMed  Google Scholar 

  130. Syedain ZH, Weinberg JS, Tranquillo RT (2008) Cyclic distension of fibrin-based tissue constructs: evidence of adaptation during growth of engineered connective tissue. Proc Natl Acad Sci USA 105(18):6537–6542

    CAS  PubMed Central  PubMed  Google Scholar 

  131. Syedain ZH et al (2011) Implantable arterial grafts from human fibroblasts and fibrin using a multi-graft pulsed flow-stretch bioreactor with noninvasive strength monitoring. Biomaterials 32(3):714–722

    CAS  PubMed Central  PubMed  Google Scholar 

  132. Gui L et al (2013) Construction of tissue-engineered small-diameter vascular grafts in fibrin scaffolds in 30 days. Tissue Eng Part A 10:10

    Google Scholar 

  133. Tower TT, Neidert MR, Tranquillo RT (2002) Fiber alignment imaging during mechanical testing of soft tissues. Ann Biomed Eng 30(10):1221–1233

    PubMed  Google Scholar 

  134. Driessen NJ et al (2003) Computational analyses of mechanically induced collagen fiber remodeling in the aortic heart valve. J Biomech Eng 125(4):549–557

    PubMed  Google Scholar 

  135. Shadwick RE (1999) Mechanical design in arteries. J Exp Biol 202(Pt 23):3305–3313

    CAS  PubMed  Google Scholar 

  136. Cox RH (1978) Differences in mechanics of arterial smooth muscle from hindlimb arteries. Am J Physiol 235(6):H649–H656

    CAS  PubMed  Google Scholar 

  137. Niklason LE et al (2010) Enabling tools for engineering collagenous tissues integrating bioreactors, intravital imaging, and biomechanical modeling. Proc Natl Acad Sci USA 107(8):3335–3339

    CAS  PubMed Central  PubMed  Google Scholar 

  138. Zoumi A et al (2004) Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy. Biophys J 87(4):2778–2786

    CAS  PubMed Central  PubMed  Google Scholar 

  139. Ferruzzi J et al (2011) Mechanical assessment of elastin integrity in fibrillin-1-deficient carotid arteries: implications for Marfan syndrome. Cardiovasc Res 92(2):287–295

    CAS  PubMed Central  PubMed  Google Scholar 

  140. Timmins LH et al (2010) Structural inhomogeneity and fiber orientation in the inner arterial media. Am J Physiol Heart Circ Physiol 298(5):19

    Google Scholar 

  141. Steelman SM et al (2010) Perivascular tethering modulates the geometry and biomechanics of cerebral arterioles. J Biomech 43(14):2717–2721

    PubMed Central  PubMed  Google Scholar 

  142. Hu JJ, Humphrey JD, Yeh AT (2009) Characterization of engineered tissue development under biaxial stretch using nonlinear optical microscopy. Tissue Eng Part A 15(7):1553–1564

    CAS  PubMed Central  PubMed  Google Scholar 

  143. Bourget JM et al (2012) Human fibroblast-derived ECM as a scaffold for vascular tissue engineering. Biomaterials 33(36):9205–9213

    CAS  PubMed  Google Scholar 

  144. Hasan A et al (2014) Electrospun scaffolds for tissue engineering of vascular grafts. Acta Biomater 10(1):11–25

    Google Scholar 

  145. Thomas V et al (2011) Electrospinning of Biosyn((R))-based tubular conduits: structural, morphological, and mechanical characterizations. Acta Biomater 7(5):2070–2079

    CAS  PubMed  Google Scholar 

  146. Soletti L et al (2010) A bilayered elastomeric scaffold for tissue engineering of small diameter vascular grafts. Acta Biomater 6(1):110–122

    CAS  PubMed Central  PubMed  Google Scholar 

  147. Subramanian A, Krishnan UM, Sethuraman S (2011) Fabrication of uniaxially aligned 3D electrospun scaffolds for neural regeneration. Biomed Mater 6(2):1748–6041

    Google Scholar 

  148. Zhao Y et al (2010) The development of a tissue-engineered artery using decellularized scaffold and autologous ovine mesenchymal stem cells. Biomaterials 31(2):296–307

    PubMed  Google Scholar 

  149. Dahl SL et al (2011) Readily available tissue-engineered vascular grafts. Sci Transl Med 3(68):3001426

    Google Scholar 

  150. Quint C et al (2011) Decellularized tissue-engineered blood vessel as an arterial conduit. Proc Natl Acad Sci USA 108(22):9214–9219

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by NIH R01 HL083895-06A1 (Niklason), 1P01HL107205-01A1(Simons), and R01 EB008366-03 Niklason, LE (PI).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laura E. Niklason.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, A.H., Niklason, L.E. Engineering of arteries in vitro. Cell. Mol. Life Sci. 71, 2103–2118 (2014). https://doi.org/10.1007/s00018-013-1546-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-013-1546-3

Keywords

Navigation