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Abstract

Engineered tissues represent an increasingly promising therapeutic approach for correcting structural defects and promoting tissue regeneration in cardiovascular diseases. One of the challenges associated with this approach has been the necessity for the replacement tissue to promote sufficient vascularization to maintain functionality after implantation. This review highlights a number of promising prevascularization design approaches for introducing vasculature into engineered tissues. Although we focus on encouraging blood vessel formation within myocardial implants, we also discuss techniques developed for other tissues that could eventually become relevant to engineered cardiac tissues. Because the ultimate solution to engineered tissue vascularization will require collaboration between wide-ranging disciplines such as developmental biology, tissue engineering, and computational modeling, we explore contributions from each field.

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2017-06-21
2024-03-29
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Literature Cited

  1. L'Heureux N, McAllister TN, de la Fuente LM. 1.  2007. Tissue-engineered blood vessel for adult arterial revascularization. N. Engl. J. Med. 357:1451–53 [Google Scholar]
  2. Hibino N, McGillicuddy E, Matsumura G, Ichihara Y, Naito Y. 2.  et al. 2010. Late-term results of tissue-engineered vascular grafts in humans. J. Thorac. Cardiovasc. Surg. 139:431–36 [Google Scholar]
  3. Dohmen PM, Lembcke A, Holinski S, Kivelitz D, Braun JP. 3.  et al. 2007. Mid-term clinical results using a tissue-engineered pulmonary valve to reconstruct the right ventricular outflow tract during the Ross procedure. Ann. Thorac. Surg. 84:729–36 [Google Scholar]
  4. Elliott MB, Gerecht S. 4.  2016. Three-dimensional culture of small-diameter vascular grafts. J. Mater. Chem. B 4:3443–53 [Google Scholar]
  5. Folkman J, Hochberg M. 5.  1973. Self-regulation of growth in three dimensions. J. Exp. Med. 138:745–53 [Google Scholar]
  6. Basavarajaiah S, Wilson M, Naghavi R, Whyte G, Turner M, Sharma S. 6.  2007. Physiological upper limits of left ventricular dimensions in highly trained junior tennis players. Br. J. Sports Med. 41:784–88 [Google Scholar]
  7. Chaturvedi RR, Stevens KR, Solorzano RD, Schwartz RE, Eyckmans J. 7.  et al. 2015. Patterning vascular networks in vivo for tissue engineering applications. Tissue Eng. C 21:509–17 [Google Scholar]
  8. Rioja AY, Tiruvannamalai Annamalai R, Paris S, Putnam AJ, Stegemann JP. 8.  2016. Endothelial sprouting and network formation in collagen- and fibrin-based modular microbeads. Acta Biomater 29:33–41 [Google Scholar]
  9. Murphy SV, Atala A. 9.  2014. 3D bioprinting of tissues and organs. Nat. Biotechnol. 32:773–85 [Google Scholar]
  10. Pashneh-Tala S, MacNeil S, Claeyssens F. 10.  2016. The tissue-engineered vascular graft—past, present, and future. Tissue Eng. B 22:68–100 [Google Scholar]
  11. Kinstlinger IS, Miller JS. 11.  2016. 3D-printed fluidic networks as vasculature for engineered tissue. Lab Chip 16:2025–43 [Google Scholar]
  12. Risau W, Flamme I. 12.  1995. Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11:73–91 [Google Scholar]
  13. Udan RS, Culver JC, Dickinson ME. 13.  2013. Understanding vascular development. Wiley Interdiscip. Rev. Dev. Biol. 2:327–46 [Google Scholar]
  14. Murakami M, Nguyen LT, Hatanaka K, Schachterle W, Chen P-Y. 14.  et al. 2011. FGF-dependent regulation of VEGF receptor 2 expression in mice. J. Clin. Investig. 121:2668–78 [Google Scholar]
  15. Welti J, Loges S, Dimmeler S, Carmeliet P. 15.  2013. Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J. Clin. Investig. 123:3190–200 [Google Scholar]
  16. Rhodes JM, Simons M. 16.  2007. The extracellular matrix and blood vessel formation: not just a scaffold. J. Cell. Mol. Med. 11:176–205 [Google Scholar]
  17. Chen HI, Sharma B, Akerberg BN, Numi HJ, Kivelä R. 17.  et al. 2014. The sinus venosus contributes to coronary vasculature through VEGFC-stimulated angiogenesis. Development 141:4500–12 [Google Scholar]
  18. Wu B, Zhang Z, Lui W, Chen X, Wang Y. 18.  et al. 2012. Endocardial cells form the coronary arteries by angiogenesis through myocardial–endocardial VEGF signaling. Cell 151:1083–96 [Google Scholar]
  19. Chen HI, Poduri A, Numi H, Kivela R, Saharinen P. 19.  et al. 2014. VEGF-C and aortic cardiomyocytes guide coronary artery stem development. J. Clin. Investig. 124:4899–914 [Google Scholar]
  20. Parera MC, van Dooren M, van Kempen M, de Krijger R, Grosveld F. 20.  et al. 2005. Distal angiogenesis: a new concept for lung vascular morphogenesis. Am. J. Physiol. Lung Cell. Mol. Physiol. 288:L141–49 [Google Scholar]
  21. Burton AC. 21.  1954. Relation of structure to function of the tissues of the wall of blood vessels. Physiol. Rev. 34:619–42 [Google Scholar]
  22. Stoker ME, Gerdes AM, May JF. 22.  1982. Regional differences in capillary density and myocyte size in the normal human heart. Anat. Rec. 202:187–91 [Google Scholar]
  23. Coulombe KL, Bajpai VK, Andreadis ST, Murry CE. 23.  2014. Heart regeneration with engineered myocardial tissue. Annu. Rev. Biomed. Eng 161–28 [Google Scholar]
  24. Sanganalmath SK, Bolli R. 24.  2013. Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ. Res. 113:810–34 [Google Scholar]
  25. Menasche P, Hagege AA, Scorsin M, Pouzet B, Desnos M. 25.  et al. 2001. Myoblast transplantation for heart failure. Lancet 357:279–80 [Google Scholar]
  26. Taylor DA, Atkins BZ, Hungspreugs P, Jones TR, Reedy MC. 26.  et al. 1998. Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat. Med. 4:929–33 [Google Scholar]
  27. Zhang M, Methot D, Poppa V, Fujio Y, Walsh K, Murry CE. 27.  2001. Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J. Mol. Cell. Cardiol. 33:907–21 [Google Scholar]
  28. Chen YH, Chung YC, Wang IJ, Young TH. 28.  2012. Control of cell attachment on pH-responsive chitosan surface by precise adjustment of medium pH. Biomaterials 33:1336–42 [Google Scholar]
  29. Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L. 29.  et al. 2005. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111:2198–202 [Google Scholar]
  30. Terrovitis J, Lautamaki R, Bonios M, Fox J, Engles JM. 30.  et al. 2009. Noninvasive quantification and optimization of acute cell retention by in vivo positron emission tomography after intramyocardial cardiac-derived stem cell delivery. J. Am. Coll. Cardiol. 54:1619–26 [Google Scholar]
  31. Sawa Y, Miyagawa S, Sakaguchi T, Fujita T, Matsuyama A. 31.  et al. 2012. Tissue engineered myoblast sheets improved cardiac function sufficiently to discontinue LVAS in a patient with DCM: report of a case. Surg. Today 42:181–84 [Google Scholar]
  32. Patel NG, Zhang G. 32.  2013. Responsive systems for cell sheet detachment. Organogenesis 9:93–100 [Google Scholar]
  33. Williams C, Xie AW, Yamato M, Okano T, Wong JY. 33.  2011. Stacking of aligned cell sheets for layer-by-layer control of complex tissue structure. Biomaterials 32:5625–32 [Google Scholar]
  34. Isenberg BC, Tsuda Y, Williams C, Shimizu T, Yamato M. 34.  et al. 2008. A thermoresponsive, microtextured substrate for cell sheet engineering with defined structural organization. Biomaterials 29:2565–72 [Google Scholar]
  35. Lin JB, Isenberg BC, Shen Y, Schorsch K, Sazonova OV, Wong JY. 35.  2012. Thermo-responsive poly(N-isopropylacrylamide) grafted onto microtextured poly(dimethylsiloxane) for aligned cell sheet engineering. Colloids Surf. B 99:108–15 [Google Scholar]
  36. Sekine H, Shimizu T, Dobashi I, Matsuura K, Hagiwara N. 36.  et al. 2011. Cardiac cell sheet transplantation improves damaged heart function via superior cell survival in comparison with dissociated cell injection. Tissue Eng. A 17:2973–80 [Google Scholar]
  37. Takeuchi R, Kuruma Y, Sekine H, Dobashi I, Yamato M. 37.  et al. 2014. In vivo vascularization of cell sheets provided better long-term tissue survival than injection of cell suspension. J. Tissue Eng. Regen. Med. 10:700–10 [Google Scholar]
  38. Masumoto H, Ikuno T, Takeda M, Fukushima H, Marui A. 38.  et al. 2014. Human iPS cell–engineered cardiac tissue sheets with cardiomyocytes and vascular cells for cardiac regeneration. Sci. Rep. 4:6716 [Google Scholar]
  39. Sekine H, Shimizu T, Hobo K, Sekiya S, Yang J. 39.  et al. 2008. Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 118:S145–52 [Google Scholar]
  40. Asakawa N, Shimizu T, Tsuda Y, Sekiya S, Sasagawa T. 40.  et al. 2010. Pre-vascularization of in vitro three-dimensional tissues created by cell sheet engineering. Biomaterials 31:3903–9 [Google Scholar]
  41. Hiroaki T, Katsuhisa S, Masatoshi K, Megumi M, Kazuyoshi I. 41.  et al. 2015. Controlling shape and position of vascular formation in engineered tissues by arbitrary assembly of endothelial cells. Biofabrication 7:045006 [Google Scholar]
  42. Muraoka M, Shimizu T, Itoga K, Takahashi H, Okano T. 42.  2013. Control of the formation of vascular networks in 3D tissue engineered constructs. Biomaterials 34:696–703 [Google Scholar]
  43. Bak S, Ahmad T, Lee YB, Lee JY, Kim EM, Shin H. 43.  2016. Delivery of a cell patch of cocultured endothelial cells and smooth muscle cells using thermoresponsive hydrogels for enhanced angiogenesis. Tissue Eng. A 22:182–93 [Google Scholar]
  44. Miyagawa S, Sawa Y, Sakakida S, Taketani S, Kondoh H. 44.  et al. 2005. Tissue cardiomyoplasty using bioengineered contractile cardiomyocyte sheets to repair damaged myocardium: their integration with recipient myocardium. Transplantation 80:1586–95 [Google Scholar]
  45. Shimizu T, Sekine H, Isoi Y, Yamato M, Kikuchi A, Okano T. 45.  2006. Long-term survival and growth of pulsatile myocardial tissue grafts engineered by the layering of cardiomyocyte sheets. Tissue Eng 12:499–507 [Google Scholar]
  46. Masuda S, Matsuura K, Anazawa M, Iwamiya T, Shimizu T, Okano T. 46.  2015. Formation of vascular network structures within cardiac cell sheets from mouse embryonic stem cells. Regen. Ther. 2:6–16 [Google Scholar]
  47. Kim SJ, Jun I, Kim DW, Lee YB, Lee YJ. 47.  et al. 2013. Rapid transfer of endothelial cell sheet using a thermosensitive hydrogel and its effect on therapeutic angiogenesis. Biomacromolecules 14:4309–19 [Google Scholar]
  48. Jun I, Kim SJ, Lee JH, Lee YJ, Shin YM. 48.  et al. 2012. Transfer printing of cell layers with an anisotropic extracellular matrix assembly using cell-interactive and thermosensitive hydrogels. Adv. Funct. Mater. 22:4060–69 [Google Scholar]
  49. Akintewe OO, DuPont SJ, Elineni KK, Cross MC, Toomey RG, Gallant ND. 49.  2015. Shape-changing hydrogel surfaces trigger rapid release of patterned tissue modules. Acta Biomater 11:96–103 [Google Scholar]
  50. Ishii M, Shibata R, Numaguchi Y, Kito T, Suzuki H. 50.  et al. 2011. Enhanced angiogenesis by transplantation of mesenchymal stem cell sheet created by a novel magnetic tissue engineering method. Arterioscler. Thromb. Vasc. Biol. 31:2210–15 [Google Scholar]
  51. Ito A, Takizawa Y, Honda H, Hata K, Kagami H. 51.  et al. 2004. Tissue engineering using magnetite nanoparticles and magnetic force: heterotypic layers of cocultured hepatocytes and endothelial cells. Tissue Eng 10:833–40 [Google Scholar]
  52. Shimizu K, Ito A, Lee JK, Yoshida T, Miwa K. 52.  et al. 2007. Construction of multi-layered cardiomyocyte sheets using magnetite nanoparticles and magnetic force. Biotechnol. Bioeng. 96:803–9 [Google Scholar]
  53. Shimizu K, Ito A, Yoshida T, Yamada Y, Ueda M, Honda H. 53.  2007. Bone tissue engineering with human mesenchymal stem cell sheets constructed using magnetite nanoparticles and magnetic force. J. Biomed. Mater. Res. B 82471–80 [Google Scholar]
  54. Seto Y, Inaba R, Okuyama T, Sassa F, Suzuki H, Fukuda J. 54.  2010. Engineering of capillary-like structures in tissue constructs by electrochemical detachment of cells. Biomaterials 31:2209–15 [Google Scholar]
  55. Mendes PM. 55.  2013. Cellular nanotechnology: making biological interfaces smarter. Chem. Soc. Rev. 42:9207–18 [Google Scholar]
  56. Gouveia RM, Castelletto V, Hamley IW, Connon CJ. 56.  2015. New self-assembling multifunctional templates for the biofabrication and controlled self-release of cultured tissue. Tissue Eng. A 21:1772–84 [Google Scholar]
  57. Sakai S, Ogushi Y, Kawakami K. 57.  2009. Enzymatically crosslinked carboxymethylcellulose–tyramine conjugate hydrogel: cellular adhesiveness and feasibility for cell sheet technology. Acta Biomater 5:554–59 [Google Scholar]
  58. de las Heras Alarcón C, Pennadam S, Alexander C. 58.  2005. Stimuli responsive polymers for biomedical applications. Chem. Soc. Rev. 34:276–85 [Google Scholar]
  59. Wirkner M, Alonso JM, Maus V, Salierno M, Lee TT. 59.  et al. 2011. Triggered cell release from materials using bioadhesive photocleavable linkers. Adv. Mater. 23:3907–10 [Google Scholar]
  60. Kim JJ, Wong JY. 60.  2016. Multi-layered cell constructs and methods of use and production using enzymatically degradable natural polymers US Patent Appl. 20160115457
  61. Lancaster MA, Knoblich JA. 61.  2014. Organogenesis in a dish: modeling development and disease using organoid technologies. Science 345:1247125 [Google Scholar]
  62. McMurtrey RJ. 62.  2016. Analytic models of oxygen and nutrient diffusion, metabolism dynamics, and architecture optimization in three-dimensional tissue constructs with applications and insights in cerebral organoids. Tissue Eng. C 22:221–49 [Google Scholar]
  63. Turner DA, Baillie-Johnson P, Martinez Arias A. 63.  2016. Organoids and the genetically encoded self-assembly of embryonic stem cells. BioEssays 38:181–91 [Google Scholar]
  64. Watson CL, Mahe MM, Múnera J, Howell JC, Sundaram N. 64.  et al. 2014. An in vivo model of human small intestine using pluripotent stem cells. Nat. Med. 20:1310–14 [Google Scholar]
  65. Takebe T, Zhang R-R, Koike H, Kimura M, Yoshizawa E. 65.  et al. 2014. Generation of a vascularized and functional human liver from an iPSC-derived organ bud transplant. Nat. Protoc. 9:396–409 [Google Scholar]
  66. Hay ED. 66.  2005. The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev. Dyn. 233:706–20 [Google Scholar]
  67. Rafii S, Butler JM, Ding B-S. 67.  2016. Angiocrine functions of organ-specific endothelial cells. Nature 529:316–25 [Google Scholar]
  68. Beauchamp P, Moritz W, Kelm JM, Ullrich ND, Agarkova I. 68.  et al. 2015. Development and characterization of a scaffold-free 3D spheroid model of induced pluripotent stem cell–derived human cardiomyocytes. Tissue Eng. C 21:852–61 [Google Scholar]
  69. Tian L, George SC. 69.  2011. Biomaterials to prevascularize engineered tissues. J. Cardiovasc. Transl. Res. 4:685–98 [Google Scholar]
  70. Bach TL, Barsigian C, Chalupowicz DG, Busler D, Yaen CH. 70.  et al. 1998. VE-Cadherin mediates endothelial cell capillary tube formation in fibrin and collagen gels. Exp. Cell Res. 238:324–34 [Google Scholar]
  71. Montesano R, Orci L. 71.  1985. Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell 42:469–77 [Google Scholar]
  72. Cummings CL, Gawlitta D, Nerem RM, Stegemann JP. 72.  2004. Properties of engineered vascular constructs made from collagen, fibrin, and collagen–fibrin mixtures. Biomaterials 25:3699–706 [Google Scholar]
  73. Rao RR, Peterson AW, Ceccarelli J, Putnam AJ, Stegemann JP. 73.  2012. Matrix composition regulates three-dimensional network formation by endothelial cells and mesenchymal stem cells in collagen/fibrin materials. Angiogenesis 15:253–64 [Google Scholar]
  74. Brougham CM, Levingstone TJ, Jockenhoevel S, Flanagan TC, O'Brien FJ. 74.  2015. Incorporation of fibrin into a collagen–glycosaminoglycan matrix results in a scaffold with improved mechanical properties and enhanced capacity to resist cell-mediated contraction. Acta Biomater 26:205–14 [Google Scholar]
  75. Feng X, Tonnesen MG, Mousa SA, Clark RA. 75.  2013. Fibrin and collagen differentially but synergistically regulate sprout angiogenesis of human dermal microvascular endothelial cells in 3-dimensional matrix. Int. J. Cell Biol. 2013:231279 [Google Scholar]
  76. Aplin AC, Nicosia RF. 76.  2015. The rat aortic ring model of angiogenesis. Methods Mol. Biol. 1214:255–64 [Google Scholar]
  77. Allen P, Kang KT, Bischoff J. 77.  2015. Rapid onset of perfused blood vessels after implantation of ECFCs and MPCs in collagen, PuraMatrix and fibrin provisional matrices. J. Tissue Eng. Regen. Med. 9:632–36 [Google Scholar]
  78. Sun W, Sun Y, Klar AS, Geutjes P, Reichmann E. 78.  et al. 2016. Functional analysis of vascularized collagen/fibrin templates by MRI in vivo. Tissue Eng. C 22:747–55 [Google Scholar]
  79. Simons M, Alitalo K, Annex BH, Augustin HG, Beam C. 79.  et al. 2015. State-of-the-art methods for evaluation of angiogenesis and tissue vascularization: a scientific statement from the American Heart Association. Circ. Res. 116:e99–132 [Google Scholar]
  80. Pagliari S, Tirella A, Ahluwalia A, Duim S, Goumans MJ. 80.  et al. 2014. A multistep procedure to prepare pre-vascularized cardiac tissue constructs using adult stem sells, dynamic cell cultures, and porous scaffolds [sic]. Front. Physiol. 5:210 [Google Scholar]
  81. Whisler JA, Chen MB, Kamm RD. 81.  2014. Control of perfusable microvascular network morphology using a multiculture microfluidic system. Tissue Eng. C 20:543–52 [Google Scholar]
  82. Lesman A, Rosenfeld D, Landau S, Levenberg S. 82.  2016. Mechanical regulation of vascular network formation in engineered matrices. Adv. Drug Deliv. Rev. 96:176–82 [Google Scholar]
  83. Baranski JD, Chaturvedi RR, Stevens KR, Eyckmans J, Carvalho B. 83.  et al. 2013. Geometric control of vascular networks to enhance engineered tissue integration and function. PNAS 110:7586–91 [Google Scholar]
  84. Rioja AY, Annamalai RT, Paris S, Putnam AJ, Stegemann JP. 84.  2016. Endothelial sprouting and network formation in collagen- and fibrin-based modular microbeads. Acta Biomater 29:33–41 [Google Scholar]
  85. Pati F, Adhikari B, Dhara S. 85.  2012. Collagen intermingled chitosan-tripolyphosphate nano/micro fibrous scaffolds for tissue-engineering application. J. Biomater. Sci. Polym. Ed. 23:1923–38 [Google Scholar]
  86. Chan EC, Kuo SM, Kong AM, Morrison WA, Dusting GJ. 86.  et al. 2016. Three dimensional collagen scaffold promotes intrinsic vascularisation for tissue engineering applications. PLOS ONE 11:e0149799 [Google Scholar]
  87. Lien SM, Ko LY, Huang TJ. 87.  2009. Effect of pore size on ECM secretion and cell growth in gelatin scaffold for articular cartilage tissue engineering. Acta Biomater 5:670–79 [Google Scholar]
  88. Peterson AW, Caldwell DJ, Rioja AY, Rao RR, Putnam AJ, Stegemann JP. 88.  2014. Vasculogenesis and angiogenesis in modular collagen–fibrin microtissues. Biomater. Sci. 2:1497–508 [Google Scholar]
  89. Boland ED, Matthews JA, Pawlowski KJ, Simpson DG, Wnek GE, Bowlin GL. 89.  2004. Electrospinning collagen and elastin: preliminary vascular tissue engineering. Front. Biosci. 9:1422–32 [Google Scholar]
  90. Sell SA, Francis MP, Garg K, McClure MJ, Simpson DG, Bowlin GL. 90.  2008. Cross-linking methods of electrospun fibrinogen scaffolds for tissue engineering applications. Biomed. Mater 3045001 [Google Scholar]
  91. Sell SA, McClure MJ, Garg K, Wolfe PS, Bowlin GL. 91.  2009. Electrospinning of collagen/biopolymers for regenerative medicine and cardiovascular tissue engineering. Adv. Drug Deliv. Rev. 61:1007–19 [Google Scholar]
  92. Hasan A, Paul A, Vrana NE, Zhao X, Memic A. 92.  et al. 2014. Microfluidic techniques for development of 3D vascularized tissue. Biomaterials 35:7308–25 [Google Scholar]
  93. Rim NG, Shin CS, Shin H. 93.  2013. Current approaches to electrospun nanofibers for tissue engineering. Biomed. Mater 8014102 [Google Scholar]
  94. Barnes CP, Pemble CW, Brand DD, Simpson DG, Bowlin GL. 94.  2007. Cross-linking electrospun type II collagen tissue engineering scaffolds with carbodiimide in ethanol. Tissue Eng 13:1593–605 [Google Scholar]
  95. Soon AS, Lee CS, Barker TH. 95.  2011. Modulation of fibrin matrix properties via knob:hole affinity interactions using peptide–PEG conjugates. Biomaterials 32:4406–14 [Google Scholar]
  96. Heydarkhan-Hagvall S, Schenke-Layland K, Dhanasopon AP, Rofail F, Smith H. 96.  et al. 2008. Three-dimensional electrospun ECM-based hybrid scaffolds for cardiovascular tissue engineering. Biomaterials 29:2907–14 [Google Scholar]
  97. Alom Ruiz S, Chen CS. 97.  2007. Microcontact printing: a tool to pattern. Soft Matter 3:168–77 [Google Scholar]
  98. Crapo PM, Gilbert TW, Badylak SF. 98.  2011. An overview of tissue and whole organ decellularization processes. Biomaterials 32:3233–43 [Google Scholar]
  99. Badylak SF, Taylor D, Uygun K. 99.  2011. Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu. Rev. Biomed. Eng 1327–53 [Google Scholar]
  100. Gilbert TW, Freund JM, Badylak SF. 100.  2009. Quantification of DNA in biologic scaffold materials. J. Surg. Res. 152:135–39 [Google Scholar]
  101. Turner NJ, Badylak SF. 101.  2015. The use of biologic scaffolds in the treatment of chronic nonhealing wounds. Adv. Wound Care 4:490–500 [Google Scholar]
  102. Guyette JP, Charest JM, Mills RW, Jank BJ, Moser PT. 102.  et al. 2016. Bioengineering human myocardium on native extracellular matrix. Circ. Res. 118:56–72 [Google Scholar]
  103. Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM. 103.  et al. 2008. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 14:213–21 [Google Scholar]
  104. Tarbell JM, Simon SI, Curry FR. 104.  2014. Mechanosensing at the vascular interface. Annu. Rev. Biomed. Eng 16505–32 [Google Scholar]
  105. Drenckhahn D, Gress T, Franke RP. 105.  1986. Vascular endothelial stress fibres: their potential role in protecting the vessel wall from rheological damage. Klin. Wochenschr. 64:986–88 [Google Scholar]
  106. Dian K, Xie Y, Zhang E, Shi Y, Chen H. 106.  2003. [Effect of turbulent flow on adhesion molecules expression of vascular endothelial cells.]. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi 20:638–41 [Google Scholar]
  107. McFetridge PS, Abe K, Horrocks M, Chaudhuri JB. 107.  2007. Vascular tissue engineering: bioreactor design considerations for extended culture of primary human vascular smooth muscle cells. ASAIO J 53:623–30 [Google Scholar]
  108. Schulte J, Friedrich A, Hollweck T, König F, Eblenkamp M. 108.  et al. 2014. A novel seeding and conditioning bioreactor for vascular tissue engineering. Processes 2:526 [Google Scholar]
  109. Sekine H, Shimizu T, Sakaguchi K, Dobashi I, Wada M. 109.  et al. 2013. In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels. Nat. Commun. 4:1399 [Google Scholar]
  110. Sakaguchi K, Shimizu T, Okano T. 110.  2015. Construction of three-dimensional vascularized cardiac tissue with cell sheet engineering. J. Control. Release 205:83–88 [Google Scholar]
  111. Song L, Zhou Q, Duan P, Guo P, Li D. 111.  et al. 2012. Successful development of small diameter tissue-engineering vascular vessels by our novel integrally designed pulsatile perfusion-based bioreactor. PLOS ONE 7:e42569 [Google Scholar]
  112. Whitesides GM. 112.  2006. The origins and the future of microfluidics. Nature 442:368–73 [Google Scholar]
  113. Bogorad MI, DeStefano J, Karlsson J, Wong AD, Gerecht S, Searson PC. 113.  2015. Review: In vitro microvessel models. Lab Chip 15:4242–55 [Google Scholar]
  114. Kaihara S, Borenstein J, Koka R, Lalan S, Ochoa ER. 114.  et al. 2000. Silicon micromachining to tissue engineer branched vascular channels for liver fabrication. Tissue Eng 6:105–17 [Google Scholar]
  115. Zheng Y, Chen J, Craven M, Choi NW, Totorica S. 115.  et al. 2012. In vitro microvessels for the study of angiogenesis and thrombosis. PNAS 109:9342–47 [Google Scholar]
  116. Nguyen D-HT, Stapleton SC, Yang MT, Cha SS, Choi CK. 116.  et al. 2013. Biomimetic model to reconstitute angiogenic sprouting morphogenesis in vitro. PNAS 110:6712–17 [Google Scholar]
  117. Zhang B, Montgomery M, Chamberlain MD, Ogawa S, Korolj A. 117.  et al. 2016. Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis. Nat. Mater. 15:669–78 [Google Scholar]
  118. Kolesky DB, Homan KA, Skylar-Scott MA, Lewis JA. 118.  2016. Three-dimensional bioprinting of thick vascularized tissues. PNAS 113:3179–84 [Google Scholar]
  119. Smith Q, Gerecht S. 119.  2014. Going with the flow: microfluidic platforms in vascular tissue engineering. Curr. Opin. Chem. Eng. 3:42–50 [Google Scholar]
  120. Chung S, Sudo R, Zervantonakis IK, Rimchala T, Kamm RD. 120.  2009. Microfluidics: surface-treatment-induced three-dimensional capillary morphogenesis in a microfluidic platform. Adv. Mater. 21:4863–67 [Google Scholar]
  121. Kim S, Lee H, Chung M, Jeon NL. 121.  2013. Engineering of functional, perfusable 3D microvascular networks on a chip. Lab Chip 13:1489–500 [Google Scholar]
  122. Hsu Y-H, Moya ML, Hughes CCW, George SC, Lee AP. 122.  2013. A microfluidic platform for generating large-scale nearly identical human microphysiological vascularized tissue arrays. Lab Chip 13:2990–98 [Google Scholar]
  123. Hsu YH, Moya ML, Abiri P, Hughes CC, George SC, Lee AP. 123.  2013. Full range physiological mass transport control in 3D tissue cultures. Lab Chip 13:81–89 [Google Scholar]
  124. Moya ML, Hsu Y-H, Lee AP, Hughes CCW, George SC. 124.  2013. In vitro perfused human capillary networks. Tissue Eng. C 19:730–37 [Google Scholar]
  125. Jeon JS, Bersini S, Whisler JA, Chen MB, Dubini G. 125.  et al. 2014. Generation of 3D functional microvascular networks with human mesenchymal stem cells in microfluidic systems. Integr. Biol. Quant. Biosci. Nano Macro 6:555–63 [Google Scholar]
  126. Moya M, Tran D, George SC. 126.  2013. An integrated in vitro model of perfused tumor and cardiac tissue. Stem Cell Res. Ther. 4:Suppl. 1S15 [Google Scholar]
  127. Deakin AS. 127.  1976. Model for initial vascular patterns in melanoma transplants. Growth 40:191–201 [Google Scholar]
  128. Qutub AA, Popel AS. 128.  2015. Angiogenesis, computational modeling perspective. Encyclopedia of Applied and Computational Mathematics B Engquist 58–67 Berlin: Springer [Google Scholar]
  129. Checa S, Prendergast PJ. 129.  2010. Effect of cell seeding and mechanical loading on vascularization and tissue formation inside a scaffold: a mechano-biological model using a lattice approach to simulate cell activity. J. Biomech. 43:961–68 [Google Scholar]
  130. Liu G, Qutub AA, Vempati P, Mac Gabhann F, Popel AS. 130.  2011. Module-based multiscale simulation of angiogenesis in skeletal muscle. Theor. Biol. Med. Model 86 [Google Scholar]
  131. Walpole J, Chappell JC, Cluceru JG, Mac Gabhann F, Bautch VL, Peirce SM. 131.  2015. Agent-based model of angiogenesis simulates capillary sprout initiation in multicellular networks. Integr. Biol. 7:987–97 [Google Scholar]
  132. Mehdizadeh H, Sumo S, Bayrak ES, Brey EM, Cinar A. 132.  2013. Three-dimensional modeling of angiogenesis in porous biomaterial scaffolds. Biomaterials 34:2875–87 [Google Scholar]
  133. Zieber L, Or S, Ruvinov E, Cohen S. 133.  2014. Microfabrication of channel arrays promotes vessel-like network formation in cardiac cell construct and vascularization in vivo. Biofabrication 6:024102 [Google Scholar]
  134. Sun XQ, Kang YQ, Bao JG, Zhang YY, Yang YZ, Zhou XB. 134.  2013. Modeling vascularized bone regeneration within a porous biodegradable CaP scaffold loaded with growth factors. Biomaterials 34:4971–81 [Google Scholar]
  135. Edgar LT, Underwood CJ, Guilkey JE, Hoying JB, Weiss JA. 135.  2014. Extracellular matrix density regulates the rate of neovessel growth and branching in sprouting angiogenesis. PLOS ONE 9:e85178 [Google Scholar]
  136. Daub JT, Merks RMH. 136.  2013. A cell-based model of extracellular-matrix-guided endothelial cell migration during angiogenesis. Bull. Math. Biol. 75:1377–99 [Google Scholar]
  137. Bersini S, Gilardi M, Arrigoni C, Talo G, Zamai M. 137.  et al. 2016. Human in vitro 3D co-culture model to engineer vascularized bone-mimicking tissues combining computational tools and statistical experimental approach. Biomaterials 76:157–72 [Google Scholar]
  138. Zermatten E, Vetsch JR, Ruffoni D, Hofmann S, Müller R, Steinfeld A. 138.  2014. Micro–computed tomography based computational fluid dynamics for the determination of shear stresses in scaffolds within a perfusion bioreactor. Ann. Biomed. Eng 421085–94 [Google Scholar]
  139. Nava MM, Raimondi MT, Pietrabissa R. 139.  2013. A multiphysics 3D model of tissue growth under interstitial perfusion in a tissue-engineering bioreactor. Biomech. Model. Mechanobiol. 12:1169–79 [Google Scholar]
  140. Wang X, Phan DT, Sobrino A, George SC, Hughes CC, Lee AP. 140.  2016. Engineering anastomosis between living capillary networks and endothelial cell–lined microfluidic channels. Lab Chip 16:282–90 [Google Scholar]
  141. Itoga K, Okano T. 141.  2010. The high functionalization of temperature-responsive culture dishes for establishing advanced cell sheet engineering. J. Mater. Chem. 20:8768–75 [Google Scholar]
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