Advertisement

Bioprinting Vasculature

  • Sanskrita Das
  • Jinah JangEmail author
Chapter

Abstract

Despite the extensive research in fabricating tissue-engineered vascularized constructs, emulating the native architecture with intricate microvascular networks in vitro remains challenging, which limits clinical applications. The 3D bioprinting technique is a promising approach for overcoming the limitations posed by the classical tissue engineering strategies. The new generation of bioprinted vascularized tissue constructs facilitates the high spatial control of cell allocation, alignment, and maturation and vessel stabilization as a result of the efficient diffusion of oxygen, nutrients, and (optionally) growth factors, thereby enhancing the metabolic activity of cells. Moreover, the bioprinted vascularized construct accelerates its integration with the host tissue upon implantation, promoting rapid microvascular formation and tissue regeneration. Additionally, the flexibility to fabricate cell-laden, multi-material, and anatomically shaped vascular grafts and vascularized tissue constructs encourages the development of modalities for screening new therapeutic drugs and for using as an in vitro disease model. In this chapter, we briefly discuss the need for using tissue-engineered vascularized constructs and summarize the different types of biomaterials and conventional approaches toward it. We also introduce the advent of 3D bioprinting in developing 3D vascularized constructs and focus on its applications in tissue regeneration and as a platform for drug discovery and testing.

Keywords

3D bioprinting Bioink Vascularization Solid organ 

Notes

Acknowledgements

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (No. 2015R1A6A3A04059015) and the MSIP (Ministry of Science, ICT and Future Planning), Korea, under the “ICT Consilience Creative Program” (IITP-R0346-16-1007) supervised by the IITP (Institute for Information & communications Technology Promotion).

References

  1. 1.
    Hoch E, Tovar GE, Borchers K (2014) Bioprinting of artificial blood vessels: current approaches towards a demanding goal. Eur J Cardiothorac Surg 46(5):767–778PubMedGoogle Scholar
  2. 2.
    Ke D, Murphy SV (2019) Current challenges of bioprinted tissues toward clinical translation. Tissue Eng Part B Rev 25(1):1–13PubMedGoogle Scholar
  3. 3.
    Clarks ER, Clark EL (1939) Microscopic observations on the growth of blood capillaries in the living mammal. Am J Anat 64(2):251–301Google Scholar
  4. 4.
    Kannan RY, Salacinski HJ, Sales K, Butler P, Seifalian AM (2005) The roles of tissue engineering and vascularisation in the development of micro-vascular networks: a review. Biomaterials 26(14):1857–1875PubMedGoogle Scholar
  5. 5.
    Elomaa L, Yang YP (2017) Additive manufacturing of vascular grafts and vascularized tissue constructs. Tissue Eng Part B Rev 23(5):436–450PubMedPubMedCentralGoogle Scholar
  6. 6.
    D Levit R (2018) Engineering vessels as good as new? JACC Basic Transl Sci 3(1):119–121PubMedPubMedCentralGoogle Scholar
  7. 7.
    Teebken OE, Haverich A (2002) Tissue engineering of small diameter vascular grafts. Eur J Vasc Endovasc 23(6):475–485Google Scholar
  8. 8.
    Wang X, Lin P, Yao Q, Chen C (2007) Development of small-diameter vascular grafts. World J Surg 31(4):682–689PubMedGoogle Scholar
  9. 9.
    Kannan RY, Salacinski HJ, Butler PE, Hamilton G, Seifalian AM (2005) Current status of prosthetic bypass grafts: a review. J Biomed Mater Res B Appl Biomater 74(1):570–581PubMedGoogle Scholar
  10. 10.
    Novosel EC, Kleinhans C, Kluger PJ (2011) Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 63(4–5):300–311PubMedGoogle Scholar
  11. 11.
    Pal A, Vernon BL, Nikkhah M (2018) Therapeutic neovascularization promoted by injectable hydrogels. Bioact Mater 3(4):389–400PubMedPubMedCentralGoogle Scholar
  12. 12.
    Schechner JS, Nath AK, Zheng L, Kluger MS, Hughes CC, Sierra-Honigmann MR, Lorber MI, Tellides G, Kashgarian M, Bothwell AL, Pober JS (2000) In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci U S A 97(16):9191–9196PubMedPubMedCentralGoogle Scholar
  13. 13.
    Li X, Tamama K, Xie X, Guan J (2016) Improving cell engraftment in cardiac stem cell therapy. Stem Cells Int 2016:7168797PubMedGoogle Scholar
  14. 14.
    Tous E, Purcell B, Ifkovits JL, Burdick JA (2011) Injectable acellular hydrogels for cardiac repair. J Cardiovasc Transl Res 4(5):528–542PubMedGoogle Scholar
  15. 15.
    Bhatia SN, Ingber DE (2014) Microfluidic organs-on-chips. Nat Biotechnol 32(8):760–772Google Scholar
  16. 16.
    Laschke MW, Harder Y, Amon M, Martin I, Farhadi J, Ring A, Torio-Padron N, Schramm R, Rucker M, Junker D, Haufel JM, Carvalho C, Heberer M, Germann G, Vollmar B, Menger MD (2006) Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes. Tissue Eng 12(8):2093–2104PubMedGoogle Scholar
  17. 17.
    Jain RK, Au P, Tam J, Duda DG, Fukumura D (2005) Engineering vascularized tissue. Nat Biotechnol 23(7):821–823PubMedGoogle Scholar
  18. 18.
    Kreimendahl F, Kopf M, Thiebes AL, Duarte Campos DF, Blaeser A, Schmitz-Rode T, Apel C, Jockenhoevel S, Fischer H (2017) Three-dimensional printing and angiogenesis: tailored agarose-type I collagen blends comprise three-dimensional printability and angiogenesis potential for tissue-engineered substitutes. Tissue Eng Part C Methods 23(10):604–615PubMedGoogle Scholar
  19. 19.
    Bayless KJ, Salazar R, Davis GE (2000) RGD-dependent vacuolation and lumen formation observed during endothelial cell morphogenesis in three-dimensional fibrin matrices involves the alpha(v)beta(3) and alpha(5)beta(1) integrins. Am J Pathol 156(5):1673–1683PubMedPubMedCentralGoogle Scholar
  20. 20.
    Wagenseil JE, Mecham RP (2009) Vascular extracellular matrix and arterial mechanics. Physiol Rev 89(3):957–989PubMedPubMedCentralGoogle Scholar
  21. 21.
    Aper T, Wilhelmi M, Gebhardt C, Hoeffler K, Benecke N, Hilfiker A, Haverich A (2016) Novel method for the generation of tissue-engineered vascular grafts based on a highly compacted fibrin matrix. Acta Biomater 29:21–32PubMedGoogle Scholar
  22. 22.
    McKenna KA, Hinds MT, Sarao RC, Wu PC, Maslen CL, Glanville RW, Babcock D, Gregory KW (2012) Mechanical property characterization of electrospun recombinant human tropoelastin for vascular graft biomaterials. Acta Biomater 8(1):225–233PubMedGoogle Scholar
  23. 23.
    Boland ED, Matthews JA, Pawlowski KJ, Simpson DG, Wnek GE, Bowlin GL (2004) Electrospinning collagen and elastin: preliminary vascular tissue engineering. Front Biosci 9:1422–1432PubMedGoogle Scholar
  24. 24.
    Elsayed Y, Lekakou C, Labeed F, Tomlins P (2016) Fabrication and characterisation of biomimetic, electrospun gelatin fibre scaffolds for tunica media-equivalent, tissue engineered vascular grafts. Mater Sci Eng C Mater Biol Appl 61:473–483PubMedGoogle Scholar
  25. 25.
    Kong X, Han B, Wang H, Li H, Xu W, Liu W (2012) Mechanical properties of biodegradable small-diameter chitosan artificial vascular prosthesis. J Biomed Mater Res A 100(8):1938–1945PubMedGoogle Scholar
  26. 26.
    Benning L, Gutzweiler L, Trondle K, Riba J, Zengerle R, Koltay P, Zimmermann S, Stark GB, Finkenzeller G (2018) Assessment of hydrogels for bioprinting of endothelial cells. J Biomed Mater Res A 106(4):935–947PubMedGoogle Scholar
  27. 27.
    Foubert P, Barillas S, Gonzalez AD, Alfonso Z, Zhao S, Hakim I, Meschter C, Tenenhaus M, Fraser JK (2015) Uncultured adipose-derived regenerative cells (ADRCs) seeded in collagen scaffold improves dermal regeneration, enhancing early vascularization and structural organization following thermal burns. Burns 41(7):1504–1516PubMedGoogle Scholar
  28. 28.
    Chung E, Rytlewski JA, Merchant AG, Dhada KS, Lewis EW, Suggs LJ (2015) Fibrin-based 3D matrices induce angiogenic behavior of adipose-derived stem cells. Acta Biomater 17:78–88PubMedPubMedCentralGoogle Scholar
  29. 29.
    Tavana S, Azarnia M, Valojerdi MR, Shahverdi A (2016) Hyaluronic acid-based hydrogel scaffold without angiogenic growth factors enhances ovarian tissue function after autotransplantation in rats. Biomed Mater 11(5):055006PubMedGoogle Scholar
  30. 30.
    Ran X, Ye Z, Fu M, Wang Q, Wu H, Lin S, Yin T, Hu T, Wang G (2018) Design, preparation, and performance of a novel bilayer tissue-engineered small-diameter vascular graft. Macromol Biosci 19(3):e1800189PubMedGoogle Scholar
  31. 31.
    Catto V, Farè S, Freddi G, Tanzi MC (2014) Vascular tissue engineering: recent advances in small diameter blood vessel regeneration. ISRN Vasc Med 2014:1–27Google Scholar
  32. 32.
    Fuchs S, Ghanaati S, Orth C, Barbeck M, Kolbe M, Hofmann A, Eblenkamp M, Gomes M, Reis RL, Kirkpatrick CJ (2009) Contribution of outgrowth endothelial cells from human peripheral blood on in vivo vascularization of bone tissue engineered constructs based on starch polycaprolactone scaffolds. Biomaterials 30(4):526–534PubMedGoogle Scholar
  33. 33.
    Gigliobianco G, Chong CK, MacNeil S (2015) Simple surface coating of electrospun poly-L-lactic acid scaffolds to induce angiogenesis. J Biomater Appl 30(1):50–60PubMedGoogle Scholar
  34. 34.
    Yokoyama T, Ohashi K, Kuge H, Kanehiro H, Iwata H, Yamato M, Nakajima Y (2006) In vivo engineering of metabolically active hepatic tissues in a neovascularized subcutaneous cavity. Am J Transplant 6(1):50–59PubMedGoogle Scholar
  35. 35.
    Sultana T, Amirian J, Park C, Lee SJ, Lee BT (2017) Preparation and characterization of polycaprolactone-polyethylene glycol methyl ether and polycaprolactone-chitosan electrospun mats potential for vascular tissue engineering. J Biomater Appl 32(5):648–662PubMedGoogle Scholar
  36. 36.
    Kim SH, Kwon JH, Chung MS, Chung E, Jung Y, Kim SH, Kim YH (2006) Fabrication of a new tubular fibrous PLCL scaffold for vascular tissue engineering. J Biomater Sci Polym Ed 17(12):1359–1374PubMedGoogle Scholar
  37. 37.
    Kolesky DB, Homan KA, Skylar-Scott MA, Lewis JA (2016) Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci U S A 113(12):3179–3184PubMedPubMedCentralGoogle Scholar
  38. 38.
    Kolesky DB, Truby RL, Gladman AS, Busbee TA, Homan KA, Lewis JA (2014) 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv Mater 26(19):3124–3130Google Scholar
  39. 39.
    McClure MJ, Sell SA, Simpson DG, Walpoth BH, Bowlin GL (2010) A three-layered electrospun matrix to mimic native arterial architecture using polycaprolactone, elastin, and collagen: a preliminary study. Acta Biomater 6(7):2422–2433PubMedGoogle Scholar
  40. 40.
    Yokota T, Ichikawa H, Matsumiya G, Kuratani T, Sakaguchi T, Iwai S, Shirakawa Y, Torikai K, Saito A, Uchimura E, Kawaguchi N, Matsuura N, Sawa Y (2008) In situ tissue regeneration using a novel tissue-engineered, small-caliber vascular graft without cell seeding. J Thorac Cardiovasc Surg 136(4):900–907PubMedGoogle Scholar
  41. 41.
    Liu J, Argenta L, Morykwas M, Wagner WD (2014) Properties of single electrospun poly(diol citrate)-collagen-proteoglycan nanofibers for arterial repair and in applications requiring viscoelasticity. J Biomater Appl 28(5):729–738PubMedGoogle Scholar
  42. 42.
    Crapo PM, Gilbert TW, Badylak SF (2011) An overview of tissue and whole organ decellularization processes. Biomaterials 32(12):3233–3243PubMedPubMedCentralGoogle Scholar
  43. 43.
    Dew L, English WR, Chong CK, MacNeil S (2016) Investigating neovascularization in rat decellularized intestine: an in vitro platform for studying angiogenesis. Tissue Eng Part A 22(23–24):1317–1326PubMedPubMedCentralGoogle Scholar
  44. 44.
    Bader A, Steinhoff G, Strobl K, Schilling T, Brandes G, Mertsching H, Tsikas D, Froelich J, Haverich A (2000) Engineering of human vascular aortic tissue based on a xenogeneic starter matrix. Transplantation 70(1):7–14PubMedGoogle Scholar
  45. 45.
    Zou Y, Zhang Y (2012) Mechanical evaluation of decellularized porcine thoracic aorta. J Surg Res 175(2):359–368PubMedGoogle Scholar
  46. 46.
    Pati F, Jang J, Ha DH, Won Kim S, Rhie JW, Shim JH, Kim DH, Cho DW (2014) Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun 5:3935PubMedPubMedCentralGoogle Scholar
  47. 47.
    Gao G, Lee JH, Jang J, Lee DH, Kong J-S, Kim BS, Choi Y-J, Jang WB, Hong YJ, Kwon S-M, Cho D-W (2017) Tissue engineered bio-blood-vessels constructed using a tissue-specific bioink and 3D coaxial cell printing technique: a novel therapy for ischemic disease. Adv Funct Mater 27(33):1700798Google Scholar
  48. 48.
    Shieh SJ, Vacanti JP (2005) State-of-the-art tissue engineering: from tissue engineering to organ building. Surgery 137(1):1–7PubMedGoogle Scholar
  49. 49.
    Lee B, Shafiq M, Jung Y, Park J-C, Kim SH (2016) Characterization and preparation of bio-tubular scaffolds for fabricating artificial vascular grafts by combining electrospinning and a co-culture system. Macromol Res 24(2):131–142Google Scholar
  50. 50.
    Karal-Yilmaz O, Serhatli M, Baysal K, Baysal BM (2011) Preparation and in vitro characterization of vascular endothelial growth factor (VEGF)-loaded poly(d,l-lactic-co-glycolic acid) microspheres using a double emulsion/solvent evaporation technique. J Microencapsul 28(1):46–54PubMedGoogle Scholar
  51. 51.
    Geiger F, Lorenz H, Xu W, Szalay K, Kasten P, Claes L, Augat P, Richter W (2007) VEGF producing bone marrow stromal cells (BMSC) enhance vascularization and resorption of a natural coral bone substitute. Bone 41(4):516–522PubMedGoogle Scholar
  52. 52.
    Zisch AH, Lutolf MP, Hubbell JA (2003) Biopolymeric delivery matrices for angiogenic growth factors. Cardiovasc Pathol 12(6):295–310PubMedGoogle Scholar
  53. 53.
    Saik JE, Gould DJ, Watkins EM, Dickinson ME, West JL (2011) Covalently immobilized platelet-derived growth factor-BB promotes angiogenesis in biomimetic poly(ethylene glycol) hydrogels. Acta Biomater 7(1):133–143PubMedGoogle Scholar
  54. 54.
    Landau S, Ben-Shaul S, Levenberg S (2018) Oscillatory strain promotes vessel stabilization and alignment through fibroblast YAP-mediated mechanosensitivity. Adv Sci (Weinh) 5(9):1800506Google Scholar
  55. 55.
    Syedain ZH, Graham ML, Dunn TB, O’Brien T, Johnson SL, Schumacher RJ, Tranquillo RT (2017) A completely biological “off-the-shelf” arteriovenous graft that recellularizes in baboons. Sci Transl Med 9(414):eaan4209PubMedGoogle Scholar
  56. 56.
    Sekine H, Shimizu T, Hobo K, Sekiya S, Yang J, Yamato M, Kurosawa H, Kobayashi E, Okano T (2008) Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 118(14 Suppl):S145–S152PubMedGoogle Scholar
  57. 57.
    Mian RW, Morrison WA, Hurley JV, Penington AJ, Romeo R, Tanaka Y, Knight KR (2000) Formation of new tissue from an arteriovenous loop in the absence of added extracellular matrix. Tissue Eng 6(6):595–603PubMedGoogle Scholar
  58. 58.
    Chang CC, Boland ED, Williams SK, Hoying JB (2011) Direct-write bioprinting three-dimensional biohybrid systems for future regenerative therapies. J Biomed Mater Res B Appl Biomater 98(1):160–170PubMedPubMedCentralGoogle Scholar
  59. 59.
    Cui X, Boland T (2009) Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials 30(31):6221–6227PubMedGoogle Scholar
  60. 60.
    Miri AK, Khalilpour A, Cecen B, Maharjan S, Shin SR, Khademhosseini A (2019) Multiscale bioprinting of vascularized models. Biomaterials 198:204–216PubMedGoogle Scholar
  61. 61.
    Kesari P, Xu T, Boland T (2005) Layer-by-layer printing of cells and its application to tissue engineering. Mater Res Soc Symp P 845:111–117Google Scholar
  62. 62.
    Nakamura M, Nishiyama Y, Henmi C, Iwanaga S, Nakagawa H, Yamaguchi K, Akita K, Mochizuki S, Takiura K (2008) Ink jet three-dimensional digital fabrication for biological tissue manufacturing: analysis of alginate microgel beads produced by ink jet droplets for three dimensional tissue fabrication. J Imaging Sci Technol 52(6):060201Google Scholar
  63. 63.
    Pataky K, Braschler T, Negro A, Renaud P, Lutolf MP, Brugger J (2012) Microdrop printing of hydrogel bioinks into 3D tissue-like geometries. Adv Mater 24(3):391–396PubMedGoogle Scholar
  64. 64.
    Chang CC, Krishnan L, Nunes SS, Church KH, Edgar LT, Boland ED, Weiss JA, Williams SK, Hoying JB (2012) Determinants of microvascular network topologies in implanted neovasculatures. Arterioscler Thromb Vasc Biol 32(1):5–14PubMedGoogle Scholar
  65. 65.
    Boland T, Xu T, Damon B, Cui X (2006) Application of inkjet printing to tissue engineering. Biotechnol J 1(9):910–917PubMedGoogle Scholar
  66. 66.
    Gudapati H, Dey M, Ozbolat I (2016) A comprehensive review on droplet-based bioprinting: past, present and future. Biomaterials 102:20–42PubMedGoogle Scholar
  67. 67.
    Guillotin B, Souquet A, Catros S, Duocastella M, Pippenger B, Bellance S, Bareille R, Remy M, Bordenave L, Amedee J, Guillemot F (2010) Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials 31(28):7250–7256PubMedGoogle Scholar
  68. 68.
    Wu PK, Ringeisen BR (2010) Development of human umbilical vein endothelial cell (HUVEC) and human umbilical vein smooth muscle cell (HUVSMC) branch/stem structures on hydrogel layers via biological laser printing (BioLP). Biofabrication 2(1):014111PubMedGoogle Scholar
  69. 69.
    Gaebel R, Ma N, Liu J, Guan J, Koch L, Klopsch C, Gruene M, Toelk A, Wang W, Mark P, Wang F, Chichkov B, Li W, Steinhoff G (2011) Patterning human stem cells and endothelial cells with laser printing for cardiac regeneration. Biomaterials 32(35):9218–9230PubMedGoogle Scholar
  70. 70.
    McCall JD, Anseth KS (2012) Thiol-ene photopolymerizations provide a facile method to encapsulate proteins and maintain their bioactivity. Biomacromolecules 13(8):2410–2417PubMedPubMedCentralGoogle Scholar
  71. 71.
    Li SJ, Xiong Z, Wang XH, Yan YN, Liu HX, Zhang RJ (2009) Direct fabrication of a hybrid cell/hydrogel construct by a double-nozzle assembling technology. J Bioact Compat Polym 24(3):249–265Google Scholar
  72. 72.
    Jang J, Park HJ, Kim SW, Kim H, Park JY, Na SJ, Kim HJ, Park MN, Choi SH, Park SH, Kim SW, Kwon SM, Kim PJ, Cho DW (2017) 3D printed complex tissue construct using stem cell-laden decellularized extracellular matrix bioinks for cardiac repair. Biomaterials 112:264–274PubMedGoogle Scholar
  73. 73.
    Jia W, Gungor-Ozkerim PS, Zhang YS, Yue K, Zhu K, Liu W, Pi Q, Byambaa B, Dokmeci MR, Shin SR, Khademhosseini A (2016) Direct 3D bioprinting of perfusable vascular constructs using a blend bioink. Biomaterials 106:58–68PubMedPubMedCentralGoogle Scholar
  74. 74.
    Lee VK, Lanzi AM, Haygan N, Yoo SS, Vincent PA, Dai G (2014) Generation of multi-scale vascular network system within 3D Hydrogel using 3D bio-printing technology. Cell Mol Bioeng 7(3):460–472PubMedPubMedCentralGoogle Scholar
  75. 75.
    Bertassoni LE, Cecconi M, Manoharan V, Nikkhah M, Hjortnaes J, Cristino AL, Barabaschi G, Demarchi D, Dokmeci MR, Yang Y, Khademhosseini A (2014) Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab Chip 14(13):2202–2211PubMedPubMedCentralGoogle Scholar
  76. 76.
    Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen DH, Cohen DM, Toro E, Chen AA, Galie PA, Yu X, Chaturvedi R, Bhatia SN, Chen CS (2012) Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 11(9):768–774PubMedPubMedCentralGoogle Scholar
  77. 77.
    Massa S, Sakr MA, Seo J, Bandaru P, Arneri A, Bersini S, Zare-Eelanjegh E, Jalilian E, Cha BH, Antona S, Enrico A, Gao Y, Hassan S, Acevedo JP, Dokmeci MR, Zhang YS, Khademhosseini A, Shin SR (2017) Bioprinted 3D vascularized tissue model for drug toxicity analysis. Biomicrofluidics 11(4):044109PubMedPubMedCentralGoogle Scholar
  78. 78.
    Wu W, DeConinck A, Lewis JA (2011) Omnidirectional printing of 3D microvascular networks. Adv Mater 23(24):H178–H183PubMedGoogle Scholar
  79. 79.
    Park JY, Shim JH, Choi SA, Jang J, Kim M, Lee SH, Cho DW (2015) 3D printing technology to control BMP-2 and VEGF delivery spatially and temporally to promote large-volume bone regeneration. J Mater Chem B 3(27):5415–5425Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Creative IT EngineeringPohang University of Science and TechnologyPohangRepublic of Korea
  2. 2.Department of Mechanical EngineeringPohang University of Science and TechnologyPohangRepublic of Korea
  3. 3.School of Interdisciplinary Bioscience and BioengineeringPohang University of Science and TechnologyPohangRepublic of Korea

Personalised recommendations