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Vascularization in Oral and Maxillofacial Tissue Engineering

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Tissue Engineering in Oral and Maxillofacial Surgery

Abstract

The oral and maxillofacial region is a complex area which contains multiple soft and hard tissue types. While tissue engineering techniques have made significant progress in the regeneration of oral and craniofacial structures, several challenges remain before these techniques can be considered as an appropriate clinical method. One of the major challenges in engineering clinically usable tissue constructs is the inclusion of vascular networks inside the tissues to provide a constant source of oxygen and nutrients to preserve tissue viability. This chapter provides an overview of the mechanisms involved in tissue vascularization and angiogenesis, outlines existing reconstructive techniques and limitations, and reviews current vascularization strategies that have been adopted for tissues.

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Notes

  1. 1.

    The term biocompatible is defined here as the ability of a biomaterial to perform its desired function with respect to a medical therapy, without eliciting any undesirable local or systemic effects in the recipient or beneficiary of that therapy, but generating the most appropriate beneficial cellular or tissue response in that specific situation, and optimizing the clinically relevant performance of that therapy.

  2. 2.

    Shear thinning is the non-Newtonian behavior of fluids whose viscosity decreases under shear strain, thus allowing controlled extrusion from a syringe, and retain their shape fidelity after print.

References

  1. Athirasala A, Lins F, Tahayeri A, Hinds M, Smith AJ, Sedgley C, et al. A novel strategy to engineer pre-vascularized full-length dental pulp-like tissue constructs. Sci Rep. 2017;7:1–11.

    Article  CAS  Google Scholar 

  2. Mao JJ, Giannobile WV, Helms JA, Hollister SJ, Krebsbach PH, Longaker MT, et al. Craniofacial tissue engineering by stem cells. J Dent Res. 2006;85:966–79.

    Article  CAS  PubMed  Google Scholar 

  3. Abou Neel EA, Chrzanowski W, Salih VM, Kim H-W, Knowles JC. Tissue engineering in dentistry. J Dent. 2014;42:915–28.

    Article  CAS  PubMed  Google Scholar 

  4. Tayebi L, Moharamzadeh K. Introduction to oral and dental tissue engineering. In: Biomaterials for oral and dental tissue engineering. Oxford: Woodhead Publishing; 2017. p. 3–6.

    Chapter  Google Scholar 

  5. Rivron NC, Liu J, Rouwkema J, De Boer J, Van Blitterswijk CA. Engineering vascularised tissues in vitro. Eur Cells Mater. 2008;15:27–40.

    Article  CAS  Google Scholar 

  6. Sun X, Altalhi W, Nunes SS. Vascularization strategies of engineered tissues and their application in cardiac regeneration. Adv Drug Deliv Rev. 2016;96:183–94.

    Article  CAS  PubMed  Google Scholar 

  7. Kaully T, Kaufman-Francis K, Lesman A, Levenberg S. Vascularization—the conduit to viable engineered tissues. Tissue Eng Part B Rev. 2009;15:159–69.

    Article  CAS  PubMed  Google Scholar 

  8. Yazdimamaghani M, Gonzalez J. Vascularization. In: Biomaterials for oral and dental tissue engineering. Oxford: Woodhead Publishing; 2017. p. 367–83.

    Chapter  Google Scholar 

  9. Rouwkema J, Rivron NC, van Blitterswijk CA. Vascularization in tissue engineering. Trends Biotechnol. 2008;26:434–41.

    Article  CAS  PubMed  Google Scholar 

  10. Laschke MW, Harder Y, Amon M, Martin I, Farhadi J, Ring A, et al. Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes. Tissue Eng. 2006;12:2093–104.

    Article  CAS  PubMed  Google Scholar 

  11. Utzinger U, Baggett B, Weiss JA, Hoying JB, Edgar LT. Large-scale time series microscopy of neovessel growth during angiogenesis. Angiogenesis. 2015;18:219–32.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Rouwkema J, Khademhosseini A. Vascularization and angiogenesis in tissue engineering: beyond creating static networks. Trends Biotechnol. 2016;34:733–45.

    Article  CAS  PubMed  Google Scholar 

  13. Jain RK, Au P, Tam J, Duda DG, Fukumura D. Engineering vascularized tissue. Nat Biotechnol. 2005;23:821–3.

    Article  CAS  PubMed  Google Scholar 

  14. Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet. 2006;367:1241–6.

    Article  PubMed  Google Scholar 

  15. Moon JJ, West JL. Vascularization of engineered tissues: approaches to promote angio-genesis in biomaterials. Curr Top Med Chem. 2008;8:300–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Shin’oka T, Imai Y, Ikada Y. Transplantation of a tissue-engineered pulmonary artery. N Engl J Med. 2001;344:532–3.

    Article  PubMed  Google Scholar 

  17. Griffith CK, Miller C, Sainson RCA, Calvert JW, Jeon NL, Hughes CCW, et al. Diffusion limits of an in vitro thick prevascularized tissue. Tissue Eng. 2005;11:257–66.

    Article  CAS  PubMed  Google Scholar 

  18. Gauvin R, Guillemette M, Dokmeci M, Khademhosseini A. Application of microtechnologies for the vascularization of engineered tissues. Vasc Cell. 2011;3:1–7.

    Article  CAS  Google Scholar 

  19. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249–57.

    Article  CAS  PubMed  Google Scholar 

  20. Barabaschi GD, Manoharan V, Li Q, Bertassoni LE. Engineering pre-vascularized scaffolds for bone regeneration. Adv Exp Med Biol. 2015;881:79–94.

    Article  CAS  PubMed  Google Scholar 

  21. Bertassoni LE, Cecconi M, Manoharan V, Nikkhah M, Hjortnaes J, Cristino AL, et al. Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab Chip. 2014;14:2202–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Charkoudian N. Mechanisms and modifiers of reflex induced cutaneous vasodilation and vasoconstriction in humans. J Appl Physiol. 2010;109:1221–8.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kim K-W, Song J-H. Emerging roles of lymphatic vasculature in immunity. Immune Netw. 2017;17:68–76.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Mendelsohn ME, Rosano GMC. Nongenomic, ER-mediated activation of endothelial nitric oxide synthase: how does it work? What does it mean? Circ Res. 2000;87:956–60.

    Article  CAS  PubMed  Google Scholar 

  25. Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng. 2007;9:121–67.

    Article  CAS  PubMed  Google Scholar 

  26. Majesky MW, Dong XR, Hoglund V, Mahoney WM, Daum G, Daum G. The adventitia: a dynamic interface containing resident progenitor cells. Arterioscler Thromb Vasc Biol. 2011;31:1530–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Sadler TW. Langman’s medical embryology. 11th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2009.

    Google Scholar 

  28. Mitchell JA, Yochim JM. Intrauterine oxygen tension during the estrous cycle in the rat: its relation to uterine respiration and vascular activity. Endocrinology. 1968;83:701–5.

    Article  CAS  PubMed  Google Scholar 

  29. Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol. 1992;80:283–5.

    CAS  PubMed  Google Scholar 

  30. Djonov VG, Galli AB, Burri PH. Intussusceptive arborization contributes to vascular tree formation in the chick chorio-allantoic membrane. Anat Embryol (Berl). 2000;202:347–57.

    Article  CAS  Google Scholar 

  31. Liu Y, Cox SR, Morita T, Kourembanas S. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5’ enhancer. Circ Res. 1995;77:638–43.

    Article  CAS  PubMed  Google Scholar 

  32. Thurston G, Kitajewski J. VEGF and Delta-Notch: interacting signalling pathways in tumour angiogenesis. Br J Cancer. 2008;99:1204–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Jakobsson L, Franco CA, Bentley K, Collins RT, Ponsioen B, Aspalter IM, et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol. 2010;12:943–53.

    Article  CAS  PubMed  Google Scholar 

  34. Holderfield MT, Hughes CCW. Crosstalk between vascular endothelial growth factor, notch, and transforming growth factor-beta in vascular morphogenesis. Circ Res. 2008;102:637–52.

    Article  CAS  PubMed  Google Scholar 

  35. Eilken HM, Adams RH. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol. 2010;22:617–25.

    Article  CAS  PubMed  Google Scholar 

  36. De Smet F, Segura I, De Bock K, Hohensinner PJ, Carmeliet P. Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler Thromb Vasc Biol. 2009;29:639–49.

    Article  PubMed  CAS  Google Scholar 

  37. Cavallaro U, Liebner S, Dejana E. Endothelial cadherins and tumor angiogenesis. Exp Cell Res. 2006;312:659–67.

    Article  CAS  PubMed  Google Scholar 

  38. Luo Y, Radice GL. N-cadherin acts upstream of VE-cadherin in controlling vascular morphogenesis. J Cell Biol. 2005;169:29–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U, Gerke V, et al. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell. 2007;128:383–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ferrari A, Veligodskiy A, Berge U, Lucas MS, Kroschewski R. ROCK-mediated contractility, tight junctions and channels contribute to the conversion of a preapical patch into apical surface during isochoric lumen initiation. J Cell Sci. 2008;121:3649–63.

    Article  CAS  PubMed  Google Scholar 

  41. Strilić B, Kučera T, Lammert E. Formation of cardiovascular tubes in invertebrates and vertebrates. Cell Mol Life Sci. 2010;67:3209–18.

    Article  PubMed  CAS  Google Scholar 

  42. Iruela-Arispe ML, Davis GE. Cellular and molecular mechanisms of vascular lumen formation. Dev Cell. 2009;16:222–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Sabin FR. Studies on the origin of blood vessels and of red blood corpuscles as seen in the living blastoderm of chicks during the second day of incubation. New York: Johnson Reprint; 1920.

    Google Scholar 

  44. Davis GE, Camarillo CW. An α2β1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp Cell Res. 1996;224:39–51.

    Article  CAS  PubMed  Google Scholar 

  45. Dejana E. Endothelial adherens junctions: implications in the control of vascular permeability and angiogenesis. J Clin Invest. 1996;98:1949–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. le Noble F, Moyon D, Pardanaud L, Yuan L, Djonov V, Matthijsen R, et al. Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development. 2004;131:361–75.

    Article  PubMed  CAS  Google Scholar 

  47. Beck L, D’Amore PA. Vascular development: cellular and molecular regulation. FASEB J. 1997;11:365–73.

    Article  CAS  PubMed  Google Scholar 

  48. Nicosia RF, Villaschi S. Rat aortic smooth muscle cells become pericytes during angiogenesis in vitro. Lab Invest. 1995;73:658–66.

    CAS  PubMed  Google Scholar 

  49. Cimpean A-M, Ribatti D, Raica M. A brief history of angiogenesis assays. Int J Dev Biol. 2011;55:377–82.

    Article  PubMed  Google Scholar 

  50. Muthukkaruppan V, Auerbach R. Angiogenesis in the mouse cornea. Science. 1979;205:1416–8.

    Article  CAS  PubMed  Google Scholar 

  51. Lawson ND, Weinstein BM. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol. 2002;248:307–18.

    Article  CAS  PubMed  Google Scholar 

  52. Auerbach R, Lewis R, Shinners B, Kubai L, Akhtar N. Angiogenesis assays: a critical overview. Clin Chem. 2003;49:32–40.

    Article  CAS  PubMed  Google Scholar 

  53. Moschouris K, Firoozi N, Kang Y. The application of cell sheet engineering in the vascularization of tissue regeneration. Regen Med. 2016;11:559–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Shimizu T, Sekine H, Yang J, Isoi Y, Yamato M, Kikuchi A, et al. Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. FASEB J. 2006;20:708–10.

    Article  CAS  PubMed  Google Scholar 

  55. Zhan W, Marre D, Mitchell GM, Morrison WA, Lim SY. Tissue Engineering by intrinsic vascularization in an in vivo tissue engineering chamber. J Vis Exp. 2016;(111) https://doi.org/10.3791/54099.

  56. Mambally SRT, Santha KK. Utility of arteriovenous loops before free tissue transfer for post-traumatic leg defects. Indian J Plast Surg. 2015;48:38–42.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Englesbe MJ, Al-Holou WN, Moyer AT, Robbins J, Pelletier SJ, Magee J, et al. Single center review of femoral arteriovenous grafts for hemodialysis. World J Surg. 2006;30:171–5.

    Article  PubMed  Google Scholar 

  58. Vlessis AA, Hovaguimian H, Arntson E, Starr A. Use of autologous umbilical artery and vein for vascular reconstruction in the newborn. J Thorac Cardiovasc Surg. 1995;109:854–7.

    Article  CAS  PubMed  Google Scholar 

  59. Kilic M, Aydin U, Sozbilen M, Ozer I, Tamsel S, Demirpolat G, et al. Comparison between allogenic and autologous vascular conduits in the drainage of anterior sector in right living donor liver transplantation. Transpl Int. 2007;20:697–701.

    Article  PubMed  Google Scholar 

  60. Bünger CM, Kröger J, Kock L, Henning A, Klar E, Schareck W. Axillary-axillary interarterial chest loop conduit as an alternative for chronic hemodialysis access. J Vasc Surg. 2005;42:290–5.

    Article  PubMed  Google Scholar 

  61. Gui L, Niklason LE. Vascular tissue engineering: building perfusable vasculature for implantation. Curr Opin Chem Eng. 2014;3:68–74.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Manasseri B, Cuccia G, Moimas S, D’Alcontres FS, Polito F, Bitto A, et al. Microsurgical arterovenous loops and biological templates: a novel in vivo chamber for tissue engineering. Microsurgery. 2007;27:623–9.

    Article  PubMed  Google Scholar 

  63. Leibig N, Wietbrock JO, Bigdeli AK, Horch RE, Kremer T, Kneser U, et al. Flow-induced axial vascularization: the arteriovenous loop in angiogenesis and tissue engineering. Plast Reconstr Surg. 2016;138:825–35.

    Article  CAS  PubMed  Google Scholar 

  64. Lokmic Z, Stillaert F, Morrison WA, Thompson EW, Mitchell GM. An arteriovenous loop in a protected space generates a permanent, highly vascular, tissue-engineered construct. FASEB J. 2007;21:511–22.

    Article  CAS  PubMed  Google Scholar 

  65. Cassell OC, Morrison WA, Messina A, Penington AJ, Thompson EW, Stevens GW, et al. The influence of extracellular matrix on the generation of vascularized, engineered, transplantable tissue. Ann N Y Acad Sci. 2001;944:429–42.

    Article  CAS  PubMed  Google Scholar 

  66. Marrella A, Lee TY, Lee DH, Karuthedom S, Syla D, Chawla A, et al. Engineering vascularized and innervated bone biomaterials for improved skeletal tissue regeneration. Mater Today. 2018;21:362–76.

    Article  CAS  Google Scholar 

  67. Lovett M, Lee K, Edwards A, Kaplan DL. Vascularization strategies for tissue engineering. Tissue Eng Part B Rev. 2009;15:353–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Morritt AN, Bortolotto SK, Dilley RJ, Han X, Kompa AR, McCombe D, et al. Cardiac tissue engineering in an in vivo vascularized chamber. Circulation. 2007;115:353–60.

    Article  PubMed  Google Scholar 

  69. Boos AM, Loew JS, Weigand A, Deschler G, Klumpp D, Arkudas A, et al. Engineering axially vascularized bone in the sheep arteriovenous-loop model. J Tissue Eng Regen Med. 2013;7:654–64.

    Article  CAS  PubMed  Google Scholar 

  70. Tanaka Y, Tsutsumi A, Crowe DM, Tajimat S, Morrison WA. Generation of an autologous tissue (matrix) flap by combining an arteriovenous shunt loop with artificial skin in rats: preliminary report. Br J Plast Surg. 2000;53:51–7.

    Article  CAS  PubMed  Google Scholar 

  71. Ren LL, Ma DY, Feng X, Mao TQ, Liu YP, Ding Y. A novel strategy for prefabrication of large and axially vascularized tissue engineered bone by using an arteriovenous loop. Med Hypotheses. 2008;71:737–40.

    Article  CAS  PubMed  Google Scholar 

  72. Balasundaram I, Al-Hadad I, Parmar S. Recent advances in reconstructive oral and maxillofacial surgery. Br J Oral Maxillofac Surg. 2012;50:695–705.

    Article  PubMed  Google Scholar 

  73. Hallock GG. The complete classification of flaps. Microsurgery. 2004;24:157–61.

    Article  PubMed  Google Scholar 

  74. Kroll SS, Schusterman MA, Reece GP, Miller MJ, Evans GR, Robb GL, et al. Choice of flap and incidence of free flap success. Plast Reconstr Surg. 1996;98:459–63.

    Article  CAS  PubMed  Google Scholar 

  75. Knackstedt R, Aliotta R, Gatherwright J, Djohan R, Gastman B, Schwarz G, et al. Single-stage versus two-stage arteriovenous loop microsurgical reconstruction: a meta-analysis of the literature. Microsurgery. 2018;38(6):706–17. https://doi.org/10.1002/micr.30204.

    Article  PubMed  Google Scholar 

  76. Cho HE, Roh S, Lee NH, Yang KM. Breakthrough technique for free tissue transfer of poorly vascularized lower extremity: arteriovenous loop revisited. Arch Plast Surg. 2015;42:652–5.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Ayad WM, Mohammed AH, Ismail HM, Osama Ouf M, Elbatawy AM. Arteriovenous loop grafts for free tissue transfer in complex lower limb defects. Plast Reconstr Surg. 2017;41:159–64.

    Google Scholar 

  78. Taeger CD, Arkudas A, Beier JP, Horch RE. Emergency arterio-venous loop for free-flap defect reconstruction of the lower thigh with a post-irradiated and heavily infected wound. Int Wound J. 2015;12:598–600.

    Article  PubMed  Google Scholar 

  79. Meyer A, Horch RE, Schoengart E, Beier JP, Taeger CD, Arkudas A, et al. Results of combined vascular reconstruction by means of AV loops and free flap transfer in patients with soft tissue defects. J Plast Reconstr Aesthet Surg. 2016;69:545–53.

    Article  PubMed  Google Scholar 

  80. Popoola J, Greene H, Kyegombe M, MacPhee IA. Patient involvement in selection of immunosuppressive regimen following transplantation. Patient Prefer Adherence. 2014;8:1705–12.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Scandling JD, Busque S, Shizuru JA, Lowsky R, Hoppe R, Dejbakhsh-Jones S, et al. Chimerism, graft survival, and withdrawal of immunosuppressive drugs in HLA matched and mismatched patients after living donor kidney and hematopoietic cell transplantation. Am J Transplant. 2015;15:695–704.

    Article  CAS  PubMed  Google Scholar 

  82. Borenstein JT, Terai H, King KR, Weinberg EJ, Kaazempur-Mofrad MR, Vacanti JP. Microfabrication technology for vascularized tissue engineering. Biomed Microdevices. 2002;4:167–75.

    Article  CAS  Google Scholar 

  83. Jabbarzadeh E, Blanchette J, Shazly T, Khademhosseini A, Camci-Unal G, Laurencin C. Vascularization of biomaterials for bone tissue engineering: current approaches and major challenges. Curr Angiogenesise. 2012;1:180–91.

    Article  CAS  Google Scholar 

  84. Peters MC, Polverini PJ, Mooney DJ. Engineering vascular networks in porous polymer matrices. J Biomed Mater Res. 2002;60:668–78.

    Article  CAS  PubMed  Google Scholar 

  85. Salehi-Nik N, Rezai Rad M, Nazeman P, Khojasteh A. Polymers for oral and dental tissue engineering. In: Biomaterials for oral and dental tissue engineering. Oxford: Woodhead Publishing; 2017. p. 25–46.

    Chapter  Google Scholar 

  86. Oh SH, Park IK, Kim JM, Lee JH. In vitro and in vivo characteristics of PCL scaffolds with pore size gradient fabricated by a centrifugation method. Biomaterials. 2007;28:1664–71.

    Article  CAS  PubMed  Google Scholar 

  87. Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials. 2005;26:5474–91.

    Article  CAS  PubMed  Google Scholar 

  88. Nguyen LH, Annabi N, Nikkhah M, Bae H, Binan L, Park S, et al. Vascularized bone tissue engineering: approaches for potential improvement. Tissue Eng Part B Rev. 2012;18:363–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Harris GM, Rutledge K, Cheng Q, Blanchette J, Jabbarzadeh E. Strategies to direct angiogenesis within scaffolds for bone tissue engineering. Curr Pharm Des. 2013;19:3456–65.

    Article  CAS  PubMed  Google Scholar 

  90. Kim K, Yeatts A, Dean D, Fisher JP. Stereolithographic bone scaffold design parameters: osteogenic differentiation and signal expression. Tissue Eng Part B Rev. 2010;16:523–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Yang S, Leong K-F, Du Z, Chua C-K. The design of scaffolds for use in tissue engineering. Part I. Traditional factors. Tissue Eng. 2001;7:679–89.

    Article  CAS  PubMed  Google Scholar 

  92. Rouwkema J, Koopman BFJM, Blitterswijk CAV, Dhert WJA, Malda J. Supply of nutrients to cells in engineered tissues. Biotechnol Genet Eng Rev. 2009;26:163–78.

    Article  Google Scholar 

  93. Bégin-drolet A, Dussault M, Fernandez SA, Larose-dutil J, Leask RL, Hoesli CA, et al. Design of a 3D printer head for additive manufacturing of sugar glass for tissue engineering applications. Addit Manuf. 2017;15:29–39.

    Article  CAS  Google Scholar 

  94. Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen D-HT, Cohen DM, et al. Rapid casting of patterned vascular networks for perfusable engineered 3D tissues. 2013;11:768–74.

    Google Scholar 

  95. Nazhat SN, Abou Neel EA, Kidane A, Ahmed I, Hope C, Kershaw M, et al. Controlled microchannelling in dense collagen scaffolds by soluble phosphate glass fibers. Biomacromolecules. 2007;8:543–51.

    Article  CAS  PubMed  Google Scholar 

  96. Sarkar S, Lee GY, Wong JY, Desai TA. Development and characterization of a porous micro-patterned scaffold for vascular tissue engineering applications. Biomaterials. 2006;27:4775–82.

    Article  CAS  PubMed  Google Scholar 

  97. Lee KY, Mooney DJ. Hydrogels for tissue engineering. Chem. Rev. 2001;101:1869–79.

    Article  CAS  PubMed  Google Scholar 

  98. Hasan A, Paul A, Vrana NE, Zhao X, Memic A, Hwang YS, et al. Microfluidic techniques for development of 3D vascularized tissue. Biomaterials. 2014;35:7308–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Sheridan MH, Shea LD, Peters MC, Mooney DJ. Bioabsorbable polymer scaffolds for tissue engineering capable of sustained growth factor delivery. J Control Release. 2000;64:91–102.

    Article  CAS  PubMed  Google Scholar 

  100. Perets A, Baruch Y, Weisbuch F, Shoshany G, Neufeld G, Cohen S. Enhancing the vascularization of three-dimensional porous alginate scaffolds by incorporating controlled release basic fibroblast growth factor microspheres. J Biomed Mater Res. 2003;65A:489–97.

    Article  CAS  Google Scholar 

  101. Doi K, Ikeda T, Marui A, Kushibiki T, Arai Y, Hirose K, et al. Enhanced angiogenesis by gelatin hydrogels incorporating basic fibroblast growth factor in rabbit model of hind limb ischemia. Heart Vessels. 2007;22:104–8.

    Article  PubMed  Google Scholar 

  102. Jiang B, Brey EM. Formation of stable vascular networks in engineered tissues. In: Regenerative medicine and tissue engineering—cells and biomaterials. Rijeka: InTech; 2011. p. 477–502.

    Google Scholar 

  103. Wissink MJ, Beernink R, Pieper J, Poot A, Engbers GH, Beugeling T, et al. Binding and release of basic fibroblast growth factor from heparinized collagen matrices. Biomaterials. 2001;22:2291–9.

    Article  CAS  PubMed  Google Scholar 

  104. Singh S, Wu BM, Dunn JCY. The enhancement of VEGF-mediated angiogenesis by polycaprolactone scaffolds with surface cross-linked heparin. Biomaterials. 2011;32:2059–69.

    Article  CAS  PubMed  Google Scholar 

  105. Liu H, Hongbin F, Cui Y, Chen Y, Yao K, Goh JCH. Effects of the controlled-released basic fibroblast growth factor from chitosan−gelatin microspheres on human fibroblasts cultured on a chitosan−gelatin scaffold. Biomacromolecules. 2007;8:1446–55.

    Article  CAS  PubMed  Google Scholar 

  106. Formiga FR, Pelacho B, Garbayo E, Abizanda G, Gavira JJ, Simon-Yarza T, et al. Sustained release of VEGF through PLGA microparticles improves vasculogenesis and tissue remodeling in an acute myocardial ischemia–reperfusion model. J Control Release. 2010;147:30–7.

    Article  CAS  PubMed  Google Scholar 

  107. Subbiah R, Hwang MP, Van SY, Do SH, Park H, Lee K, et al. Osteogenic/angiogenic dual growth factor delivery microcapsules for regeneration of vascularized bone tissue. Adv Healthc Mater. 2015;4:1982–92.

    Article  CAS  PubMed  Google Scholar 

  108. Huang Y-C, Kaigler D, Rice KG, Krebsbach PH, Mooney DJ. Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell-driven bone regeneration. J Bone Miner Res. 2004;20:848–57.

    Article  PubMed  CAS  Google Scholar 

  109. Sun Q, Silva EA, Wang A, Fritton JC, Mooney DJ, Schaffler MB, et al. Sustained release of multiple growth factors from injectable polymeric system as a novel therapeutic approach towards angiogenesis. Pharm Res. 2010;27:264–71.

    Article  CAS  PubMed  Google Scholar 

  110. Richardson TP, Peters MC, Ennett AB, Mooney DJ. Polymeric system for dual growth factor delivery. Nat Biotechnol. 2001;19:1029–34.

    Article  CAS  PubMed  Google Scholar 

  111. Chiu LLY, Radisic M. Scaffolds with covalently immobilized VEGF and angiopoietin-1 for vascularization of engineered tissues. Biomaterials. 2010;31:226–41.

    Article  CAS  PubMed  Google Scholar 

  112. Bleiziffer O, Eriksson E, Yao F, Horch RE, Kneser U. Gene transfer strategies in tissue engineering. J Cell Mol Med. 2007;11:206–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Chary SR, Jain RK, Zisch AH, Boschetti F, Swartz MA. Direct measurement of interstitial convection and diffusion of albumin in normal and neoplastic tissues by fluorescence photobleaching. Proc Natl Acad Sci U S A. 1989;86:5385–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Pola R, Ling LE, Silver M, Corbley MJ, Kearney M, Blake Pepinsky R, et al. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat Med. 2001;7:706–11.

    Article  CAS  PubMed  Google Scholar 

  115. Jabbarzadeh E, Starnes T, Khan YM, Jiang T, Wirtel AJ, Deng M, et al. Induction of angiogenesis in tissue-engineered scaffolds designed for bone repair: a combined gene therapy-cell transplantation approach. Proc Natl Acad Sci U S A. 2008;105:11099–104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Malda J, Rouwkema J, Martens DE, le Comte EP, Kooy FK, Tramper J, et al. Oxygen gradients in tissue-engineered Pegt/Pbt cartilaginous constructs: measurement and modeling. Biotechnol Bioeng. 2004;86:9–18.

    Article  CAS  PubMed  Google Scholar 

  117. Deleu J, Trueta J. Vascularisation of bone grafts in the anterior chamber of the eye. Bone Joint J. 1965;47B:319–29.

    Google Scholar 

  118. Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, et al. Engineering vascularized skeletal muscle tissue. Nat Biotechnol. 2005;23:879–84.

    Article  CAS  PubMed  Google Scholar 

  119. Rouwkema J, De BJ, Van Blitterswijk CA. Endothelial cells assemble into a 3-dimensional prevascular network in a bone tissue engineering construct. Tissue Eng. 2006;12:2685–93.

    Article  CAS  PubMed  Google Scholar 

  120. Nehls V, Herrmann R, Hühnken M. Guided migration as a novel mechanism of capillary network remodeling is regulated by basic fibroblast growth factor. Histochem Cell Biol. 1998;109:319–29.

    Article  CAS  PubMed  Google Scholar 

  121. Brey EM, Uriel S, Greisler HP, McIntire LV. Therapeutic neovascularization: contributions from bioengineering. Tissue Eng. 2005;11:567–84.

    Article  CAS  PubMed  Google Scholar 

  122. Tremblay P-L, Hudon V, Berthod F, Germain L, Auger FA. Inosculation of tissue-engineered capillaries with the host’s vasculature in a reconstructed skin transplanted on mice. Am J Transplant. 2005;5:1002–10.

    Article  PubMed  Google Scholar 

  123. Rubina K, Kalinina N, Efimenko A, Lopatina T, Melikhova V, Tsokolaeva Z, et al. Adipose stromal cells stimulate angiogenesis via promoting progenitor cell differentiation, secretion of angiogenic factors, and enhancing vessel maturation. Tissue Eng Part A. 2009;15:2039–50.

    Article  CAS  PubMed  Google Scholar 

  124. Jain RK. Molecular regulation of vessel maturation. Nat Med. 2003;9:685–93.

    Article  CAS  PubMed  Google Scholar 

  125. Sukmana I. Microvascular guidance: a challenge to support the development of vascularised tissue engineering construct. Sci World J. 2012;2012:1–10.

    Article  CAS  Google Scholar 

  126. Melero-Martin JM, De Obaldia ME, Kang S-Y, Khan ZA, Yuan L, Oettgen P, et al. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res. 2008;103:194–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Correia C, Grayson WL, Park M, Hutton D, Zhou B, Guo XE, et al. In vitro model of vascularized bone: synergizing vascular development and osteogenesis. PLoS One. 2011;6:e28352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Lesman A, Koffler J, Atlas R, Blinder YJ, Kam Z, Levenberg S. Engineering vessel-like networks within multicellular fibrin-based constructs. Biomaterials. 2011;32:7856–69.

    Article  CAS  PubMed  Google Scholar 

  129. Kirkpatrick CJ, Fuchs S, Unger RE. Co-culture systems for vascularization—learning from nature. Adv Drug Deliv Rev. 2011;63:291–9.

    Article  CAS  PubMed  Google Scholar 

  130. Salehi-Nik N, Rezai Rad M, Kheiri L, Nazeman P, Nadjmi N, Khojasteh A. Buccal fat pad as a potential source of stem cells for bone regeneration: a literature review. Stem Cells Int. 2017;2017:1–13.

    Article  CAS  Google Scholar 

  131. Ball SG, Shuttleworth AC, Kielty CM. Direct cell contact influences bone marrow mesenchymal stem cell fate. Int J Biochem Cell Biol. 2004;36:714–27.

    Article  CAS  PubMed  Google Scholar 

  132. Bidarra SJ, Barrias CC, Barbosa MA, Soares R, Amédée J, Granja PL. Phenotypic and proliferative modulation of human mesenchymal stem cells via crosstalk with endothelial cells. Stem Cell Res. 2011;7:186–97.

    Article  PubMed  Google Scholar 

  133. Kaigler D, Krebsbach PH, Wang Z, West ER, Horger K, Mooney DJ. Transplanted endothelial cells enhance orthotopic bone regeneration. J Dent Res. 2006;85:633–7.

    Article  CAS  PubMed  Google Scholar 

  134. Brey EM, McIntire LV, Johnston CM, Reece GP, Patrick CW. Three-dimensional, quantitative analysis of desmin and smooth muscle alpha actin expression during angiogenesis. Ann Biomed Eng. 2004;32:1100–7.

    Article  PubMed  Google Scholar 

  135. Folkman J, Haudenschild C. Angiogenesis in vitro. Nature. 1980;288:551–6.

    Article  CAS  PubMed  Google Scholar 

  136. Montesano R, Orci L, Vassalli P. In vitro rapid organization of endothelial cells into capillary-like networks is promoted by collagen matrices. J Cell Biol. 1983;97:1648–52.

    Article  CAS  PubMed  Google Scholar 

  137. Kim S, Lee H, Chung M, Jeon NL. Engineering of functional, perfusable 3D microvascular networks on a chip. Lab Chip. 2013;13:1489.

    Article  CAS  PubMed  Google Scholar 

  138. Hsu Y-H, Moya ML, Abiri P, Hughes CCW, George SC, Lee AP. Full range physiological mass transport control in 3D tissue cultures. Lab Chip. 2013;13:81–9.

    Article  CAS  PubMed  Google Scholar 

  139. Moya ML, Hsu Y-H, Lee AP, Hughes CCW, George SC. In vitro perfused human capillary networks. Tissue Eng Part C Methods. 2013;19:730–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Athirasala A, Lins F, Tahayeri A, Hinds M, Smith AJ, Sedgley C, et al. A Novel strategy to engineer pre-vascularized full-length dental pulp-like tissue constructs. Sci Rep. 2017;7:3323.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  141. Pedersen TO, Blois AL, Xing Z, Xue Y, Sun Y, Finne-Wistrand A, et al. Endothelial microvascular networks affect gene-expression profiles and osteogenic potential of tissue-engineered constructs. Stem Cell Res Ther. 2013;4:52.

    Article  PubMed  PubMed Central  Google Scholar 

  142. Grellier M, Granja PL, Fricain J-C, Bidarra SJ, Renard M, Bareille R, et al. The effect of the co-immobilization of human osteoprogenitors and endothelial cells within alginate microspheres on mineralization in a bone defect. Biomaterials. 2009;30:3271–8.

    Article  CAS  PubMed  Google Scholar 

  143. Terramani TT, Eton D, Bui PA, Wang Y, Fred A, Yu H. Human macrovascular endothelial cells: optimazation of culture conditions. In Vitro Cell Dev Biol. 2000;36:125–32.

    Article  CAS  Google Scholar 

  144. Craig LE, Spelman JP, Strandberg JD, Zink MC. Endothelial cells from diverse tissues exhibit differences in growth and morphology. Microvasc Res. 1998;55:65–76.

    Article  CAS  PubMed  Google Scholar 

  145. Lang I, Pabst MA, Hiden U, Blaschitz A, Dohr G, Hahn T, et al. Heterogeneity of microvascular endothelial cells isolated from human term placenta and macrovascular umbilical vein endothelial cells. Eur J Cell Biol. 2003;82:163–73.

    Article  PubMed  Google Scholar 

  146. Xing Z, Xue Y, Finne-Wistrand A, Yang Z-Q, Mustafa K. Copolymer cell/scaffold constructs for bone tissue engineering: co-culture of low ratios of human endothelial and osteoblast-like cells in a dynamic culture system. J Biomed Mater Res Part A. 2013;101A:1113–20.

    Article  CAS  Google Scholar 

  147. Chen Y-C, Lin R-Z, Qi H, Yang Y, Bae H, Melero-Martin JM, et al. Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels. Adv Funct Mater. 2012;22:2027–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Whitesides GM, Grzybowski B. Self-assembly at all scales. Science. 2002;295:2418–21.

    Article  CAS  PubMed  Google Scholar 

  149. Timmins NE, Nielsen LK. Generation of multicellular tumor spheroids by the hanging-drop method. Methods Mol Med. 2007;140:141–51.

    Article  CAS  PubMed  Google Scholar 

  150. Granato G, Ruocco MR, Iaccarino A, Masone S, Calì G, Avagliano A, et al. Generation and analysis of spheroids from human primary skin myofibroblasts: an experimental system to study myofibroblasts deactivation. Cell Death Discov. 2017;3:17038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Fayol D, Frasca G, Le Visage C, Gazeau F, Luciani N, Wilhelm C. Use of magnetic forces to promote stem cell aggregation during differentiation, and cartilage tissue modeling. Adv Mater. 2013;25:2611–6.

    Article  CAS  PubMed  Google Scholar 

  152. Desroches BR, Zhang P, Choi B-R, King ME, Maldonado AE, Li W, et al. Functional scaffold-free 3-D cardiac microtissues: a novel model for the investigation of heart cells. Am J Physiol Circ Physiol. 2012;302:2031–42.

    Article  CAS  Google Scholar 

  153. Fukuda J, Nakazawa K. Orderly arrangement of hepatocyte spheroids on a microfabricated chip. Tissue Eng. 2005;11:1254–62.

    Article  CAS  PubMed  Google Scholar 

  154. Bhang SH, Cho S-W, La W-G, Lee T-J, Yang HS, Sun A-Y, et al. Angiogenesis in ischemic tissue produced by spheroid grafting of human adipose-derived stromal cells. Biomaterials. 2011;32:2734–47.

    Article  CAS  PubMed  Google Scholar 

  155. Skiles ML, Sahai S, Rucker L, Blanchette JO. Use of culture geometry to control hypoxia-induced vascular endothelial growth factor secretion from adipose-derived stem cells: optimizing a cell-based approach to drive vascular growth. Tissue Eng Part A. 2013;19:2330–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Mironov V, Zhang J, Gentile C, Brakke K, Trusk T, Jakab K, et al. Designer ‘blueprint’ for vascular trees: morphology evolution of vascular tissue constructs. Virtual Phys Prototyp. 2009;4:63–74.

    Article  Google Scholar 

  157. Fennema E, Rivron N, Rouwkema J, van Blitterswijk C, de Boer J. Spheroid culture as a tool for creating 3D complex tissues. Trends Biotechnol. 2013;31:108–15.

    Article  CAS  PubMed  Google Scholar 

  158. Laschke MW, Menger MD. Spheroids as vascularization units: from angiogenesis research to tissue engineering applications. Biotechnol Adv. 2017;35:782–91.

    Article  CAS  PubMed  Google Scholar 

  159. Kelm JM, Djonov V, Ittner LM, Fluri D, Born W, Hoerstrup SP, et al. Design of custom-shaped vascularized tissues using microtissue spheroids as minimal building units. Tissue Eng. 2006;12:2151–60.

    Article  PubMed  Google Scholar 

  160. Alajati A, Laib AM, Weber H, Boos AM, Bartol A, Ikenberg K, et al. Spheroid-based engineering of a human vasculature in mice. Nat Methods. 2008;5:439–45.

    Article  CAS  PubMed  Google Scholar 

  161. Takahashi Y, Sekine K, Kin T, Takebe T, Taniguchi H. Self-condensation culture enables vascularization of tissue fragments for efficient therapeutic transplantation. Cell Rep. 2018;23:1620–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Bauman E, Feijão T, Carvalho DTO, Granja PL, Barrias CC. Xeno-free pre-vascularized spheroids for therapeutic applications. Sci Rep. 2018;8:230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Klingelhutz AJ, Gourronc FA, Chaly A, Wadkins DA, Burand AJ, Markan KR, et al. Scaffold-free generation of uniform adipose spheroids for metabolism research and drug discovery. Sci Rep. 2018;8:523.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  164. Bartz C, Meixner M, Giesemann P, Roël G, Bulwin G-C, Smink JJ. An ex vivo human cartilage repair model to evaluate the potency of a cartilage cell transplant. J Transl Med. 2016;14:317.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  165. Becher C, Laute V, Fickert S, Zinser W, Niemeyer P, John T, et al. Safety of three different product doses in autologous chondrocyte implantation: results of a prospective, randomised, controlled trial. J Orthop Surg Res. 2017;12:71.

    Article  PubMed  PubMed Central  Google Scholar 

  166. Kwon OH, Kikuchi A, Yamato M, Sakurai Y, Okano T. Rapid cell sheet detachment from Poly(N-isopropylacrylamide)-grafted porous cell culture membranes. J Biomed Mater Res. 2000;50:82–9.

    Article  CAS  PubMed  Google Scholar 

  167. Yang J, Yamato M, Kohno C, Nishimoto A, Sekine H, Fukai F, et al. Cell sheet engineering: recreating tissues without biodegradable scaffolds. Biomaterials. 2005;26:6415–22.

    Article  CAS  PubMed  Google Scholar 

  168. Nishida K, Yamato M, Hayashida Y, Watanabe K, Maeda N, Watanabe H, et al. Functional bioengineered corneal epithelial sheet grafts from corneal stem cells expanded ex vivo on a temperature-responsive cell culture surface. Transplantation. 2004;77:379–85.

    Article  PubMed  Google Scholar 

  169. Yong-Shun See E, Lok Toh S, Cho Hong Goh J. Multilineage potential of bone-marrow-derived mesenchymal stem cell sheets: implications for tissue engineering. Tissue Eng Part A. 2010;16:1421–31.

    Article  Google Scholar 

  170. Takahashi H, Nakayama M, Shimizu T, Yamato M, Okano T. Anisotropic cell sheets for constructing three-dimensional tissue with well-organized cell orientation. Biomaterials. 2011;32:8830–8.

    Article  CAS  PubMed  Google Scholar 

  171. Yang J, Yamato M, Shimizu T, Sekine H, Ohashi K, Kanzaki M, et al. Reconstruction of functional tissues with cell sheet engineering. Biomaterials. 2007;28:5033–43.

    Article  CAS  PubMed  Google Scholar 

  172. Berner A, Henkel J, Woodruff MA, Steck R, Nerlich M, Schuetz MA, et al. Delayed minimally invasive injection of allogenic bone marrow stromal cell sheets regenerates large bone defects in an ovine preclinical animal model. Stem Cells Transl Med. 2015;4:503–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Tsumanuma Y, Iwata T, Washio K, Yoshida T, Yamada A, Takagi R, et al. Comparison of different tissue-derived stem cell sheets for periodontal regeneration in a canine 1-wall defect model. Biomaterials. 2011;32:5819–25.

    Article  CAS  PubMed  Google Scholar 

  174. Takagi R, Murakami D, Kondo M, Ohki T, Sasaki R, Mizutani M, et al. Fabrication of human oral mucosal epithelial cell sheets for treatment of esophageal ulceration by endoscopic submucosal dissection. Gastrointest Endosc. 2010;72:1253–9.

    Article  PubMed  Google Scholar 

  175. Hasegawa M, Yamato M, Kikuchi A, Okano T, Ishikawa I. Human periodontal ligament cell sheets can regenerate periodontal ligament tissue in an athymic rat model. Tissue Eng. 2005;11:469–78.

    Article  CAS  PubMed  Google Scholar 

  176. Ryu B, Sekine H, Honma J, Kobayashi T, Kobayashi E, Kawamata T, et al. Adipose derived mesenchymal stromal cell sheet transplantation induces functional angiogenesis and enhances endogenous neurogenesis in a rat stroke model. Stroke. 2018;49

    Google Scholar 

  177. Chen C-H, Chang C-H, Liu H-W, Whu S-W, Chen S-H, Tsai C-L, et al. Bioengineered periosteal progenitor cell sheets to enhance tendon-bone healing in a bone tunnel. At a Glance Commentary. Biomed J. 2012;35:473–80.

    Article  PubMed  Google Scholar 

  178. Geng W, Ma D, Yan X, Liu L, Cui J, Xie X, et al. Engineering tubular bone using mesenchymal stem cell sheets and coral particles. Biochem Biophys Res Commun. 2013;433:595–601.

    Article  CAS  PubMed  Google Scholar 

  179. Iwata T, Yamato M, Tsuchioka H, Takagi R, Mukobata S, Washio K, et al. Periodontal regeneration with multi-layered periodontal ligament-derived cell sheets in a canine model. Biomaterials. 2009;30:2716–23.

    Article  CAS  PubMed  Google Scholar 

  180. Asakawa N, Shimizu T, Tsuda Y, Sekiya S, Sasagawa T, Yamato M, et al. Pre-vascularization of in vitro three-dimensional tissues created by cell sheet engineering. Biomaterials. 2010;31:3903–9.

    Article  CAS  PubMed  Google Scholar 

  181. Sakaguchi K, Shimizu T, Okano T. Construction of three-dimensional vascularized cardiac tissue with cell sheet engineering. J Control Release. 2015;205:83–8.

    Article  CAS  PubMed  Google Scholar 

  182. Costa M, Pirraco RP, Cerqueira MT, Reis RL, Marques AP. Growth factor-free pre-vascularization of cell sheets for tissue engineering. New York: Humana Press; 2016. p. 219–26.

    Google Scholar 

  183. Wu RX, Bi CS, Yu Y, Zhang LL, Chen FM. Age-related decline in the matrix contents and functional properties of human periodontal ligament stem cell sheets. Acta Biomater. 2015;22:70–82.

    Article  CAS  PubMed  Google Scholar 

  184. Chen KG, Mallon BS, McKay RDG, Robey PG. Human pluripotent stem cell culture: considerations for maintenance, expansion, and therapeutics. Cell Stem Cell. 2014;14:13–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Nakajima R, Kobayashi T, Moriya N, Mizutani M, Kan K, Nozaki T, et al. A novel closed cell culture device for fabrication of corneal epithelial cell sheets. J Tissue Eng Regen Med. 2015;9:1259–67.

    Article  CAS  PubMed  Google Scholar 

  186. Yoshikawa Y, Miyagawa S, Toda K, Saito A, Sakata Y, Sawa Y. Myocardial regenerative therapy using a scaffold-free skeletal-muscle-derived cell sheet in patients with dilated cardiomyopathy even under a left ventricular assist device: a safety and feasibility study. Surg Today. 2018;48:200–10.

    Article  CAS  PubMed  Google Scholar 

  187. Miyagawa S, Domae K, Yoshikawa Y, Fukushima S, Nakamura T, Saito A, et al. Phase I clinical trial of autologous stem cell-sheet transplantation therapy for treating cardiomyopathy. J Am Heart Assoc. 2017;6:1–12.

    Article  Google Scholar 

  188. Yui Y. Concerns on a new therapy for severe heart failure using cell sheets with skeletal muscle or myocardial cells from iPS cells in Japan. Regen Med. 2018;7:1–2.

    Google Scholar 

  189. Mironov V, Trusk T, Kasyanov V, Little S, Swaja R, Markwald R. Biofabrication: a 21st century manufacturing paradigm. Biofabrication. 2009;1:022001.

    Article  CAS  PubMed  Google Scholar 

  190. Kolesky DB, Homan KA, Skylar-Scott MA, Lewis JA. Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci. 2016;113:3179–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Justin AW, Brooks RA, Markaki AE. Multi-casting approach for vascular networks in cellularized hydrogels. J R Soc Interface. 2016;13:20160768.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  192. Tocchio A, Tamplenizza M, Martello F, Gerges I, Rossi E, Argentiere S, et al. Versatile fabrication of vascularizable scaffolds for large tissue engineering in bioreactor. Biomaterials. 2015;45:124–31.

    Article  CAS  PubMed  Google Scholar 

  193. Kleinman HK, Martin GR. Matrigel: Basement membrane matrix with biological activity. Semin Cancer Biol. 2005;15:378–86.

    Article  CAS  PubMed  Google Scholar 

  194. Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32:773–85.

    Article  CAS  PubMed  Google Scholar 

  195. Mori N, Morimoto Y, Takeuchi S. Skin integrated with perfusable vascular channels on a chip. Biomaterials. 2017;116:48–56.

    Article  CAS  PubMed  Google Scholar 

  196. Rolland JP, Hagberg EC, Denison GM, Carter KR, De Simone JM. High-resolution soft lithography: enabling materials for nanotechnologies. Angew Chemie Int Ed. 2004;43:5796–9.

    Article  CAS  Google Scholar 

  197. Xia Y, Whitesides GM. Soft Lithography. Angew Chemie Int Ed. 1998;37:550–75.

    Article  CAS  Google Scholar 

  198. Dy AJ, Cosmanescu A, Sluka J, Glazier JA, Stupack D, Amarie D. Fabricating microfluidic valve master molds in SU-8 photoresist. J Micromech Microeng. 2014;24:57001–7.

    Article  CAS  Google Scholar 

  199. Lake M, Lake M, Narciso C, Cowdrick K, Storey T, Zhang S, et al. Microfluidic device design, fabrication, and testing protocols. Protoc Exch. 2015; https://doi.org/10.1038/protex.2015.069.

  200. Nashimoto Y, Hayashi T, Kunita I, Nakamasu A, Torisawa Y, Nakayama M, et al. Integrating perfusable vascular networks with a three-dimensional tissue in a microfluidic device. Integr Biol. 2017;9:506–18.

    Article  Google Scholar 

  201. Malak ST, Liang G, Thevamaran R, Yoon YJ, Smith MJ, Jung J, et al. High-resolution quantum dot photopatterning via interference lithography assisted microstamping. J Phys Chem C. 2017;121:13370–80.

    Article  CAS  Google Scholar 

  202. Aubin H, Nichol JW, Hutson CB, Bae H, Sieminski AL, Cropek DM, et al. Directed 3D cell alignment and elongation in microengineered hydrogels. Biomaterials. 2010;31:6941–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  203. Khetan S, Burdick JA. Patterning network structure to spatially control cellular remodeling and stem cell fate within 3-dimensional hydrogels. Biomaterials. 2010;31:8228–34.

    Article  CAS  PubMed  Google Scholar 

  204. Shu XZ, Ahmad S, Liu Y, Prestwich GD. Synthesis and evaluation of injectable, in situ crosslinkable synthetic extracellular matrices for tissue engineering. J Biomed Mater Res Part A. 2006;79A:902–12.

    Article  CAS  Google Scholar 

  205. Shu XZ, Liu Y, Palumbo F, Prestwich GD. Disulfide-crosslinked hyaluronan-gelatin hydrogel films: a covalent mimic of the extracellular matrix for in vitro cell growth. Biomaterials. 2003;24:3825–34.

    Article  CAS  PubMed  Google Scholar 

  206. Huebsch N, Arany PR, Mao AS, Shvartsman D, Ali OA, Bencherif SA, et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater. 2010;9:518–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Williams CG, Malik AN, Kim TK, Manson PN, Elisseeff JH. Variable cytocompatibility of six cell lines with photoinitiators used for polymerizing hydrogels and cell encapsulation. Biomaterials. 2005;26:1211–8.

    Article  CAS  PubMed  Google Scholar 

  208. Shao J, Huang Y, Fan Q. Visible light initiating systems for photopolymerization: status, development and challenges. Polym Chem. 2014;5:4195–210.

    Article  CAS  Google Scholar 

  209. Hribar KC, Soman P, Warner J, Chung P, Chen S. Light-assisted direct-write of 3D functional biomaterials. Lab Chip. 2014;14:268–75.

    Article  CAS  PubMed  Google Scholar 

  210. Soman P, Fozdar DY, Lee JW, Phadke A, Varghese S, Chen S. A three-dimensional polymer scaffolding material exhibiting a zero Poisson’s ratio. Soft Matter. 2012;8:4946–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Moldovan NI. Progress in scaffold-free bioprinting for cardiovascular medicine. J Cell Mol Med. 2018;22:2964–9.

    Article  PubMed  PubMed Central  Google Scholar 

  212. Hinton TJ, Jallerat Q, Palchesko RN, Park JH, Grodzicki MS, Shue HJ, et al. Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. Sci Adv. 2015;1(9):e1500758.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  213. Zhang Y, Yu Y, Chen H, Ozbolat IT. Characterization of printable cellular micro-fluidic channels for tissue engineering related content in vitro evaluation of carbon-nanotube-reinforced bioprintable vascular conduits. Biofabrication. 2013;5:1–11.

    Google Scholar 

  214. Verseijden F, Sluijs SJP-V, Van Neck JW, Hofer SOP, Hovius SER, Van Osch GJVM. Comparing scaffold-free and fibrin-based adipose-derived stromal cell constructs for adipose tissue engineering: an in vitro and in vivo study. Cell Transplant. 2012;21:2283–97.

    Article  PubMed  Google Scholar 

  215. Hu N, Zhang YS. 3D bioprinting blood vessels. In: 3D bioprinting for reconstructive surgery. New York: Elsevier; 2018. p. 377–91.

    Chapter  Google Scholar 

  216. Ozler SB, Bakirci E, Kucukgul C, Koc B. Three-dimensional direct cell bioprinting for tissue engineering. J Biomed Mater Res B Appl Biomater. 2017;105(8):2530–44. https://doi.org/10.1002/jbm.b.33768.

    Article  CAS  PubMed  Google Scholar 

  217. Bhattacharjee T, Zehnder SM, Rowe KG, Jain S, Nixon RM, Sawyer WG, et al. Writing in the granular gel medium. Sci Adv. 2015;1:1–6.

    Article  Google Scholar 

  218. Bhattacharjee T, Gil CJ, Marshall SL, Urueña JM, O’Bryan CS, Carstens M, et al. Liquid-like solids support cells in 3D. ACS Biomater Sci Eng. 2016;2:1787–95.

    Article  CAS  PubMed  Google Scholar 

  219. Bulanova EA, Koudan EV, Degosserie J, Heymans C, Das PF, Parfenov VA, et al. Bioprinting of a functional vascularized mouse thyroid gland construct. Biofabrication. 2017;9(3):034105. https://doi.org/10.1088/1758-5090/aa7fdd.

    Article  CAS  PubMed  Google Scholar 

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Stein, F., Trikalitis, V., Rouwkema, J., Salehi-Nik, N. (2019). Vascularization in Oral and Maxillofacial Tissue Engineering. In: Seppänen-Kaijansinkko, R. (eds) Tissue Engineering in Oral and Maxillofacial Surgery. Springer, Cham. https://doi.org/10.1007/978-3-030-24517-7_8

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