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Microvascular Networks and Models, In vitro Formation

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Vascularization for Tissue Engineering and Regenerative Medicine

Abstract

The microvasculature involves the part of the vascular system made of vessels with diameters inferior to 100 μm. There are many culture models allowing for the formation of microvascular networks in vitro, developed either to study cellular and/or molecular aspects of angiogenesis and vasculogenesis or to prevascularize engineered tissues. In this chapter, we describe the cellular (Sect. 2) and material (Sect. 3) components used to generate such in vitro models. Innovative, advanced bioengineering processes, based on bioprinting or microfluidics, to create microvascular networks are also described (Sect. 4).

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References

  • Almond A (2007) Hyaluronan. Cell Mol Life Sci 64(13):1591–1596

    Article  Google Scholar 

  • Alonzo LF, Moya ML, Shirure VS, George SC (2015) Microfluidic device to control interstitial flow-mediated homotypic and heterotypic cellular communication. Lab Chip 15(17):3521–3529

    Article  Google Scholar 

  • Armulik A, Abramsson A, Betsholtz C (2005a) Endothelial/pericyte interactions. Circ Res 97(6):512–523

    Article  Google Scholar 

  • Armulik A, Abramsson A, Betsholtz C (2005b) Endothelial/pericyte interactions. Circ Res 97(6):512–523

    Article  Google Scholar 

  • Armulik A, Genove G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21(2):193–215

    Article  Google Scholar 

  • Arnaoutova I, Kleinman HK (2010) In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat Protoc 5(4):628–635

    Article  Google Scholar 

  • Arslan-Yildiz A, Assal RE, Chen P, Guven S, Inci F, Demirci U (2016) Towards artificial tissue models: past, present, and future of 3D bioprinting. Biofabrication 8(1):014103

    Article  Google Scholar 

  • Asahara T, Murohara T, Sullivan A, Silver M, vanderZee R, Li T et al (1997a) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302):964–967

    Article  Google Scholar 

  • Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T et al (1997b) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302):964–967

    Article  Google Scholar 

  • Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M et al (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85(3):221–228

    Article  Google Scholar 

  • Au P, Tam J, Fukumura D, Jain RK (2008a) Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111(9):4551–4558

    Article  Google Scholar 

  • Au P, Daheron LM, Duda DG, Cohen KS, Tyrrell JA, Lanning RM et al (2008b) Differential in vivo potential of endothelial progenitor cells from human umbilical cord blood and adult peripheral blood to form functional long-lasting vessels. Blood 111(3):1302–1305

    Article  Google Scholar 

  • Baker BM, Trappmann B, Stapleton SC, Toro E, Chen CS (2013) Microfluidics embedded within extracellular matrix to define vascular architectures and pattern diffusive gradients. Lab Chip 13(16):3246–3252

    Article  Google Scholar 

  • Balconi G, Spagnuolo R, Dejana E (2000) Development of endothelial cell lines from embryonic stem cells: a tool for studying genetically manipulated endothelial cells in vitro. Arterioscler Thromb Vasc Biol 20(6):1443–1451

    Article  Google Scholar 

  • Bautch VL, Redick SD, Scalia A, Harmaty M, Carmeliet P, Rapoport R (2000) Characterization of the vasculogenic block in the absence of vascular endothelial growth factor-a. Blood 95(6):1979–1987

    Google Scholar 

  • Bayless KJ, Davis GE (2002) The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J Cell Sci 115(Pt 6):1123–1136

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Bell SE, Mavila A, Salazar R, Bayless KJ, Kanagala S, Maxwell SA et al (2001) Differential gene expression during capillary morphogenesis in 3D collagen matrices: regulated expression of genes involved in basement membrane matrix assembly, cell cycle progression, cellular differentiation and G-protein signaling. J Cell Sci 114(Pt 15):2755–2773

    Google Scholar 

  • Benton JA, DeForest CA, Vivekanandan V, Anseth KS (2009) Photocrosslinking of gelatin macromers to synthesize porous hydrogels that promote valvular interstitial cell function. Tissue Eng Part A 15(11):3221–3230

    Article  Google Scholar 

  • Bersini S, Yazdi IK, Talo G, Shin SR, Moretti M, Khademhosseini A (2016) Cell-microenvironment interactions and architectures in microvascular systems. Biotechnol Adv 34(6):1113–1130

    Article  Google Scholar 

  • Bertassoni LE, Cecconi M, Manoharan V, Nikkhah M, Hjortnaes J, Cristino AL et al (2014) Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab Chip 14(13):2202–2211

    Article  Google Scholar 

  • Berthod F, Germain L, Tremblay N, Auger FA (2006) Extracellular matrix deposition by fibroblasts is necessary to promote capillary-like tube formation in vitro. J Cell Physiol 207(2):491–498

    Article  Google Scholar 

  • Betsholtz C, Lindblom P, Gerhardt H (2005) Role of pericytes in vascular morphogenesis. EXS (94):115–125

    Google Scholar 

  • Bhatia SN, Ingber DE (2014) Microfluidic organs-on-chips. Nat Biotechnol 32(8):760–772

    Article  Google Scholar 

  • Blache U, Metzger S, Vallmajo-Martin Q, Martin I, Djonov V, Ehrbar M (2016) Dual role of mesenchymal stem cells allows for microvascularized bone tissue-like environments in PEG hydrogels. Adv Healthc Mater 5(4):489–498

    Article  Google Scholar 

  • Black AF, Berthod F, L'Heureux N, Germain L, Auger FA (1998) Vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. FASEB J 12(13):1331–1340

    Google Scholar 

  • Bouis D, Hospers GA, Meijer C, Molema G, Mulder NH (2001) Endothelium in vitro: a review of human vascular endothelial cell lines for blood vessel-related research. Angiogenesis 4(2):91–102

    Article  Google Scholar 

  • Bray LJ, Binner M, Holzheu A, Friedrichs J, Freudenberg U, Hutmacher DW et al (2015) Multi-parametric hydrogels support 3D in vitro bioengineered microenvironment models of tumour angiogenesis. Biomaterials 53:609–620

    Article  Google Scholar 

  • Brudno Y, Ennett-Shepard AB, Chen RR, Aizenberg M, Mooney DJ (2013) Enhancing microvascular formation and vessel maturation through temporal control over multiple pro-angiogenic and pro-maturation factors. Biomaterials 34(36):9201–9209

    Article  Google Scholar 

  • Burdick JA (2011) Prestwich GD. Hyaluronic acid hydrogels for biomedical applications. Adv Mater 23(12):H41–H56

    Article  Google Scholar 

  • Caduff JH, Fischer LC, Burri PH (1986) Scanning electron microscope study of the developing microvasculature in the postnatal rat lung. Anat Rec 216(2):154–164

    Article  Google Scholar 

  • Carmeliet P (2000) Mechanisms of angiogenesis and arteriogenesis. Nat Med 6(4):389–395

    Article  Google Scholar 

  • Caspi O, Lesman A, Basevitch Y, Gepstein A, Arbel G, Habib IH et al (2007) Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 100(2):263–272

    Article  Google Scholar 

  • Chen X, Aledia AS, Ghajar CM, Griffith CK, Putnam AJ, Hughes CC et al (2009) Prevascularization of a fibrin-based tissue construct accelerates the formation of functional anastomosis with host vasculature. Tissue Eng Part A 15(6):1363–1371

    Article  Google Scholar 

  • Chen X, Aledia AS, Popson SA, Him L, Hughes CC, George SC (2010) Rapid anastomosis of endothelial progenitor cell-derived vessels with host vasculature is promoted by a high density of cotransplanted fibroblasts. Tissue Eng Part A 16(2):585–594

    Article  Google Scholar 

  • Chen JY, Feng L, Zhang HL, Li JC, Yang XW, Cao XL et al (2012a) Differential regulation of bone marrow-derived endothelial progenitor cells and endothelial outgrowth cells by the notch signaling pathway. PLoS One 7(10):e43643

    Article  Google Scholar 

  • Chen YC, Lin RZ, Qi H, Yang Y, Bae H, Melero-Martin JM et al (2012b) Functional human vascular network generated in Photocrosslinkable Gelatin methacrylate hydrogels. Adv Funct Mater 22(10):2027–2039

    Article  Google Scholar 

  • Chen P, Luo Z, Guven S, Tasoglu S, Ganesan AV, Weng A et al (2014) Microscale assembly directed by liquid-based template. Adv Mater 26(34):5936–5941

    Article  Google Scholar 

  • Chen P, Guven S, Usta OB, Yarmush ML, Demirci U (2015) Biotunable acoustic node assembly of organoids. Adv Healthc Mater 4(13):1937–1943

    Article  Google Scholar 

  • Cheng CC, Chang SJ, Chueh YN, Huang TS, Huang PH, Cheng SM et al (2013) Distinct angiogenesis roles and surface markers of early and late endothelial progenitor cells revealed by functional group analyses. BMC Genomics 14:182

    Article  Google Scholar 

  • Choi K (2002) The hemangioblast: a common progenitor of hematopoietic and endothelial cells. J Hematother Stem Cell Res 11(1):91–101

    Article  Google Scholar 

  • Choi KD, Yu J, Smuga-Otto K, Salvagiotto G, Rehrauer W, Vodyanik M et al (2009) Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 27(3):559–567

    Article  Google Scholar 

  • Chung ES, Chauhan SK, Jin Y, Nakao S, Hafezi-Moghadam A, van Rooijen N et al (2009) Contribution of macrophages to angiogenesis induced by vascular endothelial growth factor receptor-3-specific ligands. Am J Pathol 175(5):1984–1992

    Article  Google Scholar 

  • Chwalek K, Tsurkan MV, Freudenberg U, Werner C (2014a) Glycosaminoglycan-based hydrogels to modulate heterocellular communication in in vitro angiogenesis models. Sci Rep 4:4414

    Article  Google Scholar 

  • Chwalek K, Bray LJ, Werner C (2014b) Tissue-engineered 3D tumor angiogenesis models: potential technologies for anti-cancer drug discovery. Adv Drug Deliv Rev 79-80:30–39

    Article  Google Scholar 

  • Clough G (1991) Relationship between microvascular permeability and ultrastructure. Prog Biophys Mol Biol 55(1):47–69

    Article  Google Scholar 

  • Condeelis J, Pollard JW (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124(2):263–266

    Article  Google Scholar 

  • Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3(3):301–313

    Article  Google Scholar 

  • Cuchiara MP, Gould DJ, McHale MK, Dickinson ME, West JL (2012) Integration of self-assembled microvascular networks with microfabricated PEG-based hydrogels. Adv Funct Mater 22(21):4511–4518

    Article  Google Scholar 

  • Cui X, Boland T (2009) Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials 30(31):6221–6227

    Article  Google Scholar 

  • da Graca B, Filardo G (2011) Vascular bioprinting. Am J Cardiol 107(1):141–142

    Article  Google Scholar 

  • Davis GE, Senger DR (2005) Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 97(11):1093–1107

    Article  Google Scholar 

  • Davis GE, Black SM, Bayless KJ (2000) Capillary morphogenesis during human endothelial cell invasion of three-dimensional collagen matrices. In Vitro Cell Dev Biol Anim 36(8):513–519

    Article  Google Scholar 

  • Davis GE, Stratman AN, Sacharidou A, Koh W (2011) Molecular basis for endothelial lumen formation and tubulogenesis during vasculogenesis and angiogenic sprouting. Int Rev Cell Mol Biol 288:101–165

    Article  Google Scholar 

  • Diaz-Flores L, Gutierrez R, Madrid JF, Varela H, Valladares F, Acosta E et al (2009) Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 24(7):909–969

    Google Scholar 

  • Djonov V, Baum O, Burri PH (2003) Vascular remodeling by intussusceptive angiogenesis. Cell Tissue Res 314(1):107–117

    Article  Google Scholar 

  • Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87:27–45

    Google Scholar 

  • Doulatov S, Notta F, Laurenti E, Dick JE (2012) Hematopoiesis: a human perspective. Cell Stem Cell 10(2):120–136

    Article  Google Scholar 

  • Ehrbar M, Zeisberger SM, Raeber GP, Hubbell JA, Schnell C, Zisch AH (2008) The role of actively released fibrin-conjugated VEGF for VEGF receptor 2 gene activation and the enhancement of angiogenesis. Biomaterials 29(11):1720–1729

    Article  Google Scholar 

  • Eming SA, Brachvogel B, Odorisio T, Koch M (2007) Regulation of angiogenesis: wound healing as a model. Prog Histochem Cytochem 42(3):115–170

    Article  Google Scholar 

  • Fantin A, Vieira JM, Gestri G, Denti L, Schwarz Q, Prykhozhij S et al (2010) Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116(5):829–840

    Article  Google Scholar 

  • Feder J, Marasa JC, Olander JV (1983) The formation of capillary-like tubes by calf aortic endothelial cells grown in vitro. J Cell Physiol 116(1):1–6

    Article  Google Scholar 

  • Feng Q, SJ L, Klimanskaya I, Gomes I, Kim D, Chung Y et al (2010) Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells 28(4):704–712

    Article  Google Scholar 

  • Flamme I, Risau W (1992) Induction of vasculogenesis and hematopoiesis in vitro. Development 116(2):435–439

    Google Scholar 

  • Flamme I, Baranowski A, Risau W (1993) A new model of vasculogenesis and angiogenesis in vitro as compared with vascular growth in the avian area vasculosa. Anat Rec 237(1):49–57

    Article  Google Scholar 

  • Folkman J, Haudenschild C (1980) Angiogenesis in vitro. Nature 288(5791):551–556

    Article  Google Scholar 

  • Fuchs S, Hermanns MI, Kirkpatrick CJ (2006a) Retention of a differentiated endothelial phenotype by outgrowth endothelial cells isolated from human peripheral blood and expanded in long-term cultures. Cell Tissue Res 326(1):79–92

    Article  Google Scholar 

  • Fuchs S, Motta A, Migliaresi C, Kirkpatrick CJ (2006b) Outgrowth endothelial cells isolated and expanded from human peripheral blood progenitor cells as a potential source of autologous cells for endothelialization of silk fibroin biomaterials. Biomaterials 27(31):5399–5408

    Article  Google Scholar 

  • Fuchs S, Jiang X, Schmidt H, Dohle E, Ghanaati S, Orth C et al (2009) Dynamic processes involved in the pre-vascularization of silk fibroin constructs for bone regeneration using outgrowth endothelial cells. Biomaterials 30(7):1329–1338

    Article  Google Scholar 

  • Gaengel K, Genove G, Armulik A, Betsholtz C (2009) Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 29(5):630–638

    Article  Google Scholar 

  • Gallagher G, Sumpio BE (1997) Vascular endothelial cells. In: Sumpio BE, Sidawy AS (eds) Basic science of vascular disease. Futura Publishing Co, Mt. Kisco, pp 151–186

    Google Scholar 

  • Gao B, Yang Q, Zhao X, Jin G, Ma Y, Xu F (2016) 4D bioprinting for biomedical applications. Trends Biotechnol

    Google Scholar 

  • Garvin KA, Dalecki D, Hocking DC (2011) Vascularization of three-dimensional collagen hydrogels using ultrasound standing wave fields. Ultrasound Med Biol 37(11):1853–1864

    Article  Google Scholar 

  • Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K, Otte M et al (2000) Vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95(10):3106–3112

    Google Scholar 

  • Ghajar CM, Chen X, Harris JW, Suresh V, Hughes CC, Jeon NL et al (2008) The effect of matrix density on the regulation of 3-D capillary morphogenesis. Biophys J 94(5):1930–1941

    Article  Google Scholar 

  • Ghajar CM, Kachgal S, Kniazeva E, Mori H, Costes SV, George SC et al (2010) Mesenchymal cells stimulate capillary morphogenesis via distinct proteolytic mechanisms. Exp Cell Res 316(5):813–825

    Article  Google Scholar 

  • Gobin AS, West JL (2002) Cell migration through defined, synthetic ECM analogs. FASEB J 16(7):751–753

    Google Scholar 

  • Grant DS, Tashiro K, Segui-Real B, Yamada Y, Martin GR, Kleinman HK (1989) Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell 58(5):933–943

    Article  Google Scholar 

  • Guerrero J, Oliveira H, Catros S, Siadous R, Derkaoui SM, Bareille R et al (2015) The use of total human bone marrow fraction in a direct three-dimensional expansion approach for bone tissue engineering applications: focus on angiogenesis and osteogenesis. Tissue Eng Part A 21(5-6):861–874

    Article  Google Scholar 

  • Hanjaya-Putra D, Bose V, Shen YI, Yee J, Khetan S, Fox-Talbot K et al (2011) Controlled activation of morphogenesis to generate a functional human microvasculature in a synthetic matrix. Blood 118(3):804–815

    Article  Google Scholar 

  • Hanjaya-Putra D, Wong KT, Hirotsu K, Khetan S, Burdick JA, Gerecht S (2012) Spatial control of cell-mediated degradation to regulate vasculogenesis and angiogenesis in hyaluronan hydrogels. Biomaterials 33(26):6123–6131

    Article  Google Scholar 

  • Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C (1999) Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126(14):3047–3055

    Google Scholar 

  • Higashiyama S, Abraham JA, Klagsbrun M (1993) Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: dependence on interactions with cell surface heparan sulfate. J Cell Biol 122(4):933–940

    Article  Google Scholar 

  • Hirashima M, Kataoka H, Nishikawa S, Matsuyoshi N, Nishikawa S (1999a) Maturation of embryonic stem cells into endothelial cells in an in vitro model of vasculogenesis. Blood 93(4):1253–1263

    Google Scholar 

  • Hirashima M, Kataoka H, Nishikawa S, Matsuyoshi N, Nishikawa SI (1999b) Maturation of embryonic stem cells into endothelial cells in an in vitro model of vasculogenesis. Blood 93(4):1253–1263

    Google Scholar 

  • Hirschi KK, Rohovsky SA, D'Amore PA (1998) PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 141(3):805–814

    Article  Google Scholar 

  • Homma K, Sone M, Taura D, Yamahara K, Suzuki Y, Takahashi K et al (2010) Sirt1 plays an important role in mediating greater functionality of human ES/iPS-derived vascular endothelial cells. Atherosclerosis 212(1):42–47

    Article  Google Scholar 

  • Hsu CW, Poche RA, Saik JE, Ali S, Wang S, Yosef N et al (2015) Improved angiogenesis in response to localized delivery of macrophage-recruiting molecules. PLoS One 10(7):e0131643

    Article  Google Scholar 

  • Ingber DE, Folkman J (1989) Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J Cell Biol 109(1):317–330

    Article  Google Scholar 

  • Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K et al (2004) Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104(9):2752–2760

    Article  Google Scholar 

  • Irwin D, Helm K, Campbell N, Imamura M, Fagan K, Harral J et al (2007) Neonatal lung side population cells demonstrate endothelial potential and are altered in response to hyperoxia-induced lung simplification. Am J Physiol Lung Cell Mol Physiol 293(4):L941–L951

    Article  Google Scholar 

  • Itskovitz-Eldor J, Schuldiner M, Karsenti D, Eden A, Yanuka O, Amit M et al (2000) Differentiation of human embryonic stem cells into embryoid bodies comprising the three embryonic germ layers. Mol Med 6(2):88–95

    Google Scholar 

  • Jain RK (2003) Molecular regulation of vessel maturation. Nat Med 9(6):685–693

    Article  Google Scholar 

  • Janmey PA, Winer JP, Weisel JW (2009) Fibrin gels and their clinical and bioengineering applications. J R Soc Interface 6(30):1–10

    Article  Google Scholar 

  • Jeon JS, Bersini S, Gilardi M, Dubini G, Charest JL, Moretti M et al (2015) Human 3D vascularized organotypic microfluidic assays to study breast cancer cell extravasation. Proc Natl Acad Sci U S A 112(1):214–219

    Article  Google Scholar 

  • Jetten N, Verbruggen S, Gijbels MJ, Post MJ, De Winther MP, Donners MM (2014) Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis 17(1):109–118

    Article  Google Scholar 

  • Kachgal S, Putnam AJ (2011) Mesenchymal stem cells from adipose and bone marrow promote angiogenesis via distinct cytokine and protease expression mechanisms. Angiogenesis 14(1):47–59

    Article  Google Scholar 

  • Kachgal S, Carrion B, Janson IA, Putnam AJ (2012) Bone marrow stromal cells stimulate an angiogenic program that requires endothelial MT1-MMP. J Cell Physiol 227(11):3546–3555

    Article  Google Scholar 

  • Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M et al (2000) Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A 97(7):3422–3427

    Article  Google Scholar 

  • Kamath S, Lip GY (2003) Fibrinogen: biochemistry, epidemiology and determinants. QJM 96(10):711–729

    Article  Google Scholar 

  • Kaufman DS, Hanson ET, Lewis RL, Auerbach R, Thomson JA (2001) Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A 98(19):10716–10721

    Article  Google Scholar 

  • Khetan S, Burdick JA (2010) Patterning network structure to spatially control cellular remodeling and stem cell fate within 3-dimensional hydrogels. Biomaterials 31(32):8228–8234

    Article  Google Scholar 

  • Kim KW, Song JH (2017) Emerging roles of lymphatic vasculature in immunity. Immune Netw 17(1):68–76

    Article  Google Scholar 

  • Kim S, Lee H, Chung M, Jeon NL (2013) Engineering of functional, perfusable 3D microvascular networks on a chip. Lab Chip 13(8):1489–1500

    Article  Google Scholar 

  • Klar AS, Guven S, Biedermann T, Luginbuhl J, Bottcher-Haberzeth S, Meuli-Simmen C et al (2014) Tissue-engineered dermo-epidermal skin grafts prevascularized with adipose-derived cells. Biomaterials 35(19):5065–5078

    Article  Google Scholar 

  • Klar AS, Guven S, Zimoch J, Zapiorkowska NA, Biedermann T, Bottcher-Haberzeth S et al (2016) Characterization of vasculogenic potential of human adipose-derived endothelial cells in a three-dimensional vascularized skin substitute. Pediatr Surg Int 32(1):17–27

    Article  Google Scholar 

  • Kleinman HK, Martin GR (2005) Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol 15(5):378–386

    Article  Google Scholar 

  • Kleinman HK, McGarvey ML, Liotta LA, Robey PG, Tryggvason K, Martin GR (1982) Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21(24):6188–6193

    Article  Google Scholar 

  • Kleinman HK, McGarvey ML, Hassell JR, Star VL, Cannon FB, Laurie GW et al (1986) Basement membrane complexes with biological activity. Biochemistry 25(2):312–318

    Article  Google Scholar 

  • Kleinstreuer NC, Judson RS, Reif DM, Sipes NS, Singh AV, Chandler KJ et al (2011) Environmental impact on vascular development predicted by high-throughput screening. Environ Health Perspect 119(11):1596–1603

    Article  Google Scholar 

  • Kniazeva E, Putnam AJ (2009) Endothelial cell traction and ECM density influence both capillary morphogenesis and maintenance in 3-D. Am J Physiol Cell Physiol 297(1):C179–C187

    Article  Google Scholar 

  • Koh W, Stratman AN, Sacharidou A, Davis GE (2008) Vitro three dimensional collagen matrix models of endothelial lumen formation during vasculogenesis and angiogenesis. Methods Enzymol 443:83–101

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Krah K, Mironov V, Risau W, Flamme I (1994) Induction of vasculogenesis in quail blastodisc-derived embryoid bodies. Dev Biol 164(1):123–132

    Article  Google Scholar 

  • Kreuger J, Phillipson M (2016) Targeting vascular and leukocyte communication in angiogenesis, inflammation and fibrosis. Nat Rev Drug Discov 15(2):125–142

    Article  Google Scholar 

  • Kubota Y, Kleinman HK, Martin GR, Lawley TJ (1988) Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 107(4):1589–1598

    Article  Google Scholar 

  • Kucukgul C, Ozler SB, Inci I, Karakas E, Irmak S, Gozuacik D et al (2015) 3D bioprinting of biomimetic aortic vascular constructs with self-supporting cells. Biotechnol Bioeng 112(4):811–821

    Article  Google Scholar 

  • Kunder CA, St John AL, Abraham SN (2011) Mast cell modulation of the vascular and lymphatic endothelium. Blood 118(20):5383–5393

    Article  Google Scholar 

  • Kundu B, Rajkhowa R, Kundu SC, Wang X (2013) Silk fibroin biomaterials for tissue regenerations. Adv Drug Deliv Rev 65(4):457–470

    Article  Google Scholar 

  • Kusuma S, Shen YI, Hanjaya-Putra D, Mali P, Cheng L, Gerecht S (2013) Self-organized vascular networks from human pluripotent stem cells in a synthetic matrix. Proc Natl Acad Sci U S A 110(31):12601–12606

    Article  Google Scholar 

  • Lesman A, Koffler J, Atlas R, Blinder YJ, Kam Z, Levenberg S (2011) Engineering vessel-like networks within multicellular fibrin-based constructs. Biomaterials 32(31):7856–7869

    Article  Google Scholar 

  • Levenberg S (2005) Engineering blood vessels from stem cells: recent advances and applications. Curr Opin Biotechnol 16(5):516–523

    Article  Google Scholar 

  • Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R (2002) Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A 99(7):4391–4396

    Article  Google Scholar 

  • Levenberg S, Huang NF, Lavik E, Rogers AB, Itskovitz-Eldor J, Langer R (2003) Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proc Natl Acad Sci U S A 100(22):12741–12746

    Article  Google Scholar 

  • Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC et al (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23(7):879–884

    Article  Google Scholar 

  • Li S, Li B, Jiang H, Wang Y, Qu M, Duan H et al (2013) Macrophage depletion impairs corneal wound healing after autologous transplantation in mice. PLoS One 8(4):e61799

    Article  Google Scholar 

  • Lin Y, Weisdorf DJ, Solovey A, Hebbel RP (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105(1):71–77

    Article  Google Scholar 

  • Lin K, Matsubara Y, Masuda Y, Togashi K, Ohno T, Tamura T et al (2008) Characterization of adipose tissue-derived cells isolated with the Celution system. Cytotherapy 10(4):417–426

    Article  Google Scholar 

  • Liu Y, Teoh SH, Chong MS, Lee ES, Mattar CN, Randhawa NK et al (2012) Vasculogenic and osteogenesis-enhancing potential of human umbilical cord blood endothelial colony-forming cells. Stem Cells 30(9):1911–1924

    Article  Google Scholar 

  • Loessner D, Meinert C, Kaemmerer E, Martine LC, Yue K, Levett PA et al (2016) Functionalization, preparation and use of cell-laden gelatin methacryloyl-based hydrogels as modular tissue culture platforms. Nat Protoc 11(4):727–746

    Article  Google Scholar 

  • Looney MR, Matthay MA (2009) Neutrophil sandwiches injure the microcirculation. Nat Med 15(4):364–366

    Article  Google Scholar 

  • Lord ST (2007) Fibrinogen and fibrin: scaffold proteins in hemostasis. Curr Opin Hematol 14(3):236–241

    Article  Google Scholar 

  • Lutolf MP, Hubbell JA (2003) Synthesis and physicochemical characterization of end-linked poly(ethylene glycol)-co-peptide hydrogels formed by Michael-type addition. Biomacromolecules 4(3):713–722

    Article  Google Scholar 

  • Lutolf MP, Weber FE, Schmoekel HG, Schense JC, Kohler T, Muller R et al (2003a) Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nat Biotechnol 21(5):513–518

    Article  Google Scholar 

  • Lutolf MP, Lauer-Fields JL, Schmoekel HG, Metters AT, Weber FE, Fields GB et al (2003b) Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci U S A 100(9):5413–5418

    Article  Google Scholar 

  • Maciag T, Kadish J, Wilkins L, Stemerman MB, Weinstein R (1982) Organizational behavior of human umbilical vein endothelial cells. J Cell Biol 94(3):511–520

    Article  Google Scholar 

  • Madri JA, Williams SK (1983) Capillary endothelial cell cultures: phenotypic modulation by matrix components. J Cell Biol 97(1):153–165

    Article  Google Scholar 

  • Majka SM, Jackson KA, Kienstra KA, Majesky MW, Goodell MA, Hirschi KK (2003) Distinct progenitor populations in skeletal muscle are bone marrow derived and exhibit different cell fates during vascular regeneration. J Clin Invest 111(1):71–79

    Article  Google Scholar 

  • Marino D, Luginbuhl J, Scola S, Meuli M, Reichmann E (2014) Bioengineering dermo-epidermal skin grafts with blood and lymphatic capillaries. Sci Transl Med 6(221):221ra14

    Article  Google Scholar 

  • Masuda H, Asahara T (2003) Post-natal endothelial progenitor cells for neovascularization in tissue regeneration. Cardiovasc Res 58(2):390–398

    Article  Google Scholar 

  • Mathiisen TM, Lehre KP, Danbolt NC, Ottersen OP (2010) The perivascular Astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 58(9):1094–1103

    Article  Google Scholar 

  • McKercher SR, Torbett BE, Anderson KL, Henkel GW, Vestal DJ, Baribault H et al (1996) Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J 15(20):5647–5658

    Google Scholar 

  • Medina RJ, O'Neill CL, Sweeney M, Guduric-Fuchs J, Gardiner TA, Simpson DA et al (2010) Molecular analysis of endothelial progenitor cell (EPC) subtypes reveals two distinct cell populations with different identities. BMC Med Genet 3:18

    Google Scholar 

  • Melchiorri AJ, Nguyen BNB, Fisher JP (2014) Mesenchymal stem cells: roles and relationships in vascularization. Tissue Eng Part B-Re 20(3):218–228

    Article  Google Scholar 

  • Miranville A, Heeschen C, Sengenes C, Curat CA, Busse R, Bouloumie A (2004) Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 110(3):349–355

    Article  Google Scholar 

  • Mironov V, Kasyanov V, Markwald RR (2008) Nanotechnology in vascular tissue engineering: from nanoscaffolding towards rapid vessel biofabrication. Trends Biotechnol 26(6):338–344

    Article  Google Scholar 

  • Montano I, Schiestl C, Schneider J, Pontiggia L, Luginbuhl J, Biedermann T et al (2010) Formation of human capillaries in vitro: the engineering of prevascularized matrices. Tissue Eng Part A 16(1):269–282

    Article  Google Scholar 

  • Montesano R, Orci L (1985) Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell 42(2):469–477

    Article  Google Scholar 

  • Montesano R, Orci L, Vassalli P (1983) Vitro rapid organization of endothelial cells into capillary-like networks is promoted by collagen matrices. J Cell Biol 97(5 Pt 1):1648–1652

    Article  Google Scholar 

  • Montesano R, Mouron P, Orci L (1985) Vascular outgrowths from tissue explants embedded in fibrin or collagen gels: a simple in vitro model of angiogenesis. Cell Biol Int Rep 9(10):869–875

    Article  Google Scholar 

  • Montesano R, Vassalli JD, Baird A, Guillemin R, Orci L (1986) Basic fibroblast growth factor induces angiogenesis in vitro. Proc Natl Acad Sci U S A 83(19):7297–7301

    Article  Google Scholar 

  • Montesano R, Pepper MS, Vassalli JD, Orci L (1987) Phorbol ester induces cultured endothelial cells to invade a fibrin matrix in the presence of fibrinolytic inhibitors. J Cell Physiol 132(3):509–516

    Article  Google Scholar 

  • Moon JJ, Saik JE, Poche RA, Leslie-Barbick JE, Lee SH, Smith AA et al (2010) Biomimetic hydrogels with pro-angiogenic properties. Biomaterials 31(14):3840–3847

    Article  Google Scholar 

  • Mukai N, Akahori T, Komaki M, Li Q, Kanayasu-Toyoda T, Ishii-Watabe A et al (2008) A comparison of the tube forming potentials of early and late endothelial progenitor cells. Exp Cell Res 314(3):430–440

    Article  Google Scholar 

  • Naldini A, Carraro F (2005) Role of inflammatory mediators in angiogenesis. Curr Drug Targets Inflamm Allergy 4(1):3–8

    Article  Google Scholar 

  • Nguyen DH, Stapleton SC, Yang MT, Cha SS, Choi CK, Galie PA et al (2013) Biomimetic model to reconstitute angiogenic sprouting morphogenesis in vitro. Proc Natl Acad Sci U S A 110(17):6712–6717

    Article  Google Scholar 

  • Nichol JW, Koshy ST, Bae H, Hwang CM, Yamanlar S, Khademhosseini A (2010) Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 31(21):5536–5544

    Article  Google Scholar 

  • Nicosia RF, Madri JA (1987) The microvascular extracellular matrix. Developmental changes during angiogenesis in the aortic ring-plasma clot model. Am J Pathol 128(1):78–90

    Google Scholar 

  • Nicosia RF, Tchao R, Leighton J (1982) Histotypic angiogenesis in vitro: light microscopic, ultrastructural, and radioautographic studies. In Vitro 18(6):538–549

    Article  Google Scholar 

  • Nicosia RF, Tchao R, Leighton J (1986) Interactions between newly formed endothelial channels and carcinoma cells in plasma clot culture. Clin Exp Metastasis 4(2):91–104

    Article  Google Scholar 

  • Nishikawa S, Nishikawa S, Hirashima M, Matsuyoshi N, Kodama H (1998) Progressive lineage analysis by cell sorting and culture identifies FLK1(+)VE-cadherin(+) cells at a diverging point of endothelial and hemopoietic lineages. Development 125(9):1747–1757

    Google Scholar 

  • Nolan DJ, Ciarrocchi A, Mellick AS, Jaggi JS, Bambino K, Gupta S et al (2007) Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization. Genes Dev 21(12):1546–1558

    Article  Google Scholar 

  • Norotte C, Marga FS, Niklason LE, Forgacs G (2009) Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30(30):5910–5917

    Article  Google Scholar 

  • Novosel EC, Kleinhans C, Kluger PJ (2011) Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 63(4-5):300–311

    Article  Google Scholar 

  • Olander JV, Bremer ME, Marasa JC, Feder J (1985) Fibrin-enhanced endothelial cell organization. J Cell Physiol 125(1):1–9

    Article  Google Scholar 

  • Oyama T, Nagai T, Wada H, Naito AT, Matsuura K, Iwanaga K et al (2007) Cardiac side population cells have a potential to migrate and differentiate into cardiomyocytes in vitro and in vivo. J Cell Biol 176(3):329–341

    Article  Google Scholar 

  • Park KM, Gerecht S (2014) Harnessing developmental processes for vascular engineering and regeneration. Development 141(14):2760–2769

    Article  Google Scholar 

  • Park HJ, Zhang Y, Georgescu SP, Johnson KL, Kong D, Galper JB (2006) Human umbilical vein endothelial cells and human dermal microvascular endothelial cells offer new insights into the relationship between lipid metabolism and angiogenesis. Stem Cell Rev 2(2):93–102

    Article  Google Scholar 

  • Park YK, TY T, Lim SH, Clement IJ, Yang SY, Kamm RD (2014) Microvessel growth and Remodeling within a three-dimensional microfluidic environment. Cell Mol Bioeng 7(1):15–25

    Article  Google Scholar 

  • Peck M, Gebhart D, Dusserre N, McAllister TN, L'Heureux N (2012) The evolution of vascular tissue engineering and current state of the art. Cells Tissues Organs 195(1-2):144–158

    Article  Google Scholar 

  • Pedersen TO, Blois AL, Xue Y, Xing Z, Sun Y, Finne-Wistrand A et al (2014) Mesenchymal stem cells induce endothelial cell quiescence and promote capillary formation. Stem Cell Res Ther 5(1):23

    Article  Google Scholar 

  • Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M et al (2000) Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 95(3):952–958

    Google Scholar 

  • Pelletier L, Regnard J, Fellmann D, Charbord P (2000) An in vitro model for the study of human bone marrow angiogenesis: role of hematopoietic cytokines. Lab Invest 80(4):501–511

    Article  Google Scholar 

  • Phelps EA, Garcia AJ (2010) Engineering more than a cell: vascularization strategies in tissue engineering. Curr Opin Biotechnol 21(5):704–709

    Article  Google Scholar 

  • Phelps EA, Landazuri N, Thule PM, Taylor WR, Garcia AJ (2010) Bioartificial matrices for therapeutic vascularization. Proc Natl Acad Sci U S A 107(8):3323–3328

    Article  Google Scholar 

  • Piskin S, Undar A, Pekkan K (2015) Computational Modeling of neonatal cardiopulmonary bypass Hemodynamics with full circle of Willis anatomy. Artif Organs 39(10):E164–E175

    Article  Google Scholar 

  • Planat-Benard V, Silvestre JS, Cousin B, Andre M, Nibbelink M, Tamarat R et al (2004) Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 109(5):656–663

    Article  Google Scholar 

  • Pollard JW (2009) Trophic macrophages in development and disease. Nat Rev Immunol 9(4):259–270

    Article  Google Scholar 

  • Rafii S, Lyden D (2003) Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9(6):702–712

    Article  Google Scholar 

  • Rafii S, Shapiro F, Rimarachin J, Nachman RL, Ferris B, Weksler B et al (1994) Isolation and characterization of human bone marrow microvascular endothelial cells: hematopoietic progenitor cell adhesion. Blood 84(1):10–19

    Google Scholar 

  • Rao RR, Peterson AW, Ceccarelli J, Putnam AJ, Stegemann JP (2012) Matrix composition regulates three-dimensional network formation by endothelial cells and mesenchymal stem cells in collagen/fibrin materials. Angiogenesis 15(2):253–264

    Article  Google Scholar 

  • Rathjen PD, Lake J, Whyatt LM, Bettess MD, Rathjen J (1998) Properties and uses of embryonic stem cells: prospects for application to human biology and gene therapy. Reprod Fert Develop 10(1):31–47

    Article  Google Scholar 

  • Risau W (1991) Embryonic angiogenesis factors. Pharmacol Therapeut 51(3):371–376

    Article  Google Scholar 

  • Risau W (1997) Mechanisms of angiogenesis. Nature 386(6626):671–674

    Article  Google Scholar 

  • Risau W, Sariola H, Zerwes HG, Sasse J, Ekblom P, Kemler R et al (1988) Vasculogenesis and angiogenesis in embryonic-stem-cell-derived embryoid bodies. Development 102(3):471–478

    Google Scholar 

  • Roudsari LC, Jeffs SE, Witt AS, Gill BJ, West JL (2016) A 3D poly(ethylene glycol)-based tumor angiogenesis model to study the influence of vascular cells on lung tumor cell behavior. Sci Rep 6:32726

    Article  Google Scholar 

  • Rouwkema J, Khademhosseini A (2016) Vascularization and angiogenesis in tissue engineering: beyond creating static networks. Trends Biotechnol. 34(9):733–45. https://doi.org/10.1016/j.tibtech.2016.03.002.

  • Sage EH, Vernon RB (1994) Regulation of angiogenesis by extracellular matrix: the growth and the glue. Journal of hypertension supplement : official journal of the international society of. Hypertension 12(10):S145–S152

    Google Scholar 

  • Sakaguchi K, Shimizu T, Horaguchi S, Sekine H, Yamato M, Umezu M et al (2013) In vitro engineering of vascularized tissue surrogates. Sci Rep 3:1316

    Article  Google Scholar 

  • Sala A, Hanseler P, Ranga A, Lutolf MP, Voros J, Ehrbar M et al (2011) Engineering 3D cell instructive microenvironments by rational assembly of artificial extracellular matrices and cell patterning. Integr Biol 3(11):1102–1111

    Article  Google Scholar 

  • Salazar R, Bell SE, Davis GE (1999) Coordinate induction of the actin cytoskeletal regulatory proteins gelsolin, vasodilator-stimulated phosphoprotein, and profilin during capillary morphogenesis in vitro. Exp Cell Res 249(1):22–32

    Article  Google Scholar 

  • Salven P, Mustjoki S, Alitalo R, Alitalo K, Rafii S (2003) VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells. Blood 101(1):168–172

    Article  Google Scholar 

  • Scherberich A, Galli R, Jaquiery C, Farhadi J, Martin I (2007) Three-dimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem Cells 25(7):1823–1829

    Article  Google Scholar 

  • Scherberich A, Muller AM, Schafer DJ, Banfi A, Martin I (2010) Adipose tissue-derived progenitors for engineering osteogenic and vasculogenic grafts. J Cell Physiol 225(2):348–353

    Article  Google Scholar 

  • Schuh AC, Faloon P, QL H, Bhimani M, Choi K (1999) Vitro hematopoietic and endothelial potential of flk-1(−/−) embryonic stem cells and embryos. Proc Natl Acad Sci U S A 96(5):2159–2164

    Article  Google Scholar 

  • Shepherd BR, Chen HY, Smith CM, Gruionu G, Williams SK, Hoying JB (2004) Rapid perfusion and network remodeling in a microvascular construct after implantation. Arterioscler Thromb Vasc Biol 24(5):898–904

    Article  Google Scholar 

  • Shi Q, Rafii S, MH W, Wijelath ES, Yu C, Ishida A et al (1998) Evidence for circulating bone marrow-derived endothelial cells. Blood 92(2):362–367

    Google Scholar 

  • Shi Y, Kramer G, Schroder A, Kirkpatrick CJ, Seekamp A, Schmidt H et al (2014) Early endothelial progenitor cells as a source of myeloid cells to improve the pre-vascularisation of bone constructs. Eur Cell Mater 27:64–79. discussion 79–80

    Article  Google Scholar 

  • Shin Y, Jeon JS, Han S, Jung GS, Shin S, Lee SH et al (2011) In vitro 3D collective sprouting angiogenesis under orchestrated ANG-1 and VEGF gradients. Lab Chip 11(13):2175–2181

    Article  Google Scholar 

  • Sieminski AL, Hebbel RP, Gooch KJ (2004) The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro. Exp Cell Res 297(2):574–584

    Article  Google Scholar 

  • Sieveking DP, Buckle A, Celermajer DS, Ng MK (2008) Strikingly different angiogenic properties of endothelial progenitor cell subpopulations: insights from a novel human angiogenesis assay. J Am Coll Cardiol 51(6):660–668

    Article  Google Scholar 

  • Sims DE (1986) The pericyte – a review. Tissue Cell 18(2):153–174

    Article  Google Scholar 

  • Sims DE (1991) Recent advances in pericyte biology – implications for health and disease. Can J Cardiol 7(10):431–443

    Google Scholar 

  • Singh RK, Seliktar D, Putnam AJ (2013) Capillary morphogenesis in PEG-collagen hydrogels. Biomaterials 34(37):9331–9340

    Article  Google Scholar 

  • Skardal A, Zhang J, Prestwich GD (2010) Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates. Biomaterials 31(24):6173–6181

    Article  Google Scholar 

  • Slaughter BV, Khurshid SS, Fisher OZ, Khademhosseini A, Peppas NA (2009) Hydrogels in regenerative medicine. Adv Mater 21(32-33):3307–3329

    Article  Google Scholar 

  • Smith AG (1992) Mouse embryo stem cells: their identification, propagation and manipulation. Semin Cell Biol 3(6):385–399

    Article  Google Scholar 

  • Smith AO, Bowers SL, Stratman AN, Davis GE (2013) Hematopoietic stem cell cytokines and fibroblast growth factor-2 stimulate human endothelial cell-pericyte tube co-assembly in 3D fibrin matrices under serum-free defined conditions. PLoS One 8(12):e85147

    Article  Google Scholar 

  • Sobrino A, Phan DT, Datta R, Wang X, Hachey SJ, Romero-Lopez M et al (2016) 3D microtumors in vitro supported by perfused vascular networks. Sci Rep 6:31589

    Article  Google Scholar 

  • Sooppan R, Paulsen SJ, Han J, Ta AH, Dinh P, Gaffey AC et al (2016) In vivo anastomosis and perfusion of a three-dimensionally-printed construct containing microchannel networks. Tissue Eng Part C Methods 22(1):1–7

    Article  Google Scholar 

  • Spiller KL, Anfang RR, Spiller KJ, Ng J, Nakazawa KR, Daulton JW et al (2014) The role of macrophage phenotype in vascularization of tissue engineering scaffolds. Biomaterials 35(15):4477–4488

    Article  Google Scholar 

  • Stratman AN, Malotte KM, Mahan RD, Davis MJ, Davis GE (2009) Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 114(24):5091–5101

    Article  Google Scholar 

  • Stratman AN, Davis MJ, Davis GE (2011) VEGF and FGF prime vascular tube morphogenesis and sprouting directed by hematopoietic stem cell cytokines. Blood 117(14):3709–3719

    Article  Google Scholar 

  • Sun G, Shen YI, Kusuma S, Fox-Talbot K, Steenbergen CJ, Gerecht S (2011) Functional neovascularization of biodegradable dextran hydrogels with multiple angiogenic growth factors. Biomaterials 32(1):95–106

    Article  Google Scholar 

  • Susienka MJ, Medici D (2013) Vascular endothelium as a novel source of stem cells for bioengineering. Biomatter 3(3):e24647

    Article  Google Scholar 

  • Szoke K, Beckstrom KJ, Brinchmann JE (2012) Human adipose tissue as a source of cells with angiogenic potential. Cell Transplant 21(1):235–250

    Article  Google Scholar 

  • Taura D, Sone M, Homma K, Oyamada N, Takahashi K, Tamura N et al (2009) Induction and isolation of vascular cells from human induced pluripotent stem cells–brief report. Arterioscler Thromb Vasc Biol 29(7):1100–1103

    Article  Google Scholar 

  • ten Dijke P, Arthur HM (2007) Extracellular control of TGFbeta signalling in vascular development and disease. Nat Rev Mol Cell Biol 8(11):857–869

    Article  Google Scholar 

  • Tennent GA, Brennan SO, Stangou AJ, O'Grady J, Hawkins PN, Pepys MB (2007) Human plasma fibrinogen is synthesized in the liver. Blood 109(5):1971–1974

    Article  Google Scholar 

  • Tice RR, Austin CP, Kavlock RJ, Bucher JR (2013) Improving the human hazard characterization of chemicals: a Tox21 update. Environ Health Perspect 121(7):756–765

    Article  Google Scholar 

  • Tille JC, Pepper MS (2002) Mesenchymal cells potentiate vascular endothelial growth factor-induced angiogenesis in vitro. Exp Cell Res 280(2):179–191

    Article  Google Scholar 

  • Tremblay PL, Berthod F, Germain L, Auger FA (2005a) Vitro evaluation of the angiostatic potential of drugs using an endothelialized tissue-engineered connective tissue. J Pharmacol Exp Ther 315(2):510–516

    Article  Google Scholar 

  • Tremblay PL, Hudon V, Berthod F, Germain L, Auger FA (2005b) Inosculation of tissue-engineered capillaries with the host's vasculature in a reconstructed skin transplanted on mice. Am J Transplant 5(5):1002–1010

    Article  Google Scholar 

  • Tsurkan MV, Chwalek K, Prokoph S, Zieris A, Levental KR, Freudenberg U et al (2013) Defined polymer-peptide conjugates to form cell-instructive starPEG-heparin matrices in situ. Adv Mater 25(18):2606–2610

    Article  Google Scholar 

  • Unger RE, Krump-Konvalinkova V, Peters K, Kirkpatrick CJ (2002) In vitro expression of the endothelial phenotype: comparative study of primary isolated cells and cell lines, including the novel cell line HPMEC-ST1.6R. Microvasc Res 64(3):384–397

    Article  Google Scholar 

  • Unger RE, Peters K, Wolf M, Motta A, Migliaresi C, Kirkpatrick CJ (2004a) Endothelialization of a non-woven silk fibroin net for use in tissue engineering: growth and gene regulation of human endothelial cells. Biomaterials 25(21):5137–5146

    Article  Google Scholar 

  • Unger RE, Wolf M, Peters K, Motta A, Migliaresi C, James Kirkpatrick C (2004b) Growth of human cells on a non-woven silk fibroin net: a potential for use in tissue engineering. Biomaterials 25(6):1069–1075

    Article  Google Scholar 

  • Unger RE, Sartoris A, Peters K, Motta A, Migliaresi C, Kunkel M et al (2007) Tissue-like self-assembly in cocultures of endothelial cells and osteoblasts and the formation of microcapillary-like structures on three-dimensional porous biomaterials. Biomaterials 28(27):3965–3976

    Article  Google Scholar 

  • Unger RE, Ghanaati S, Orth C, Sartoris A, Barbeck M, Halstenberg S et al (2010) The rapid anastomosis between prevascularized networks on silk fibroin scaffolds generated in vitro with cocultures of human microvascular endothelial and osteoblast cells and the host vasculature. Biomaterials 31(27):6959–6967

    Article  Google Scholar 

  • Vailhe B, Ronot X, Tracqui P, Usson Y, Tranqui L (1997) In vitro angiogenesis is modulated by the mechanical properties of fibrin gels and is related to alpha(v)beta3 integrin localization. In Vitro Cell Dev Biol Anim 33(10):763–773

    Article  Google Scholar 

  • van Amerongen MJ, Harmsen MC, van Rooijen N, Petersen AH, van Luyn MJA (2007) Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice. Am J Pathol 170(3):818–829

    Article  Google Scholar 

  • Van Den Bulcke AI, Bogdanov B, De Rooze N, Schacht EH, Cornelissen M, Berghmans H (2000) Structural and rheological properties of methacrylamide modified gelatin hydrogels. Biomacromolecules 1(1):31–38

    Article  Google Scholar 

  • Vernon RB, Sage EH (1995) Between molecules and morphology. Extracellular matrix and creation of vascular form. Am J Pathol 147(4):873–883

    Google Scholar 

  • Vernon RB, Lara SL, Drake CJ, Iruela-Arispe ML, Angello JC, Little CD et al (1995) Organized type I collagen influences endothelial patterns during “spontaneous angiogenesis in vitro”: planar cultures as models of vascular development. In Vitro Cell Dev Biol Anim 31(2):120–131

    Article  Google Scholar 

  • Vigen M, Ceccarelli J, Putnam AJ (2014) Protease-sensitive PEG hydrogels regulate vascularization in vitro and in vivo. Macromol Biosci 14(10):1368–1379

    Article  Google Scholar 

  • Visconti RP (2010) Towards organ printing_ engineering an intra-organ branched vascular tree. Expert Opin Biol Ther 10:409–420

    Article  Google Scholar 

  • Vittet D, Prandini MH, Berthier R, Schweitzer A, Martin-Sisteron H, Uzan G et al (1996) Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood 88(9):3424–3431

    Google Scholar 

  • Vittet D, Buchou T, Schweitzer A, Dejana E, Huber P (1997) Targeted null-mutation in the vascular endothelial-cadherin gene impairs the organization of vascular-like structures in embryoid bodies. Proc Natl Acad Sci U S A 94(12):6273–6278

    Article  Google Scholar 

  • Wang R, Clark R, Bautch VL (1992) Embryonic stem cell-derived cystic embryoid bodies form vascular channels: an in vitro model of blood vessel development. Development 114(2):303–316

    Google Scholar 

  • Watanabe S, Morisaki N, Tezuka M, Fukuda K, Ueda S, Koyama N et al (1997) Cultured retinal pericytes stimulate in vitro angiogenesis of endothelial cells through secretion of a fibroblast growth factor-like molecule. Atherosclerosis 130(1-2):101–107

    Article  Google Scholar 

  • Weisel JW (2005) Fibrinogen and fibrin. Adv Protein Chem 70:247–299

    Article  Google Scholar 

  • Weisel JW (2008) Biophysics. Enigmas of blood clot elasticity. Science (New York, NY) 320(5875):456–457

    Article  Google Scholar 

  • Westermark B, Siegbahn A, Heldin CH, Claesson-Welsh L (1990) B-type receptor for platelet-derived growth factor mediates a chemotactic response by means of ligand-induced activation of the receptor protein-tyrosine kinase. Proc Natl Acad Sci U S A 87(1):128–132

    Article  Google Scholar 

  • Wetmore BA, Wambaugh JF, Ferguson SS, Li L, Clewell HJ 3rd, Judson RS et al (2013) Relative impact of incorporating pharmacokinetics on predicting in vivo hazard and mode of action from high-throughput in vitro toxicity assays. Toxicol Sci 132(2):327–346

    Article  Google Scholar 

  • White SM, Pittman CR, Hingorani R, Arora R, Esipova TV, Vinogradov SA et al (2014) Implanted cell-dense prevascularized tissues develop functional vasculature that supports reoxygenation after thrombosis. Tissue Eng Part A 20(17-18):2316–2328

    Article  Google Scholar 

  • Wong KH, Chan JM, Kamm RD, Tien J (2012) Microfluidic models of vascular functions. Annu Rev Biomed Eng 14:205–230

    Article  Google Scholar 

  • Xing Q, Yates K, Vogt C, Qian Z, Frost MC, Zhao F (2014) Increasing mechanical strength of gelatin hydrogels by divalent metal ion removal. Sci Rep 4:4706

    Article  Google Scholar 

  • Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T et al (2000) Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408(6808):92–96

    Article  Google Scholar 

  • Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F et al (2007) Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109(5):1801–1809

    Article  Google Scholar 

  • Zanotelli MR, Ardalani H, Zhang J, Hou Z, Nguyen EH, Swanson S et al (2016) Stable engineered vascular networks from human induced pluripotent stem cell-derived endothelial cells cultured in synthetic hydrogels. Acta Biomater 35:32–41

    Article  Google Scholar 

  • Zhang WJ, Park C, Arentson E, Choi K (2005) Modulation of hematopoietic and endothelial cell differentiation from mouse embryonic stem cells by different culture conditions. Blood 105(1):111–114

    Article  Google Scholar 

  • Zhang P, Baxter J, Vinod K, Tulenko TN, Di Muzio PJ (2009) Endothelial differentiation of amniotic fluid-derived stem cells: synergism of biochemical and shear force stimuli. Stem Cells Dev 18(9):1299–1308

    Article  Google Scholar 

  • Zhang B, Montgomery M, Chamberlain MD, Ogawa S, Korolj A, Pahnke A et al (2016) Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis. Nat Mater 15:669–678

    Article  Google Scholar 

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Blache, U., Guerrero, J., Güven, S., Klar, A.S., Scherberich, A. (2018). Microvascular Networks and Models, In vitro Formation. In: Holnthoner, W., Banfi, A., Kirkpatrick, J., Redl, H. (eds) Vascularization for Tissue Engineering and Regenerative Medicine. Reference Series in Biomedical Engineering(). Springer, Cham. https://doi.org/10.1007/978-3-319-21056-8_9-1

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  • DOI: https://doi.org/10.1007/978-3-319-21056-8_9-1

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  • Print ISBN: 978-3-319-21056-8

  • Online ISBN: 978-3-319-21056-8

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