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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Hoch E, Tovar GE, Borchers K (2014) Bioprinting of artificial blood vessels: current approaches towards a demanding goal. Eur J Cardiothorac Surg 46(5):767–778
Ke D, Murphy SV (2019) Current challenges of bioprinted tissues toward clinical translation. Tissue Eng Part B Rev 25(1):1–13
Clarks ER, Clark EL (1939) Microscopic observations on the growth of blood capillaries in the living mammal. Am J Anat 64(2):251–301
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):1857–1875
Elomaa L, Yang YP (2017) Additive manufacturing of vascular grafts and vascularized tissue constructs. Tissue Eng Part B Rev 23(5):436–450
D Levit R (2018) Engineering vessels as good as new? JACC Basic Transl Sci 3(1):119–121
Teebken OE, Haverich A (2002) Tissue engineering of small diameter vascular grafts. Eur J Vasc Endovasc 23(6):475–485
Wang X, Lin P, Yao Q, Chen C (2007) Development of small-diameter vascular grafts. World J Surg 31(4):682–689
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):570–581
Novosel EC, Kleinhans C, Kluger PJ (2011) Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 63(4–5):300–311
Pal A, Vernon BL, Nikkhah M (2018) Therapeutic neovascularization promoted by injectable hydrogels. Bioact Mater 3(4):389–400
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):9191–9196
Li X, Tamama K, Xie X, Guan J (2016) Improving cell engraftment in cardiac stem cell therapy. Stem Cells Int 2016:7168797
Tous E, Purcell B, Ifkovits JL, Burdick JA (2011) Injectable acellular hydrogels for cardiac repair. J Cardiovasc Transl Res 4(5):528–542
Bhatia SN, Ingber DE (2014) Microfluidic organs-on-chips. Nat Biotechnol 32(8):760–772
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):2093–2104
Jain RK, Au P, Tam J, Duda DG, Fukumura D (2005) Engineering vascularized tissue. Nat Biotechnol 23(7):821–823
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):604–615
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):1673–1683
Wagenseil JE, Mecham RP (2009) Vascular extracellular matrix and arterial mechanics. Physiol Rev 89(3):957–989
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 29:21–32
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):225–233
Boland ED, Matthews JA, Pawlowski KJ, Simpson DG, Wnek GE, Bowlin GL (2004) Electrospinning collagen and elastin: preliminary vascular tissue engineering. Front Biosci 9:1422–1432
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 61:473–483
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):1938–1945
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):935–947
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):1504–1516
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 17:78–88
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):055006
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):e1800189
Catto V, Farè S, Freddi G, Tanzi MC (2014) Vascular tissue engineering: recent advances in small diameter blood vessel regeneration. ISRN Vasc Med 2014:1–27
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):526–534
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):50–60
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):50–59
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):648–662
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):1359–1374
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):3179–3184
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):3124–3130
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):2422–2433
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):900–907
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):729–738
Crapo PM, Gilbert TW, Badylak SF (2011) An overview of tissue and whole organ decellularization processes. Biomaterials 32(12):3233–3243
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):1317–1326
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):7–14
Zou Y, Zhang Y (2012) Mechanical evaluation of decellularized porcine thoracic aorta. J Surg Res 175(2):359–368
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 5:3935
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):1700798
Shieh SJ, Vacanti JP (2005) State-of-the-art tissue engineering: from tissue engineering to organ building. Surgery 137(1):1–7
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):131–142
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):46–54
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):516–522
Zisch AH, Lutolf MP, Hubbell JA (2003) Biopolymeric delivery matrices for angiogenic growth factors. Cardiovasc Pathol 12(6):295–310
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):133–143
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):1800506
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):eaan4209
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–S152
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):595–603
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):160–170
Cui X, Boland T (2009) Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials 30(31):6221–6227
Miri AK, Khalilpour A, Cecen B, Maharjan S, Shin SR, Khademhosseini A (2019) Multiscale bioprinting of vascularized models. Biomaterials 198:204–216
Kesari P, Xu T, Boland T (2005) Layer-by-layer printing of cells and its application to tissue engineering. Mater Res Soc Symp P 845:111–117
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):060201
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):391–396
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):5–14
Boland T, Xu T, Damon B, Cui X (2006) Application of inkjet printing to tissue engineering. Biotechnol J 1(9):910–917
Gudapati H, Dey M, Ozbolat I (2016) A comprehensive review on droplet-based bioprinting: past, present and future. Biomaterials 102:20–42
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):7250–7256
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):014111
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):9218–9230
McCall JD, Anseth KS (2012) Thiol-ene photopolymerizations provide a facile method to encapsulate proteins and maintain their bioactivity. Biomacromolecules 13(8):2410–2417
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):249–265
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 112:264–274
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 106:58–68
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):460–472
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):2202–2211
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):768–774
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):044109
Wu W, DeConinck A, Lewis JA (2011) Omnidirectional printing of 3D microvascular networks. Adv Mater 23(24):H178–H183
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):5415–5425
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).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Das, S., Jang, J. (2019). Bioprinting Vasculature. In: Guvendiren, M. (eds) 3D Bioprinting in Medicine. Springer, Cham. https://doi.org/10.1007/978-3-030-23906-0_4
Download citation
DOI: https://doi.org/10.1007/978-3-030-23906-0_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-23905-3
Online ISBN: 978-3-030-23906-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)