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In Vitro and In Vivo Approaches for Pre-vascularization of 3-Dimensional Engineered Tissues

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Vascularization for Tissue Engineering and Regenerative Medicine

Part of the book series: Reference Series in Biomedical Engineering ((TIENRE))

Abstract

A major hurdle in tissue engineering of organs is the incorporation of a functioning blood vessel network integrated throughout the engineered tissue that readily links to the surrounding host blood vessels to provide the oxygen and nutrients required by the engineered construct. In the early years of tissue engineering development, vascularization was not a priority and generally angiogenic ingrowth from neighboring host capillary networks, a process termed extrinsic vascularization was used to vascularize implanted tissue engineering constructs. Extrinsic vascularization takes weeks, and much of the implanted tissue becomes ischemic and dies before capillary ingrowth is complete. In 2000, intrinsic vascularization was devised by Tanaka et al. who isolated a macrovascular pedicle in a plastic chamber which subsequently underwent considerable angiogenic sprouting. A new arteriovenous capillary network was therefore formed within the chamber space which was capable of growing with and supporting the survival of tissue/organ specific cells implanted in the chamber. There was a time lag to development of this pedicle-based angiogenic network, and in recent years a new technique termed pre-vascularization has been developed that involves co-culture of endothelial cells with parenchymal cells or stem cells as they assemble in vitro. Capillary networks are formed throughout the construct, and upon implantation inosculate (functionally join) with host capillaries. Inosculation takes at least 2 days and provides blood flow within this time period within the construct. The most efficient vascularization technique for thick three-dimensional tissue engineering would be the combination of pre-vascularization in vitro with vascularization via angiogenic sprouting of a vascular pedicle, this combination has rarely been successfully utilized.

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References

  • Arkudas A, Beier JP, Heidner K, Tjiawi J, Polykandriotis E, Srour S, Sturzl M, Horch RE, Kneser U (2007a) Axial prevascularization of porous matrices using an arteriovenous loop promotes survival and differentiation of transplanted autologous osteoblasts. Tissue Eng 13:1549–1560

    Article  Google Scholar 

  • Arkudas A, Tjiawi J, Bleiziffer O, Grabinger L, Polykandriotis E, Beier JP, Stürzl M, Horch RE, Kneser U (2007b) Fibrin gel-immobilized VEGF and bFGF efficiently stimulate angiogenesis in the AV loop model. Mol Med 13:480–487

    Article  Google Scholar 

  • Arkudas A, Tjiawi J, Saumweber A, Beier JP, Polykandriotis E, Bleiziffer O, Horch RE, Kneser U (2009) Evaluation of blood vessel ingrowth in fibrin gel subject to type and concentration of growth factors. J Cell Mol Med 13:2864–2874

    Article  Google Scholar 

  • Arkudas A, Pryymachuk G, Hoereth T, Beier JP, Polykandriotis E, Bleiziffer O, Gulle H, Horch RE, Kneser U (2012) Composition of fibrin glues significantly influences axial vascularization and degradation in isolation chamber model. Blood Coagul Fibrinolysis 23:419–427

    Article  Google Scholar 

  • Arkudas A, Balzer A, Buehrer G, Arnold I, Hoppe A, Detsch R, Newby P, Fey T, Greil P, Horch RE, Boccaccini AR, Kneser U (2013) Evaluation of angiogenesis of bioactive glass in the arteriovenous loop model. Tissue Eng Part C 19:479–486

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Auger FA, Berthod F, Moulin V, Pouliot R, Germain L (2004) Tissue-engineered skin substitutes: from in vitro constructs to in vivo applications. Biotechnol Appl Biochem 39:263–275

    Article  Google Scholar 

  • Auger FA, Gibot L, Lacroix D (2013) The pivotal role of vascularization in tissue engineering. Annu Rev Biomed Eng 15:177–200

    Article  Google Scholar 

  • Ayvazyan A, Morimoto N, Kanda N, Takemoto S, Kawai K, Sakamoto Y, Taira T, Suzuki S (2011) Collagen-gelatin scaffold impregnated with bFGF accelerates palatal wound healing of palatal mucosa in dogs. J Surg Res 17:e247–e257

    Article  Google Scholar 

  • Bach AD, Arkudas A, Tjiawi J, Polykandriotis E, Kneser U, Horch RE, Beier JP (2006) A new approach to tissue engineering of vascularized skeletal muscle. J Cell Mol Med 10:716–726

    Article  Google Scholar 

  • Bak S, Ahmad T, Lee YB, Lee JY, Kim EM, Shin H (2016) Delivery of a cell patch of cocultured endothelial cells and smooth muscle cells using thermoresponsive hydrogels for enhanced angiogenesis. Tissue Eng Part A 22:182–193

    Article  Google Scholar 

  • Barreto-Ortiz SF, Fradkin J, Eoh J, Trivero J, Davenport M, Ginn B, Mao HQ, Gerecht S (2015) Fabrication of 3-dimensional multicellular microvascular structures. FASEB J 29:3302–3314

    Article  Google Scholar 

  • Benjamin LE, Hemo I, Keshet E (1998) A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 125:1591–1598

    Google Scholar 

  • Bitto FF, Klumpp D, Lange C, Boos AM, Arkudas A, Bleiziffer O, Horch RE, Kneser U, Beier JP (2013) Myogenic differentiation of mesenchymal stem cells in a newly developed neurotised AV-loop model. Biomed Res Int 2013:935046

    Google Scholar 

  • Black AF, Berthod F, L’heureux N, Germain L, Auger FA (1998) In vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. FASEB J 12:1331–1334

    Google Scholar 

  • Boos AM, Loew JS, Weigand A, Deschler G, Klumpp D, Arkudas A, Bleiziffer O, Gulle H, Kneser U, Horch RE, Beier JP (2013) Engineering axially vascularized bone in the sheep arteriovenous-loop model. J Tissue Eng Regen Med 7:654–664

    Article  Google Scholar 

  • Bowers SL, Meng CX, Davis MT, Davis GE (2015) Investigating human vascular tube morphogenesis and maturation using endothelial cell-pericyte co-cultures and a doxycycline-inducible genetic system in 3D extracellular matrices. Methods Mol Biol 1189:171–189

    Article  Google Scholar 

  • Browne S, Monaghan MG, Brauchle E, Berrio DC, Chantepie S, Papy-Garcia D, Schenke-Layland K, Pandit A (2015) Modulation of inflammation and angiogenesis and changes in ECM GAG-activity via dual delivery of nucleic acids. Biomaterials 69:133–147

    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 34:9201–9209

    Article  Google Scholar 

  • Buehrer G, Balzer A, Arnold I, Beier JP, Koerner C, Bleiziffer O, Brandl A, Weis C, Horch RE, Kneser U, Arkudas A (2015) Combination of BMP2 and MSCs significantly increases bone formation in the rat arterio-venous loop model. Tissue Eng Part A 21:96–105

    Article  Google Scholar 

  • Butler MJ, Sefton MV (2012) Cotransplantation of adipose-derived mesenchymal stromal cells and endothelial cells drives vascularization in SCID/bg mice. Tissue Eng Part A 18:1628–1641

    Article  Google Scholar 

  • Cao Y, Mitchell G, Messina A, Price L, Thompson E, Penington A, Morrison W, O’Connor A, Stevens G, Cooper-White JJ (2006) The influence of architecture on degradation and tissue ingrowth into three dimensional Poly(Lactic-co-Glycolic Acid) scaffolds in vitro and in vivo. Biomaterials 27:2854–2864

    Article  Google Scholar 

  • Cassell OC, Morrison WA, Messina A, Penington AJ, Thompson EW, Stevens GW, Perera JM, Kleinman HK, Hurley JV, Romeo R, Knight KR (2001) The influence of extracellular matrix on the generation of vascularized, engineered, transplantable tissue. Ann N Y Acad Sci 944:429–442

    Article  Google Scholar 

  • Chan XY, Black R, Dickerman K, Federico J, Lévesque M, Mumm J, Gerecht S (2015) Three-dimensional vascular network assembly from diabetic patient-derived induced pluripotent stem cells. Arterioscler Thromb Vasc Biol 35:2677–2685

    Article  Google Scholar 

  • Chan EC, Kuo S-M, Kong AM, Morrison WA, Dusting GJ, Mitchell GM, Lim SY, Liu G-S (2016) Three dimensional collagen scaffold promotes intrinsic vascularisation for tissue engineering applications. PLoS One 11:e01497992

    Google Scholar 

  • Chang EI, Bonillas RG, El-ftesi S, Chang EI, Ceradini DJ, Vial IN, Chan DA, Michaels J 5th, Gurtner GC (2009) Tissue engineering using autologous microcirculatory beds as vascularized bioscaffolds. FASEB J 23:906–915

    Article  Google Scholar 

  • Chaturvedi RR, Stevens KR, Solorzano RD, Schwartz RE, Eyckmans J, Baranski JD, Stapleton SC, Bhatia SN, Chen CS (2015) Patterning vascular networks in vivo for tissue engineering applications. Tissue Eng Part C 21:509–517

    Article  Google Scholar 

  • Chen X, Aledia AS, Ghajar CM, Griffith CK, Putman AJ, Hughes CCW, George SC (2009) Prevascularization of a fibrin based tissue construct accelerates the formation of functional anastomoses with host vasculature. Tissue Eng Part A 15:1363–1371

    Article  Google Scholar 

  • Chen X, Aledia AS, Popson MS, Him L, Hughes CCW, 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 16:585–594

    Article  Google Scholar 

  • Chew GL, Huang D, Lin SJ, Huo C, Blick T, Henderson MA, Hill P, Cawson J, Morrison WA, Campbell IG, Hopper JL, Southey MC, Haviv I, Thompson EW (2012) High and low mammographic density human breast tissues maintain histological differential in murine tissue engineering chambers. Breast Cancer Res Treat 135:177–187

    Article  Google Scholar 

  • Chiu LL, Montgomery M, Liang Y, Liu H, Radisic M (2012) Perfusable branching microvessel bed for vascularization of engineered tissues. Proc Natl Acad Sci U S A 109:E3414–E3423

    Article  Google Scholar 

  • Choi YS, Matsuda K, Dusting GJ, Morrison WA, Dilley RJ (2010) Engineering cardiac tissue in vivo from human adipose-derived stem cells. Biomaterials 31:2236–2242

    Article  Google Scholar 

  • Converse JM, Smahel J, Ballantyne DL Jr, Harper AD (1975) Inosculation of vessels of skin graft and host bed: a fortuitous encounter. Br J Plast Surg 28:274–282

    Article  Google Scholar 

  • Cronin KJ, Messina A, Knight KR, Cooper-White JJ, Stevens GW, Penington AJ, Morrison WA (2004) New murine model of spontaneous autologous tissue engineering, combining an arteriovenous pedicle with matrix materials. Plastic Reconstr Surg 113:260–269

    Article  Google Scholar 

  • Czekanska EM, Ralphs JR, Alini M, Stoddart MJ (2014) Enhancing inflammatory and chemotactic signals to regulate bone regeneration. Eur Cell Mater 28:320–334

    Article  Google Scholar 

  • Darland DC, D’Amore PA (1999) Blood vessel maturation: vascular development comes of age. J Clin Invest 103:157–158

    Article  Google Scholar 

  • Del Gaudio C, Baiguera S, Boieri M, Mazzanti B, Ribatti D, Bianco A, Macchiarini P (2013) Induction of angiogenesis using VEGF releasing genipin-crosslinked electrospun gelatin mats. Biomaterials 34:7754–7765

    Article  Google Scholar 

  • Dolderer JH, Abberton KM, Thompson EW, Slavin JL, Stevens GW, Penington AJ, Morrison WA (2007) Spontaneous large volume adipose tissue generation from a vascularized pedicled fat flap inside a chamber space. Tissue Eng 13:673–681

    Article  Google Scholar 

  • Dolderer JH, Thompson EW, Slavin J, Trost N, Cooper-White JJ, Cao Y, O’Connor AJ, Penington A, Morrison WA, Abberton KM (2011) Long-term stability of adipose tissue generated from a vascularized pedicled fat flap inside a chamber. Plast Reconstr Surg 127:2283–2292

    Article  Google Scholar 

  • Elçin YM, Dixit V, Gitnick G (1996) Controlled release of endothelial cell growth factor from chitosan-albumin microspheres for localized angiogenesis: in vitro and in vivo studies. Artif Cells Blood Substit Immobil Biotechnol 24:257–271

    Article  Google Scholar 

  • Erol OO, Spira M (1980) New capillary bed formation with a surgically constructed arteriovenous fistula. Plast Reconstr Surg 66:109–115

    Article  Google Scholar 

  • Ferreira LS, Gerecht S, Shieh HF, Watson N, Rupnick MA, Dallabrida SM, Vunjak-Novakovic G, Langer R (2007) Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res 101:286–294

    Article  Google Scholar 

  • Findlay MW, Messina A, Thompson EW, Morrison WA (2009) Long-term persistence of tissue-engineered adipose flaps in a murine model to 1 year: an update. Plast Reconstr Surg 124:1077–1084

    Article  Google Scholar 

  • Findlay MW, Dolderer JH, Trost N, Craft RO, Cao Y, Cooper-White J, Stevens G, Morrison WA (2011) Tissue-engineered breast reconstruction: bridging the gap toward large-volume tissue engineering in humans. Plast Reconstr Surg 128:1206–1215

    Article  Google Scholar 

  • Folkman J, Hochberg M (1973) Self-regulation of growth in three dimensions. J Exp Med 138:745–753

    Article  Google Scholar 

  • Forster NA, Penington AJ, Hardikar AA, Palmer JA, Hussey A, Tai J, Morrison WA, Feeney SJ (2011) A prevascularized tissue engineering chamber supports growth and function of islets and progenitor cells in diabetic mice. Islets 3:271–283

    Article  Google Scholar 

  • Freiman A, Shandalov Y, Rozenfeld D, Shor E, Segal S, Ben-David D, Meretzki S, Egozi D, Levenberg S (2016) Adipose-derived endothelial and mesenchymal stem cells enhance vascular network formation on three-dimensional constructs in vitro. Stem Cell Res Ther 7:5

    Article  Google Scholar 

  • Glaser DE, Gower RM, Lauer NE, Tam K, Blancas AA, Shih AJ, Simon SI, McCloskey KE (2011) Functional characterization of embryonic stem cell-derived endothelial cells. J Vasc Res 48:415–428

    Article  Google Scholar 

  • Go DP, Palmer JA, Mitchell GM, Gras SL, O’Connor AJ (2015) Porous PLGA microspheres tailored for dual delivery of biomolecules via layer-by-layer assembly. J Biomed Mater Res A 103:1849–1863

    Article  Google Scholar 

  • Goerke SM, Obermeyer J, Plaha J, Stark GB, Finkenzeller G (2015) Endothelial progenitor cells from peripoheral blood support bone regeneration by provoking an angiogenic response. Microvasc Res 98:40–47

    Article  Google Scholar 

  • Guo L, Pribaz JJ (2009) Clinical flap prefabrication. Plast Reconstr Surg 124(6 Suppl):e340–350

    Google Scholar 

  • He S, Xia T, Wang H, Wei L, Luo X, Li X (2012) Multiple release of polyplexes of plasmids VEGF and bFGF from electrospun fibrous scaffolds towards regeneration of mature blood vessels. Acta Biomater 8:2659–2669

    Article  Google Scholar 

  • Hegen A, Blois A, Tiron CE, Hellesøy M, Micklem DR, Nör JE, Akslen LA, Lorens JB (2011) Efficient in vivo vascularization of tissue-engineering scaffolds. J Tissue Eng Regen Med 5:e52–e62

    Article  Google Scholar 

  • Hemmrich K, Thomas GP, Abberton KM, Thompson EW, Rophael JA, Penington AJ, Morrison WA (2007) Monocyte chemoattractant protein-1 and nitric oxide promote adipogenesis in a model that mimics obesity. Obesity 15:2951–2957

    Article  Google Scholar 

  • Hernández D, Millard R, Sivakumaran P, Wong RC, Crombie DE, Hewitt AW, Liang H, Hung SS, Pébay A, Shepherd RK, Dusting GJ, Lim SY (2016) Electrical stimulation promotes cardiac differentiation of human induced pluripotent stem cells. Stem Cells Int 2016:1718041

    Google Scholar 

  • Hofer SO, Knight KM, Cooper-White JJ, O’Connor AJ, Perera JM, Romeo-Meeuw R, Penington AJ, Knight KR, Morrison WA, Messina A (2003) Increasing the volume of vascularized tissue formation in engineered constructs: an experimental study in rats. Plast Reconstr Surg 111:1186–1192

    Article  Google Scholar 

  • Hofer SO, Mitchell GM, Penington AJ, Morrison WA, RomeoMeeuw R, Keramidaris E, Palmer J, Knight KR (2005) The use of pimonidazole to characterise hypoxia in the internal environment of an in vivo tissue engineering chamber. Br J Plast Surg 58:1104–1114

    Article  Google Scholar 

  • Hori Y, Tamai S, Okuda H, Sakamoto H, Takita T, Masuhara K (1979) Blood vessel transplantation to bone. J Hand Surg 4:23–33

    Article  Google Scholar 

  • Hsiao ST, Asgari A, Lokmic Z, Sinclair R, Dusting GJ, Lim SY, Dilley RJ (2012) Comparative analysis of paracrine factor expression in MSCs from bone marrow, adipose, and dermal tissue. Stem Cells Dev 21:2189–2203

    Article  Google Scholar 

  • Hu X, Yu SP, Fraser JL, Lu Z, Ogle ME, Wang JA, Wei L (2008) Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg 135:799–808

    Google Scholar 

  • Hung SSC, van Bergen N, Jackson S, Liang H, Hewitt AW, Hernández D, Lim SY, Trounce I, Pébay A, Wong RCB (2016) Study of mitochondrial respiratory defects on reprogramming to human induced pluripotent stem cells. Aging 8:945–957

    Article  Google Scholar 

  • Hussey AJ, Winardi M, Han XL, Thomas GP, Penington AJ, Morrison WA, Knight KR, Feeney SJ (2009) Seeding of pancreatic islets into prevascularized tissue engineering chambers. Tissue Eng Part A 15:3823–3833

    Article  Google Scholar 

  • Hussey AJ, Winardi M, Wilson J, Forster N, Morrison WA, Penington AJ, Knight KR, Feeney SJ (2010) Pancreatic islet transplantation using vascularised chambers containing nerve growth factor ameliorates hyperglycaemia in diabetic mice. Cells Tissues Organs 191:382–393

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Johannesson B, Sagi I, Gore A, Paull D, Yamada M, Golan-Lev T, Li Z, LeDuc C, Shen Y, Stern S, Xu N, Ma H, Kang E, Mitalipov S, Sauer MV, Zhang K, Benvenisty N, Egli D (2014) Comparable frequencies of coding mutations and loss of imprinting in human pluripotent cells derived by nuclear transfer and defined factors. Cell Stem Cell 15:634–642

    Article  Google Scholar 

  • Kelly JL, Findlay MW, Knight KR, Penington A, Thompson EW, Messina A, Morrison WA (2006) Contact with existing adipose tissue is inductive for adipogenesis in matrigel. Tissue Eng 12:2041–2047

    Article  Google Scholar 

  • Khouri RK, Upton J, Shaw WW (1992) Principles of flap prefabrication. Clin Plast Surg 19:763–771

    Google Scholar 

  • Khouri RK, Hong SP, Deune EG, Tarpley JE, Song SZ, Serdar CM, Pierce GF (1994) De novo generation of permanent neovascularized soft tissue appendages by platelet-derived growth factor. J Clin Invest 94:1757–1763

    Article  Google Scholar 

  • Kim PH, Yim HG, Choi YJ, Kang BJ, Kim J, Kwon SM, Kim BS, Hwang NS, Cho JY (2014) Injectable multifunctional microgel encapsulating outgrowth endothelial cells and growth factors for enhanced neovascularization. J Control Release 187:1–13

    Article  Google Scholar 

  • Koike N, Fukumura D, Gralla O, Au P, Schechner JS, Jain RK (2004) Tissue engineering: creation of long-lasting blood vessels. Nature 428:138–139

    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 110:12601–12606

    Article  Google Scholar 

  • Lai HJ, Kuan CH, Wu HC, Tsai JC, Chen TM, Hsieh DJ, Wang TW (2014) Tailored design of electrospun composite nanofibers with staged release of multiple angiogenic growth factors for chronic wound healing. Acta Biomater 10:4156–4166

    Google Scholar 

  • Laschke MW, Vollmar B, Menger MD (2009) Inosculation: connecting the life-sustaining pipelines. Tissue Eng Part B 15:455–465

    Article  Google Scholar 

  • Lee S, Valmikinathan CM, Byun J, Kim S, Lee G, Mokarram N, Pai SB, Um E, Bellamkonda RV, Yoon YS (2015) Enhanced therapeutic neovascularization by CD31-expressing cells and embryonic stem cell-derived endothelial cells engineered with chitosan hydrogel containing VEGF-releasing microtubes. Biomaterials 63:158–167

    Article  Google Scholar 

  • Lepore DA, Thomas GP, Knight KR, Hussey AJ, Callahan T, Wagner J, Morrison WA, Thomas PQ (2007) Survival and differentiation of pituitary colony-forming cells in vivo. Stem Cells 25:1730–1736

    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 32:7856–7869

    Article  Google Scholar 

  • Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, Marini R, van Blitterswijk CA, Mulligan RC, D’Amore PA, Langer R (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23:879–884

    Article  Google Scholar 

  • Li W, Lan Y, Guo R, Zhang Y, Xue W, Zhang Y (2015) In vitro and in vivo evaluation of a novel collagen/cellulose nanocrystals scaffold for achieving the sustained release of basic fibroblast growth factor. J Biomater Appl 29:882–893

    Article  Google Scholar 

  • Lilja HE, Morrison WA, Han XL, Palmer J, Taylor C, Tee R, Möller A, Thompson EW, Abberton KM (2013) An adipoinductive role of inflammation in adipose tissue engineering: key factors in the early development of engineered soft tissues. Stem Cells Dev 22:1602–1613

    Article  Google Scholar 

  • Lim SY, Hsiao ST, Lokmic Z, Sivakumaran P, Dusting GJ, Dilley RJ (2012) Ischemic preconditioning enhanced in vivo intrinsic vascularisation for tissue engineering. Tissue Eng Part A 18:2210–2219

    Article  Google Scholar 

  • Lim SY, Sivakumaran P, Crombie DE, Dusting GJ, Pébay A, Dilley RJ (2013) Trichostatin A enhances differentiation of human induced pluripotent stem cells to cardiogenic cells for cardiac tissue engineering. Stem Cells Transl Med 2:715–725

    Article  Google Scholar 

  • Lokmic Z, Stillaert F, Morrison WA, Thompson EW, Mitchell GM (2007) An arterio-venous loop in a protected space generates a permanent, highly vascular, tissue engineered construct. FASEB J 21:511–522

    Google Scholar 

  • Lokmic Z, Mitchell GM (2008) Engineering the microcirculation. Tissue Eng 14B:87–103

    Article  Google Scholar 

  • Lokmic ZJ, Thomas JL, Morrison WA, Thompson EW, Mitchell GM (2008) An endogenously deposited fibrin scaffold determines construct size in the surgically created arterio-venous loop chamber model of tissue engineering. J Vasc Surg 48:974–985

    Article  Google Scholar 

  • Lokmic Z, Mitchell GM, Chong NKW, Bastiaanse J, Gerrand Y-W, Zeng Y, Williams ED, Penington AJ (2014) Isolation of human lymphatic malformation endothelial cells, their in vitro characterization and in vivo survival in a mouse xenograft model. Angiogenesis 17:1–15

    Article  Google Scholar 

  • Lu F, Zhan W, Chang Q, Li X (2014) The impact of angiogenic and adipogenic microenvironment on adipose tissue regeneration in tissue engineering chamber. Zhoughua Zheng Xing Wai Ke Za Zhi 30:442–447

    Google Scholar 

  • Macdonald ML, Samuel RE, Shah NJ, Padera RF, Beben YM, Hammond PT (2011) Tissue integration of growth factor-eluting layer-by-layer polyelectrolyte multilayer coated implants. Biomaterials 32:1446–1453

    Article  Google Scholar 

  • Matsuda K, Falkenberg KJ, Woods AA, Choi YS, Morrison WA, Dilley RJ (2013) Adipose-derived stem cells promote angiogenesis and tissue formation for in vivo tissue engineering. Tissue Eng Part A 19:1327–1335

    Article  Google Scholar 

  • Matsui M, Tabata Y (2012) Enhanced angiogenesis by multiple release of platelet-rich plasma contents and basic fibroblast growth factor from gelatin hydrogels. Acta Biomater 8:1792–1801

    Article  Google Scholar 

  • Mazzitelli D, Nöbauer C, Rankin JS, Vogt M, Lange R, Schreiber C (2015) Complete aortic valve cusp replacement in the pediatric population using tissue-engineered bovine pericardium. Ann Thorac Surg 100:1923–1925

    Article  Google Scholar 

  • Mehrabani M, Najafi M, Kamarul T, Mansouri K, Iranpour M, Nematollahi MH, Ghazi-Khansari M, Sharifi AM (2015) Deferoxamine preconditioning to restore impaired HIF-1α-mediated angiogenic mechanisms in adipose-derived stem cells from STZ-induced type 1 diabetic rats. Cell Prolif 48(5):532–549

    Article  Google Scholar 

  • Messina A, Bortolotto SK, Cassell OC, Abberton KM, Morrison WA (2005) Generation of a vascularized organoid using skeletal muscle as the inductive source. FASEB J 19:1570–1572

    Google Scholar 

  • Mian R, 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 6:595–603

    Article  Google Scholar 

  • 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 11:768–774

    Article  Google Scholar 

  • Mirabella T, Cheng D, Longshamp A, Ozaki CK, Chen C (2015) Patterned vascular networks rescue limb ischemia via Dll4/Notch1-mediated anastomoses. Presented at the tissue engineering and regenerative medicine international society meeting Sept 2015, Boston and Abstract published in Tissue Eng Part A, 21 (S1):S23

    Google Scholar 

  • Morrison WA, Dvir E, Doi K, Hurley JV, Hickey MJ, O’Brien BM (1990) Prefabrication of thin transferable axial-pattern skin flaps: an experimental study in rabbits. Br J Plast Surg 43:645–654

    Article  Google Scholar 

  • Morrison WA, Penington AJ, Kumpta SK, Callan P (1997) Clinical applications and technical limitations of prefabricated flaps. Plast Reconstr Surg 99:378–385

    Article  Google Scholar 

  • Morrison WA, Marre D, Grinsell D, Batty A, Trost N, O’Connor AJ (2016) Creation of a large adipose tissue construct in humans using a tissue-engineering chamber: a step forward in the clinical application of soft tissue engineering. EBioMedicine 6:238–245

    Article  Google Scholar 

  • Morritt AN, Bortolotto SK, Dilley RJ, Han X, Kompa AR, McCombe D, Wright CE, Itescu S, Angus JA, Morrison WA (2007) Cardiac tissue engineering in an in vivo vascularized chamber. Circulation 115:353–360

    Article  Google Scholar 

  • Nair A, Thevenot P, Dey J, Shen J, Sun MW, Yang J, Tang L (2010) Novel polymeric scaffolds using protein microbubbles as porogen and growth factor carriers. Tissue Eng Part C 16:23–32

    Article  Google Scholar 

  • Newman AC, Nakatsu M, Chou W, Gershon PD, Hughes CC (2011) Fibroblasts in angiogenesis: fibroblast-derived matrix proteins are essential for endothelial cell lumen formation. Mol Biol Cell 22:3791–3800

    Article  Google Scholar 

  • O’Connor AJ, Morrison WA (2012) Tissue engineering, Chapter 19. In: Gurtner GC, Neligan PC (eds) Plastic surgery principles, vol 1. Elsevier Health Sciences, Atlanta, Georgia, USA. pp 367–396

    Google Scholar 

  • O’Ceallaigh S, Herrick SE, Bluff JE, McGrouther DA, Ferguson MW (2006) Quantification of total and perfused blood vessels in murine skin autografts using a fluorescent double-labeling technique. PRS 117:140–151

    Google Scholar 

  • Oliviero O, Ventre M, Netti PA (2012) Functional porous hydrogels to study angiogenesis under the effect of controlled release of vascular endothelial growth factor. Acta Biomater 8:3294–3301

    Article  Google Scholar 

  • Orlova VV, Drabsch Y, Freund C, Petrus-Reurer S, van den Hil FE, Muenthaisong S, Dijke PT, Mummery CL (2014) Functionality of endothelial cells and pericytes from human pluripotent stem cells demonstrated in cultured vascular plexus and zebrafish xenografts. Arterioscler Thromb Vasc Biol 34:177–186

    Article  Google Scholar 

  • Paige KT, Vacanti CA (1995) Engineering new tissue: formation of neo-cartilage. Tissue Eng 1:97–106

    Article  Google Scholar 

  • Park KD, Kwon IK, Kim YH (2000) Tissue engineering of urinary organs. Yonsei Med J 41:780–788

    Article  Google Scholar 

  • Pasha Z, Wang Y, Sheikh R, Zhang D, Zhao T, Ashraf M (2008) Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc Res 77:134–142

    Article  Google Scholar 

  • Patsch C, Challet-Meylan L, Thoma EC, Urich E, Heckel T, O’Sullivan JF, Grainger SJ, Kapp FG, Sun L, Christensen K, Xia Y, Florido MH, He W, Pan W, Prummer M, Warren CR, Jakob-Roetne R, Certa U, Jagasia R, Freskgård PO, Adatto I, Kling D, Huang P, Zon LI, Chaikof EL, Gerszten RE, Graf M, Iacone R, Cowan CA (2015) Generation of vascular endothelial and smooth muscle cells from human pluripotent stem cells. Nat Cell Biol 17:994–1003

    Article  Google Scholar 

  • Pedersen TO, Blois AL, Xue Y, Xing Z, Sun Y, Finne-Wistrand A, Lorens JB, Fristad I, Leknes KN, Mustafa K (2014) Mesenchymal stem cells induce endothelial cell quiescence and promote capillary formation. Stem Cell Res Ther 5:23

    Article  Google Scholar 

  • Peters MC, Isenberg BC, Rowley JA, Mooney DJ (1998) Release from alginate enhances the biological activity of vascular endothelial growth factor. J Biomater Sci Polym Ed 9:1267–1278

    Article  Google Scholar 

  • Piao Y, Hung SS, Lim SY, Wong RC, Ko MS (2014) Efficient generation of integration-free human induced pluripotent stem cells from keratinocytes by simple transfection of episomal vectors. Stem Cells Transl Med 3:787–791

    Article  Google Scholar 

  • Polykandriotis E, Arkudas A, Beier JP, Hess A, Greil P, Papadopoulos T, Kopp J, Bach AD, Horch RE, Kneser U (2007) Intrinsic axial vascularization of an osteoconductive bone matrix by means of an arteriovenous vascular bundle. Plast Reconstr Surg 120:855–868

    Article  Google Scholar 

  • Potapova IA, Gaudette GR, Brink P, Robinson RB, Rosen MR, Cohen IS, Doronin SV (2007) Mesenchymal stem cells support migration, ECM invasion, proliferation, and survival of endothelial cells in vitro. Stem Cells 25:1761–1768

    Article  Google Scholar 

  • Pribaz JJ, Fine N, Orgill DP (1999a) Flap prefabrication in the head and neck: a 10-year experience. Plast Reconstr Surg 103:808–820

    Article  Google Scholar 

  • Pribaz JJ, Weiss DD, Mulliken JB, Erikson E (1999b) Prelaminated free flaps reconstruction of complex central facial defects. Plast Reconstr Surg 104:357–365

    Article  Google Scholar 

  • Raya-Rivera A, Esquiliano DR, Yoo JJ, Lopez-Bayghen E, Soker S, Atala A (2011) Tissue-engineered autologous urethras for patients who need reconstruction: an observational study. Lancet 377:1175–1182

    Article  Google Scholar 

  • Richardson TP, Peters MC, Ennett AB, Mooney DJ (2001) Polymeric system for dual growth factor delivery. Nat Biotechnol 19:1029–1034

    Article  Google Scholar 

  • Riemenschneider S, Mattia D, Wendel J, Ye L, Zhang P., Tranquillo R (2015) Perfusion of implanted pre-formed microvascular heart patches. Presented at the tissue engineering and regenerative medicine international society meeting Sept 2015, Boston and Abstract published in Tissue Eng Part A 21:(S1):S22

    Google Scholar 

  • Robinson ST, Douglas AM, Chadid T, Kuo K, Rajabalan A, Li H, Copland IB, Barker TH, Galipeau J, Brewster LP (2016) A novel platelet lysate hydrogel for endothelial cell and mesenchymal stem cell-directed neovascularization. Acta Biomater 36:86–98

    Article  Google Scholar 

  • Rophael JA, Craft RO, Palmer JA, Thomas GPL, Hussey AJ, Morrison WA, Penington AJ, Mitchell GM (2007) Angiogenic growth factor synergism in a murine tissue-engineering model of angiogenesis and adipogenesis. Am J Pathol 171:2048–2057

    Article  Google Scholar 

  • Saharinen P, Alitalo K (2011) The yin, the yang, and the angiopoietin-1. J Clin Invest 121:2157–2159

    Article  Google Scholar 

  • Samuel R, Daheron L, Liao S, Vardam T, Kamoun WS, Batista A, Buecker C, Schäfer R, Han X, Au P, Scadden DT, Duda DG, Fukumura D, Jain RK (2013) Generation of functionally competent and durable engineered blood vessels from human induced PS Cells. Proc Natl Acad Sci U S A 110:12774–12779

    Article  Google Scholar 

  • Seach N, Mattesich M, Abberton K, Matsuda K, Tilkorn DJ, Rophael J, Boyd RL, Morrison WA (2010) Vascularized tissue engineering mouse chamber model supports thymopoiesis of ectopic thymus tissue grafts. Tissue Eng Part C 16:543–551

    Article  Google Scholar 

  • Sekine H, Shimizu T, Sakaguchi K, Dobashi I, Wada M, Yamato M, Kobayashi E, Umezu M, Okano T (2013) In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels. Nat Commun 4:1399

    Article  Google Scholar 

  • Shandalov Y, Egozi D, Koffler J, Dado-Rosenfeld D, Ben-Shimol D, Freiman A, Shor E, Kabala A, Levenberg S (2014) An engineered muscle flap for reconstruction of large soft tissue defects. Proc Natl Acad Sci U S A 111:6010–6015

    Article  Google Scholar 

  • Shevchenko R, James SL, James SE (2010) A review of tissue-engineered skin bioconstructs available for skin reconstruction. J R Soc Interface 7:229–258

    Article  Google Scholar 

  • Simcock JW, Penington AJ, Morrison WA, Thompson EW, Mitchell GM (2009) Endothelial precursor cells home to a vascularised tissue engineering chamber by application of the angiogenic chemokine CXCL12. Tissue Eng Part A 15:655–664

    Article  Google Scholar 

  • Solomon S, Pitossi F, Rao MS (2015) Banking on iPSC-is it doable and is it worthwhile. Stem Cell Rev Rep 11:1–10

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Sriram G, Tan JY, Islam I, Rufaihah AJ, Cao T (2015) Efficient differentiation of human embryonic stem cells to arterial and venous endothelial cells under feeder- and serum-free conditions. Stem Cell Res Ther 6:261 doi: 10.1186/s13287-015-0260-5

    Google Scholar 

  • Subbiah R, Hwang MP, Van SY, Do SH, Park H, Lee K, Kim SH, Yun K, Park K (2015) Osteogenic/angiogenic dual growth factor delivery microcapsules for regeneration of vascularized bone tissue. Adv Healthc Mater 4:1982–1992

    Article  Google Scholar 

  • Tabata Y, Miyao M, Ozeki M, Ikada Y (2000) Controlled release of vascular endothelial growth factor by use of collagen hydrogels. J Biomater Sci Polym Ed 11:915–930

    Article  Google Scholar 

  • Takato T, Komuro Y, Yonehara H, Zuker RM (1993) Prefabricated venous flaps: an experimental study in rabbits. Br J Plast Surg 46:122–126

    Article  Google Scholar 

  • Takazawa K, Adachi N, Deie M, Kamei G, Uchio Y, Iwasa J, Kumahashi N, Tadenuma T, Kuwata S, Yasuda K, Tohyama H, Minami A, Muneta T, Takahashi S, Ochi M (2012) Evaluation of magnetic resonance imaging and clinical outcome after tissue-engineered cartilage implants: prospective 6-year follow-up study. J Orthop Sci 17:413–424

    Article  Google Scholar 

  • Takebe T, Sekine K, Enomura M, Koike H, Kimura M, Ogaeri T, Zhang RR, Ueno Y, Zheng YW, Koike N, Aoyama S, Adachi Y, Taniguchi H (2013) Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499:481–484

    Article  Google Scholar 

  • Tanaka Y, Tsutsumi A, Crowe DM, Tajima S, Morrison WA (2000) Generation of an autologous tissue (matrix) flap by combining an arteriovenous shunt loop with artificial skin in rats: preliminary report. Br J Plast Surg 53:51–57

    Article  Google Scholar 

  • Tanaka Y, Sung KC, Tsutsumi A, Ohba S, Ueda K, Morrison WA (2003) Tissue engineering skin flaps: which vascular carrier, arteriovenous shunt loop or arteriovenous bundle, has more potential for angiogenesis and tissue generation? Plast Reconstr Surg 112:1636–1644

    Article  Google Scholar 

  • Tanaka Y, Sung KC, Fumimoto M, Tsutsumi A, Kondo S, Hinohara Y, Morrison WA (2006) Prefabricated engineered skin flap using an arteriovenous vascular bundle as a vascular carrier in rabbits. Plast Reconstr Surg 117:1860–1875

    Article  Google Scholar 

  • Taylor CJ, Church JE, Williams MD, Gerrand Y-W, Keramidaris E, Palmer JA, Galea LA, Penington AJ, Morrison WA, Mitchell GM (2016) Hypoxic preconditioning of myoblasts implanted in a tissue engineering chamber significantly increases local angiogenesis via upregulation of myoblast VEGF-A expression, and downregulation of miRNA-1, miRNA-206 and Angiopoietin 1. J Tissue Eng Regen Med. 2017 May 6. doi: 10.1002/term.2440. [Epub ahead of print]

    Google Scholar 

  • Tee R, Morrison WA, Dusting GJ, Liu GS, Choi YS, Hsiao ST, Dilley RJ (2012) Transplantation of engineered cardiac muscle flaps in syngeneic rats. Tissue Eng Part A 18:1992–1999

    Article  Google Scholar 

  • Thomas GP, Hemmrich K, Abberton KM, McCombe D, Penington AJ, Thompson EW, Morrison WA (2007) Zymosan-induced inflammation stimulates neo-adipogenesis. Int J Obes 32:239–248

    Article  Google Scholar 

  • Tilkorn D, Bedogni A, Keramidaris E, Han X, Palmer J, Dingle AM, Cowling BS, Williams MD, Mc Kay SM, Pepe L, Deftereos A, Morrison WA, Penington A, Mitchell GM (2010) Implantedmyoblast survival is dependent on the degree of vascularization in a novel delayed implantation/prevascularization tissue engineering model. Tissue Eng Part A 16:165–178

    Article  Google Scholar 

  • Tilkorn DJ, Davies EM, Keramidaris E, Dingle AM, Gerrand Y-W, Taylor CJ, Han XL, Palmer JA, Penington AJ, Mitchell CA, Morrison WA, Dusting GJ, Mitchell GM (2012) In vitro myoblast preconditioning enhances subsequent survival post in vivo implantation into a tissue engineering chamber. Biomaterials 33:3868–3879

    Article  Google Scholar 

  • Ting ACH, Craft RO, Palmer JA, Gerrand Y-W, Penington AJ, Morrison WA, Mitchell GM (2014) The adipogenic potential of various extracellular matrices under the influence of an angiogenic growth factor combination in a mouse tissue engineering chamber. Acta Biomater 10:1907–1918

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • van Hinsbergh VW, Collen A, Koolwijk P (2001) Role of fibrin matrix in angiogenesis. Ann N Y Acad Sci 936:426–437

    Article  Google Scholar 

  • Vashi AV, Abberton KM, Thomas GP, Morrison WA, O’Connor AJ, Cooper-White JJ, Thompson EW (2006) Adipose tissue engineering based on the controlled release of fibroblast growth factor-2 in a collagen matrix. Tissue Eng 12:3035–3043

    Article  Google Scholar 

  • Vashi AV, Keramidaris E, Abberton KM, Morrison WA, Wilson JL, O’Connor AJ, Cooper-White JJ, Thompson EW (2008) Adipose differentiation of bone marrow-derived mesenchymal stem cells using Pluronic F-127 hydrogel in vitro. Biomaterials 29:573–579

    Article  Google Scholar 

  • Walton RL, Beahm EK, Wu L (2004) De novo adipose formation in a vascularized engineered construct. Microsurgery 24:378–384

    Article  Google Scholar 

  • Wang K, Chen X, Pan Y, Cui Y, Zhou X, Kong D, Zhao Q (2015) Enhanced vascularization in hybrid PCL/gelatin fibrous scaffolds with sustained release of VEGF. Biomed Res Int 2015:865076

    Google Scholar 

  • Wanjare M, Kuo F, Gerecht S (2013) Derivation and maturation of synthetic and contractile vascular smooth muscle cells from human pluripotent stem cells. Cardiovasc Res 97:321–330

    Article  Google Scholar 

  • Wanjare M, Kusuma S, Gerecht S (2014) Defining differences among perivascular cells derived from human pluripotent stem cells. Stem Cell Rep 2:561–575

    Article  Google Scholar 

  • Yamahara K, Harada K, Ohshima M, Ishikane S, Ohnishi S, Tsuda H, Otani K, Taguchi A, Soma T, Ogawa H, Katsuragi S, Yoshimatsu J, Harada-Shiba M, Kangawa K, Ikeda T. (2014) Comparison of angiogenic, cytoprotective, and immunosuppressive properties of human amnion- and chorion-derived mesenchymal stem cells. PLoS One 14; 9(2):e88319.

    Google Scholar 

  • Yap KK, Dingle AM, Palmer JA, Dhillon R, Lokmic Z, Penington AJ, Yeoh GC, Morrison WA, Mitchell GM (2013) Enhanced liver progenitor cell survival and differentiation in vivo by spheroid implantation in a vascularized tissue engineering chamber. Biomaterials 34:3992–4001

    Article  Google Scholar 

  • Zachman AL, Crowder SW, Ortiz O, Zienkiewicz KJ, Bronikowski CM, Yu SS, Giorgio TD, Guelcher SA, Kohn J, Sung HJ (2013) Pro-angiogenic and anti-inflammatory regulation by functional peptides loaded in polymeric implants for soft tissue regeneration. Tissue Eng Part A 19:437–447

    Google Scholar 

  • Zanotelli MR, Ardalani H, Zhang J, Hou Z, Nguyen EH, Swanson S, Nguyen BK, Bolin J, Elwell A, Bischel LL, Xie AW, Stewart R, Beebe DJ, Thomson JA, Schwartz MP, Murphy WL (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 

  • Zdolsek JM, Morrison WA, Dingle AM, Penington AJ, Mitchell GM (2011) An “off the shelf” vascular allograft supports angiogenic growth in three dimensional tissue engineering. J Vasc Surg 53:435–444

    Article  Google Scholar 

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

    Google Scholar 

  • Zhang Q, Hubenak J, Iyyanki T, Alred E, Turza KC, Davis G, Chang EI, Branch-Brooks CD, Beahm EK, Butler CE (2015a) Engineering vascularized soft tissue flaps in an animal model using human adipose-derived stem cells and VEGF+PLGA/PEG microspheres on a collagen-chitosan scaffold with a flow-through vascular pedicle. Biomaterials 73:198–213

    Article  Google Scholar 

  • Zhang Y, Sivakumaran P, Newcomb AE, Hernandez D, Harris N, Khanabdali R, Liu GS, Kelly DJ, Pébay A, Hewitt AW, Boyle A, Harvey R, Morrison WA, Elliott DA, Dusting GJ, Lim SY (2015b) Cardiac repair with a novel population of mesenchymal stem cells resident in the human heart. Stem Cells 33:3100–3113

    Google Scholar 

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Acknowledgments

The authors acknowledge funding from the National Health & Medical Research Council of Australia, funding from the Australian Catholic University/O’Brien Institute Tissue Engineering Centre, the Stafford Fox Foundation Australia; the Jack Brockhoff Foundation, Australia; the Research Endowment Fund, St.Vincent’s Hospital, Melbourne, Australia; and the Victorian State Government’s Department of Innovation, Industry and Regional Development’s Operational Infrastructure Support Program.

We also acknowledge the assistance of Dr. Anne Kong, Dr. Shiang Lim, and Dr. Kiryu Yap (O’Brien Institute Department of St Vincent’s Institute, Melbourne, Australia); Dr. Guei-Sheung Liu (Centre for Eye Research Australia); Dr. Zerina Lokmic (University of Melbourne, Department of Paediatrics and Nursing, Melbourne, Australia); and Prof Shyh-Ming Kuo (Department of Biomedical Engineering, I-Shou University, Kaohsiung, Taiwan).

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Authors and Affiliations

  1. O’Brien Institute Department, St Vincent’s Institute of Medical Research, 42 Fitzroy Street, Fitzroy, 3065, VIC, Australia

    Geraldine M. Mitchell & Wayne A. Morrison

  2. Department of Surgery, St Vincent’s Hospital, University of Melbourne, Fitzroy, VIC, Australia

    Geraldine M. Mitchell & Wayne A. Morrison

  3. Health Sciences Faculty, Australian Catholic University, Fitzroy, VIC, Australia

    Geraldine M. Mitchell & Wayne A. Morrison

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  1. Geraldine M. Mitchell
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Correspondence to Geraldine M. Mitchell .

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Editors and Affiliations

  1. AUVA Research Center, Ludwig Boltzmann Inst. Exp. a. Clinical AUVA Research Center, Wien, Holy See (Vatican City State)

    Wolfgang Holnthoner

  2. Department of Biomedicine, University Hospital Basel Department of Biomedicine, Basel, Switzerland

    Andrea Banfi

  3. Institute for Pathology, Johannes Gutenberg University Institute for Pathology, Mainz, Germany

    James Kirkpatrick

  4. LBI für experimentelle und klinisch , Wien, Austria

    Heinz Redl

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Mitchell, G.M., Morrison, W.A. (2017). In Vitro and In Vivo Approaches for Pre-vascularization of 3-Dimensional Engineered Tissues. 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_13-1

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