Advertisement

Vascularization in Oral and Maxillofacial Tissue Engineering

  • Fabian Stein
  • Vasileios Trikalitis
  • Jeroen RouwkemaEmail author
  • Nasim Salehi-Nik
Chapter

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.

Keywords

Angiogenesis Biofabrication Endothelial cells Growth factor gradient Nutrient supply Prevascularization Tissue engineering Vasculogenesis Vascular network 

References

  1. 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.CrossRefGoogle Scholar
  2. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Abou Neel EA, Chrzanowski W, Salih VM, Kim H-W, Knowles JC. Tissue engineering in dentistry. J Dent. 2014;42:915–28.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Yazdimamaghani M, Gonzalez J. Vascularization. In: Biomaterials for oral and dental tissue engineering. Oxford: Woodhead Publishing; 2017. p. 367–83.CrossRefGoogle Scholar
  9. 9.
    Rouwkema J, Rivron NC, van Blitterswijk CA. Vascularization in tissue engineering. Trends Biotechnol. 2008;26:434–41.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Rouwkema J, Khademhosseini A. Vascularization and angiogenesis in tissue engineering: beyond creating static networks. Trends Biotechnol. 2016;34:733–45.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Jain RK, Au P, Tam J, Duda DG, Fukumura D. Engineering vascularized tissue. Nat Biotechnol. 2005;23:821–3.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet. 2006;367:1241–6.CrossRefGoogle Scholar
  15. 15.
    Moon JJ, West JL. Vascularization of engineered tissues: approaches to promote angio-genesis in biomaterials. Curr Top Med Chem. 2008;8:300–10.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Shin’oka T, Imai Y, Ikada Y. Transplantation of a tissue-engineered pulmonary artery. N Engl J Med. 2001;344:532–3.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Gauvin R, Guillemette M, Dokmeci M, Khademhosseini A. Application of microtechnologies for the vascularization of engineered tissues. Vasc Cell. 2011;3:1–7.CrossRefGoogle Scholar
  19. 19.
    Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249–57.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Barabaschi GD, Manoharan V, Li Q, Bertassoni LE. Engineering pre-vascularized scaffolds for bone regeneration. Adv Exp Med Biol. 2015;881:79–94.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Charkoudian N. Mechanisms and modifiers of reflex induced cutaneous vasodilation and vasoconstriction in humans. J Appl Physiol. 2010;109:1221–8.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Kim K-W, Song J-H. Emerging roles of lymphatic vasculature in immunity. Immune Netw. 2017;17:68–76.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng. 2007;9:121–67.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Sadler TW. Langman’s medical embryology. 11th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2009.Google Scholar
  28. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 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.PubMedPubMedCentralGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Thurston G, Kitajewski J. VEGF and Delta-Notch: interacting signalling pathways in tumour angiogenesis. Br J Cancer. 2008;99:1204–9.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Eilken HM, Adams RH. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol. 2010;22:617–25.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Cavallaro U, Liebner S, Dejana E. Endothelial cadherins and tumor angiogenesis. Exp Cell Res. 2006;312:659–67.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Luo Y, Radice GL. N-cadherin acts upstream of VE-cadherin in controlling vascular morphogenesis. J Cell Biol. 2005;169:29–34.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Strilić B, Kučera T, Lammert E. Formation of cardiovascular tubes in invertebrates and vertebrates. Cell Mol Life Sci. 2010;67:3209–18.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Iruela-Arispe ML, Davis GE. Cellular and molecular mechanisms of vascular lumen formation. Dev Cell. 2009;16:222–31.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 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. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Dejana E. Endothelial adherens junctions: implications in the control of vascular permeability and angiogenesis. J Clin Invest. 1996;98:1949–53.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Beck L, D’Amore PA. Vascular development: cellular and molecular regulation. FASEB J. 1997;11:365–73.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Nicosia RF, Villaschi S. Rat aortic smooth muscle cells become pericytes during angiogenesis in vitro. Lab Invest. 1995;73:658–66.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Cimpean A-M, Ribatti D, Raica M. A brief history of angiogenesis assays. Int J Dev Biol. 2011;55:377–82.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Muthukkaruppan V, Auerbach R. Angiogenesis in the mouse cornea. Science. 1979;205:1416–8.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Lawson ND, Weinstein BM. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol. 2002;248:307–18.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Auerbach R, Lewis R, Shinners B, Kubai L, Akhtar N. Angiogenesis assays: a critical overview. Clin Chem. 2003;49:32–40.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 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. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Gui L, Niklason LE. Vascular tissue engineering: building perfusable vasculature for implantation. Curr Opin Chem Eng. 2014;3:68–74.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 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.CrossRefGoogle Scholar
  67. 67.
    Lovett M, Lee K, Edwards A, Kaplan DL. Vascularization strategies for tissue engineering. Tissue Eng Part B Rev. 2009;15:353–70.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Hallock GG. The complete classification of flaps. Microsurgery. 2004;24:157–61.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 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. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 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.CrossRefGoogle Scholar
  83. 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.CrossRefGoogle Scholar
  84. 84.
    Peters MC, Polverini PJ, Mooney DJ. Engineering vascular networks in porous polymer matrices. J Biomed Mater Res. 2002;60:668–78.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 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.CrossRefGoogle Scholar
  86. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials. 2005;26:5474–91.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 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.CrossRefGoogle Scholar
  93. 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.CrossRefGoogle Scholar
  94. 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. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Lee KY, Mooney DJ. Hydrogels for tissue engineering. Chem. Rev. 2001;101:1869–79.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 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.CrossRefGoogle Scholar
  101. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 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. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  107. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  109. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Richardson TP, Peters MC, Ennett AB, Mooney DJ. Polymeric system for dual growth factor delivery. Nat Biotechnol. 2001;19:1029–34.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Chiu LLY, Radisic M. Scaffolds with covalently immobilized VEGF and angiopoietin-1 for vascularization of engineered tissues. Biomaterials. 2010;31:226–41.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  115. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  117. 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. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  119. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  120. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Brey EM, Uriel S, Greisler HP, McIntire LV. Therapeutic neovascularization: contributions from bioengineering. Tissue Eng. 2005;11:567–84.PubMedCrossRefPubMedCentralGoogle Scholar
  122. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  123. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  124. 124.
    Jain RK. Molecular regulation of vessel maturation. Nat Med. 2003;9:685–93.PubMedCrossRefPubMedCentralGoogle Scholar
  125. 125.
    Sukmana I. Microvascular guidance: a challenge to support the development of vascularised tissue engineering construct. Sci World J. 2012;2012:1–10.CrossRefGoogle Scholar
  126. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  127. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  129. 129.
    Kirkpatrick CJ, Fuchs S, Unger RE. Co-culture systems for vascularization—learning from nature. Adv Drug Deliv Rev. 2011;63:291–9.PubMedCrossRefPubMedCentralGoogle Scholar
  130. 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.CrossRefGoogle Scholar
  131. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  132. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  133. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  134. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  135. 135.
    Folkman J, Haudenschild C. Angiogenesis in vitro. Nature. 1980;288:551–6.PubMedCrossRefPubMedCentralGoogle Scholar
  136. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  137. 137.
    Kim S, Lee H, Chung M, Jeon NL. Engineering of functional, perfusable 3D microvascular networks on a chip. Lab Chip. 2013;13:1489.PubMedCrossRefPubMedCentralGoogle Scholar
  138. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  139. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  141. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  143. 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.CrossRefGoogle Scholar
  144. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  145. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  146. 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.CrossRefGoogle Scholar
  147. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Whitesides GM, Grzybowski B. Self-assembly at all scales. Science. 2002;295:2418–21.PubMedCrossRefPubMedCentralGoogle Scholar
  149. 149.
    Timmins NE, Nielsen LK. Generation of multicellular tumor spheroids by the hanging-drop method. Methods Mol Med. 2007;140:141–51.PubMedCrossRefPubMedCentralGoogle Scholar
  150. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  151. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  152. 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.CrossRefGoogle Scholar
  153. 153.
    Fukuda J, Nakazawa K. Orderly arrangement of hepatocyte spheroids on a microfabricated chip. Tissue Eng. 2005;11:1254–62.PubMedCrossRefPubMedCentralGoogle Scholar
  154. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  155. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  156. 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.CrossRefGoogle Scholar
  157. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  158. 158.
    Laschke MW, Menger MD. Spheroids as vascularization units: from angiogenesis research to tissue engineering applications. Biotechnol Adv. 2017;35:782–91.PubMedCrossRefPubMedCentralGoogle Scholar
  159. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  160. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  161. 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.PubMedCrossRefGoogle Scholar
  162. 162.
    Bauman E, Feijão T, Carvalho DTO, Granja PL, Barrias CC. Xeno-free pre-vascularized spheroids for therapeutic applications. Sci Rep. 2018;8:230.PubMedPubMedCentralCrossRefGoogle Scholar
  163. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  164. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  165. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  166. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  167. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  168. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  169. 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.CrossRefGoogle Scholar
  170. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  171. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  172. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  173. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  174. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  175. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  176. 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;49Google Scholar
  177. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  178. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  179. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  180. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  181. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  182. 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. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  184. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  185. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  186. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  187. 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.CrossRefGoogle Scholar
  188. 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. 189.
    Mironov V, Trusk T, Kasyanov V, Little S, Swaja R, Markwald R. Biofabrication: a 21st century manufacturing paradigm. Biofabrication. 2009;1:022001.PubMedCrossRefPubMedCentralGoogle Scholar
  190. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  191. 191.
    Justin AW, Brooks RA, Markaki AE. Multi-casting approach for vascular networks in cellularized hydrogels. J R Soc Interface. 2016;13:20160768.PubMedPubMedCentralCrossRefGoogle Scholar
  192. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  193. 193.
    Kleinman HK, Martin GR. Matrigel: Basement membrane matrix with biological activity. Semin Cancer Biol. 2005;15:378–86.PubMedCrossRefPubMedCentralGoogle Scholar
  194. 194.
    Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32:773–85.PubMedCrossRefPubMedCentralGoogle Scholar
  195. 195.
    Mori N, Morimoto Y, Takeuchi S. Skin integrated with perfusable vascular channels on a chip. Biomaterials. 2017;116:48–56.PubMedCrossRefPubMedCentralGoogle Scholar
  196. 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.CrossRefGoogle Scholar
  197. 197.
    Xia Y, Whitesides GM. Soft Lithography. Angew Chemie Int Ed. 1998;37:550–75.CrossRefGoogle Scholar
  198. 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.CrossRefGoogle Scholar
  199. 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. 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.CrossRefGoogle Scholar
  201. 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.CrossRefGoogle Scholar
  202. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  203. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  204. 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.CrossRefGoogle Scholar
  205. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  206. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  207. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  208. 208.
    Shao J, Huang Y, Fan Q. Visible light initiating systems for photopolymerization: status, development and challenges. Polym Chem. 2014;5:4195–210.CrossRefGoogle Scholar
  209. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  210. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  211. 211.
    Moldovan NI. Progress in scaffold-free bioprinting for cardiovascular medicine. J Cell Mol Med. 2018;22:2964–9.PubMedPubMedCentralCrossRefGoogle Scholar
  212. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  213. 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. 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.PubMedCrossRefPubMedCentralGoogle Scholar
  215. 215.
    Hu N, Zhang YS. 3D bioprinting blood vessels. In: 3D bioprinting for reconstructive surgery. New York: Elsevier; 2018. p. 377–91.CrossRefGoogle Scholar
  216. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  217. 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.CrossRefGoogle Scholar
  218. 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.CrossRefGoogle Scholar
  219. 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.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Fabian Stein
    • 1
  • Vasileios Trikalitis
    • 1
  • Jeroen Rouwkema
    • 1
    Email author
  • Nasim Salehi-Nik
    • 1
  1. 1.Vascularization Lab, Department of Biomechanical Engineering, Faculty of Engineering Technology, Technical Medical CentreUniversity of TwenteEnschedeThe Netherlands

Personalised recommendations