Towards organ printing: engineering an intra-organ branched vascular tree

Importance of the field: Effective vascularization of thick three-dimensional engineered tissue constructs is a problem in tissue engineering. As in native organs, a tissue-engineered intra-organ vascular tree must be comprised of a network of hierarchically branched vascular segments. Despite this requirement, current tissue-engineering efforts are still focused predominantly on engineering either large-diameter macrovessels or microvascular networks. Areas covered in this review: We present the emerging concept of organ printing or robotic additive biofabrication of an intra-organ branched vascular tree, based on the ability of vascular tissue spheroids to undergo self-assembly. What the reader will gain: The feasibility and challenges of this robotic biofabrication approach to intra-organ vascularization for tissue engineering based on organ-printing technology using self-assembling vascular tissue spheroids including clinically relevantly vascular cell sources are analyzed. Take home message: It is not possible to engineer 3D thick tissue or organ constructs without effective vascularization. An effective intra-organ vascular system cannot be built by the simple connection of large-diameter vessels and microvessels. Successful engineering of functional human organs suitable for surgical implantation will require concomitant engineering of a ‘built in’ intra-organ branched vascular system. Organ printing enables biofabrication of human organ constructs with a ‘built in’ intra-organ branched vascular tree.

[1]  S. Cole,et al.  Sequences Human Induced Pluripotent Stem Cells Free of Vector and Transgene , 2012 .

[2]  F. Zannad,et al.  Extracellular matrix fibrotic markers in heart failure , 2010, Heart Failure Reviews.

[3]  Yan Jin,et al.  Innovative strategies for tissue engineered skin based on multiple growth factors gene transfection. , 2009, Medical hypotheses.

[4]  Kristopher L. Nazor,et al.  Adult mice generated from induced pluripotent stem cells , 2009, Nature.

[5]  D. Butler,et al.  Tensile stimulation of murine stem cell-collagen sponge constructs increases collagen type I gene expression and linear stiffness. , 2009, Tissue engineering. Part A.

[6]  V. Mironov,et al.  Designer ‘blueprint’ for vascular trees: morphology evolution of vascular tissue constructs , 2009 .

[7]  Shuichi Takayama,et al.  Microfluidic system for formation of PC-3 prostate cancer co-culture spheroids. , 2009, Biomaterials.

[8]  V Mironov,et al.  Biofabrication: a 21st century manufacturing paradigm , 2009, Biofabrication.

[9]  R. Stewart,et al.  Human Induced Pluripotent Stem Cells Free of Vector and Transgene Sequences , 2009, Science.

[10]  Ellen M Arruda,et al.  Ultrastructure of myotendinous junctions in tendon-skeletal muscle constructs engineered in vitro. , 2009, Histology and histopathology.

[11]  Marcin Maruszewski,et al.  Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: a multicentre cohort study , 2009, The Lancet.

[12]  Vladimir Mironov,et al.  Emergence of clinical vascular tissue engineering , 2009, The Lancet.

[13]  Vladimir Mironov,et al.  Organ printing: tissue spheroids as building blocks. , 2009, Biomaterials.

[14]  J. Morgan,et al.  Fibroblast elongation and dendritic extensions in constrained versus unconstrained microtissues. , 2009, Cell motility and the cytoskeleton.

[15]  J. Thomson,et al.  Hematopoietic and Endothelial Differentiation of Human Induced Pluripotent Stem Cells , 2009, Stem cells.

[16]  Jeffrey R Morgan,et al.  Controlling cell position in complex heterotypic 3D microtissues by tissue fusion , 2009, Biotechnology and bioengineering.

[17]  N. L'Heureux,et al.  Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery. , 2009, Biomaterials.

[18]  Gideon Rechavi,et al.  Donor-Derived Brain Tumor Following Neural Stem Cell Transplantation in an Ataxia Telangiectasia Patient , 2009, PLoS medicine.

[19]  Vladimir Mironov,et al.  Rapid biofabrication of tubular tissue constructs by centrifugal casting in a decellularized natural scaffold with laser-machined micropores , 2009, Journal of materials science. Materials in medicine.

[20]  Sara Mantero,et al.  Clinical transplantation of a tissue-engineered airway , 2008, The Lancet.

[21]  Katja Schenke-Layland,et al.  Non‐invasive multiphoton imaging of extracellular matrix structures , 2008, Journal of biophotonics.

[22]  Marcin Maruszewski,et al.  Cell-based therapeutics from an economic perspective: primed for a commercial success or a research sinkhole? , 2008, Regenerative medicine.

[23]  Hwan-You Chang,et al.  Recent advances in three‐dimensional multicellular spheroid culture for biomedical research , 2008, Biotechnology journal.

[24]  Hwan-You Chang,et al.  Magnetic reconstruction of three-dimensional tissues from multicellular spheroids. , 2008, Tissue engineering. Part C, Methods.

[25]  W. Landis,et al.  Tissue Engineering Models of Human Digits: Effect of Periosteum on Growth Plate Cartilage Development , 2008, Cells Tissues Organs.

[26]  Jeroen Rouwkema,et al.  Vascularization in tissue engineering. , 2008, Trends in biotechnology.

[27]  D. Letourneur,et al.  Mechanical properties of rat thoracic and abdominal aortas. , 2008, Journal of biomechanics.

[28]  K. Plath,et al.  Reprogrammed Mouse Fibroblasts Differentiate into Cells of the Cardiovascular and Hematopoietic Lineages , 2008, Stem cells.

[29]  L. Niklason,et al.  Small‐diameter human vessel wall engineered from bone marrow‐derived mesenchymal stem cells (hMSCs) , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[30]  Dai Fukumura,et al.  Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. , 2008, Blood.

[31]  Adrian Neagu,et al.  Tissue engineering by self-assembly of cells printed into topologically defined structures. , 2008, Tissue engineering. Part A.

[32]  Geraldine M Mitchell,et al.  Engineering the microcirculation. , 2008, Tissue engineering. Part B, Reviews.

[33]  C. V. van Blitterswijk,et al.  Engineering vascularised tissues in vitro. , 2008, European cells & materials.

[34]  Doris A Taylor,et al.  Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart , 2008, Nature Medicine.

[35]  Vladimir Mironov,et al.  Organ printing: promises and challenges. , 2008, Regenerative medicine.

[36]  A. Hess,et al.  The venous graft as an effector of early angiogenesis in a fibrin matrix. , 2008, Microvascular research.

[37]  Masatoshi Watanabe,et al.  [Biological behavior of prostate cancer cells in 3D culture systems]. , 2008, Yakugaku zasshi : Journal of the Pharmaceutical Society of Japan.

[38]  William E. Higgins,et al.  System for the analysis and visualization of large 3D anatomical trees , 2007, Comput. Biol. Medicine.

[39]  I. Kosztin,et al.  Developmental biology and tissue engineering. , 2007, Birth defects research. Part C, Embryo today : reviews.

[40]  W. Sanger,et al.  Producing primate embryonic stem cells by somatic cell nuclear transfer , 2007, Nature.

[41]  Rei Ogawa,et al.  Vascular tissue engineering and vascularized 3D tissue regeneration. , 2007, Regenerative medicine.

[42]  W. Hennink,et al.  Hydrogels as extracellular matrices for skeletal tissue engineering: state-of-the-art and novel application in organ printing. , 2007, Tissue engineering.

[43]  S. Gerecht,et al.  Vascular Progenitor Cells Isolated From Human Embryonic Stem Cells Give Rise to Endothelial and Smooth Muscle–Like Cells and Form Vascular Networks In Vivo , 2007, Circulation research.

[44]  M. S. Steinberg,et al.  Differential adhesion in morphogenesis: a modern view. , 2007, Current opinion in genetics & development.

[45]  Sergio Garrido,et al.  Technology Insight: the evolution of tissue-engineered vascular grafts—from research to clinical practice , 2007, Nature Clinical Practice Cardiovascular Medicine.

[46]  Jennifer L West,et al.  Poly(ethylene glycol) hydrogels conjugated with a collagenase-sensitive fluorogenic substrate to visualize collagenase activity during three-dimensional cell migration. , 2007, Biomaterials.

[47]  Hessel Wijkstra,et al.  Vascular fluorescence casting and imaging cryomicrotomy for computerized three‐dimensional renal arterial reconstruction , 2007, BJU international.

[48]  Wayne A Morrison,et al.  An arteriovenous loop in a protected space generates a permanent, highly vascular, tissue‐engineered construct , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[49]  Silviu Itescu,et al.  Cardiac Tissue Engineering in an In Vivo Vascularized Chamber , 2007, Circulation.

[50]  Matthew P. Brennan,et al.  Construction of an autologous tissue-engineered venous conduit from bone marrow-derived vascular cells: optimization of cell harvest and seeding techniques. , 2007, Journal of pediatric surgery.

[51]  Jenny Dankelman,et al.  Relation between branching patterns and perfusion in stochastic generated coronary arterial trees , 2007, Medical & Biological Engineering & Computing.

[52]  Robert T Tranquillo,et al.  Cytokine-induced differentiation of multipotent adult progenitor cells into functional smooth muscle cells. , 2006, The Journal of clinical investigation.

[53]  J. H. Kim,et al.  Sphingosylphosphorylcholine induces differentiation of human mesenchymal stem cells into smooth-muscle-like cells through a TGF-β-dependent mechanism , 2006, Journal of Cell Science.

[54]  J. Peter Rubin,et al.  Regulation of α-Smooth Muscle Actin Protein Expression in Adipose-Derived Stem Cells , 2006, Cells Tissues Organs.

[55]  L. Ignarro,et al.  Clonogenic multipotent stem cells in human adipose tissue differentiate into functional smooth muscle cells , 2006, Proceedings of the National Academy of Sciences.

[56]  J. Pérez-Pomares,et al.  Tissue fusion and cell sorting in embryonic development and disease: biomedical implications , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[57]  M. Stojkovic,et al.  Using Therapeutic Cloning to Fight Human Disease: A Conundrum or Reality? , 2006, Stem cells.

[58]  Nicolas P Smith,et al.  Structural morphology of renal vasculature. , 2006, American journal of physiology. Heart and circulatory physiology.

[59]  R. Karch,et al.  Optimized arterial trees supplying hollow organs. , 2006, Medical engineering & physics.

[60]  Vladimir Mironov,et al.  Review: bioprinting: a beginning. , 2006, Tissue engineering.

[61]  James J. Yoo,et al.  Tissue-engineered autologous bladders for patients needing cystoplasty , 2006, The Lancet.

[62]  Masayuki Yamato,et al.  Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[63]  L. Niklason,et al.  Relevance and safety of telomerase for human tissue engineering. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Chrysanthi Williams,et al.  Small-diameter artificial arteries engineered in vitro. , 2005, Circulation research.

[65]  J. Rubin,et al.  Regulation of alpha-smooth muscle actin protein expression in adipose-derived stem cells. , 2006, Cells, tissues, organs.

[66]  Ghassan S. Kassab,et al.  Large-Scale 3-D Geometric Reconstruction of the Porcine Coronary Arterial Vasculature Based on Detailed Anatomical Data , 2005, Annals of Biomedical Engineering.

[67]  Adrian Neagu,et al.  Role of physical mechanisms in biological self-organization. , 2005, Physical review letters.

[68]  N. Stergiopulos,et al.  Biomechanical properties of decellularized porcine common carotid arteries. , 2005, American journal of physiology. Heart and circulatory physiology.

[69]  R. Torensma Blood vessels engineered from human cells , 2005, The Lancet.

[70]  Rebekah Drezek,et al.  Protease-activated quantum dot probes. , 2005, Biochemical and biophysical research communications.

[71]  G. S. Kassab,et al.  A Computer Reconstruction of the Entire Coronary Arterial Tree Based on Detailed Morphometric Data , 2005, Annals of Biomedical Engineering.

[72]  Peter J Hunter,et al.  Anatomically based finite element models of the human pulmonary arterial and venous trees including supernumerary vessels. , 2005, Journal of applied physiology.

[73]  Gerard Pasterkamp,et al.  Endothelialization but Stimulates Intimal Hyperplasia in Porcine Arteriovenous in Vivo Cell Seeding with Anti-cd34 Antibodies Successfully Accelerates in Vivo Cell Seeding with Anti-cd34 Antibodies Successfully Accelerates Endothelialization but Stimulates Intimal Hyperplasia in Porcine Arteriovenou , 2022 .

[74]  J. Rees The Problem with Academic Medicine: Engineering Our Way into and out of the Mess , 2005, PLoS medicine.

[75]  M. S. Steinberg,et al.  The differential adhesion hypothesis: a direct evaluation. , 2005, Developmental biology.

[76]  Sangeeta N Bhatia,et al.  Three-dimensional tissue fabrication. , 2004, Advanced drug delivery reviews.

[77]  V Mironov,et al.  What is regenerative medicine? Emergence of applied stem cell and developmental biology , 2004, Expert opinion on biological therapy.

[78]  Martin Fussenegger,et al.  Microscale tissue engineering using gravity-enforced cell assembly. , 2004, Trends in biotechnology.

[79]  V. Mironov,et al.  Engineering biological structures of prescribed shape using self-assembling multicellular systems. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[80]  Martin Neumann,et al.  Staged Growth of Optimized Arterial Model Trees , 2000, Annals of Biomedical Engineering.

[81]  M. Pera Unnatural selection of cultured human ES cells? , 2004, Nature Biotechnology.

[82]  J. Thomson,et al.  Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells , 2004, Nature Biotechnology.

[83]  P. J. Hunter,et al.  Generation of an Anatomically Based Geometric Coronary Model , 2004, Annals of Biomedical Engineering.

[84]  Adrian Neagu,et al.  Organ printing: fiction or science. , 2004, Biorheology.

[85]  P. Doevendans,et al.  Stem cell‐derived angiogenic/vasculogenic cells: Possible therapies for tissue repair and tissue engineering , 2003, Clinical and experimental pharmacology & physiology.

[86]  Y. Ikada,et al.  First Evidence That Bone Marrow Cells Contribute to the Construction of Tissue-Engineered Vascular Autografts In Vivo , 2003, Circulation.

[87]  Vladimir Mironov,et al.  Organ printing: computer-aided jet-based 3D tissue engineering. , 2003, Trends in biotechnology.

[88]  Simon P Hoerstrup,et al.  A new source for cardiovascular tissue engineering: human bone marrow stromal cells. , 2002, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[89]  Shulamit Levenberg,et al.  Endothelial cells derived from human embryonic stem cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[90]  H. Lorenz,et al.  Multilineage cells from human adipose tissue: implications for cell-based therapies. , 2001, Tissue engineering.

[91]  Jun Yamashita,et al.  Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors , 2000, Nature.

[92]  P. Carmeliet Mechanisms of angiogenesis and arteriogenesis , 2000, Nature Medicine.

[93]  W Schreiner,et al.  Shear stress distribution in arterial tree models, generated by constrained constructive optimization. , 1999, Journal of theoretical biology.

[94]  R Langer,et al.  Functional arteries grown in vitro. , 1999, Science.

[95]  A. Mikos,et al.  Growing new organs. , 1999, Scientific American.

[96]  M. Sefton,et al.  Tissue engineering. , 1998, Journal of cutaneous medicine and surgery.

[97]  F A Auger,et al.  A completely biological tissue‐engineered human blood vessel , 1998, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[98]  G. S. Davis,et al.  Germ-layer surface tensions and "tissue affinities" in Rana pipiens gastrulae: quantitative measurements. , 1997, Developmental biology.

[99]  W. Risau,et al.  Mechanisms of angiogenesis , 1997, Nature.

[100]  Stuart K. Williams,et al.  Use of freshly isolated capillary endothelial cells for the immediate establishment of a monolayer on a vascular graft at surgery. , 1986, Surgery.

[101]  M Zamir,et al.  Optimality principles in arterial branching. , 1976, Journal of theoretical biology.

[102]  T Togawa,et al.  Optimal branching structure of the vascular tree. , 1972, The Bulletin of mathematical biophysics.

[103]  C D Murray,et al.  The Physiological Principle of Minimum Work: I. The Vascular System and the Cost of Blood Volume. , 1926, Proceedings of the National Academy of Sciences of the United States of America.