Tissue engineering by decellularization and 3D bioprinting

Discarded human donor organs have been shown to provide decellularized extracellular matrix (dECM) scaffolds suitable for organ engineering. The quest for appropriate cell sources to satisfy the need of multiple cells types in order to fully repopulate human organ-derived dECM scaffolds has opened new venues for the use of human pluripotent stem cells (hPSCs) for recellularization. In addition, three-dimensional (3D) bioprinting techniques are advancing towards the fabrication of biomimetic cell-laden biomaterial constructs. Here, we review recent progress in decellularization/recellularization and 3D bioprinting technologies, aiming to fabricate autologous tissue grafts and organs with an impact in regenerative medicine.

[1]  Nathaniel Huebsch,et al.  Three-dimensional filamentous human diseased cardiac tissue model. , 2014, Biomaterials.

[2]  Shinya Yamanaka,et al.  Pluripotency and nuclear reprogramming , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  Soichiro Kitamura,et al.  Cell removal with supercritical carbon dioxide for acellular artificial tissue , 2008 .

[4]  Sandeep Kumar Vishwakarma,et al.  Repopulation of decellularized whole organ scaffold using stem cells: an emerging technology for the development of neo-organ , 2014, Journal of Artificial Organs.

[5]  Xi Ren,et al.  Perfusion decellularization of human and porcine lungs: bringing the matrix to clinical scale. , 2014, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[6]  Hiroshi Yagi,et al.  Human-Scale Whole-Organ Bioengineering for Liver Transplantation: A Regenerative Medicine Approach , 2013, Cell transplantation.

[7]  Daniel J. Weiss,et al.  Three-dimensional scaffolds of acellular human and porcine lungs for high throughput studies of lung disease and regeneration. , 2014, Biomaterials.

[8]  Kyung-Mee Park,et al.  Biocompatibility evaluation of tissue-engineered decellularized scaffolds for biomedical application. , 2016, Materials science & engineering. C, Materials for biological applications.

[9]  Rashid Bashir,et al.  Three-dimensional photopatterning of hydrogels using stereolithography for long-term cell encapsulation. , 2010, Lab on a chip.

[10]  R. Hynes,et al.  Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. , 1993, Development.

[11]  Juergen A. Knoblich,et al.  Organogenesis in a dish: Modeling development and disease using organoid technologies , 2014, Science.

[12]  Christian Schuetz,et al.  Regeneration and orthotopic transplantation of a bioartificial lung , 2010, Nature Medicine.

[13]  Shaochen Chen,et al.  Light-assisted direct-write of 3D functional biomaterials. , 2014, Lab on a chip.

[14]  Ali Khademhosseini,et al.  Direct 3D bioprinting of perfusable vascular constructs using a blend bioink. , 2016, Biomaterials.

[15]  S. Takayama,et al.  Rapid generation of multiplexed cell cocultures using acoustic droplet ejection followed by aqueous two-phase exclusion patterning. , 2012, Tissue engineering. Part C, Methods.

[16]  Dong-Woo Cho,et al.  Tailoring mechanical properties of decellularized extracellular matrix bioink by vitamin B2-induced photo-crosslinking. , 2016, Acta biomaterialia.

[17]  Bo Wang,et al.  Dual-Purpose Bioreactors to Monitor Noninvasive Physical and Biochemical Markers of Kidney and Liver Scaffold Recellularization. , 2015, Tissue engineering. Part C, Methods.

[18]  M L Chu,et al.  Nucleotide sequences of complementary deoxyribonucleic acids for the pro alpha 1 chain of human type I procollagen. Statistical evaluation of structures that are conserved during evolution. , 1983, Biochemistry.

[19]  Angela Panoskaltsis-Mortari,et al.  Development of a decellularized lung bioreactor system for bioengineering the lung: the matrix reloaded. , 2010, Tissue engineering. Part A.

[20]  Xiaofeng Cui,et al.  Thermal inkjet printing in tissue engineering and regenerative medicine. , 2012, Recent patents on drug delivery & formulation.

[21]  S. Kimber,et al.  Directed differentiation of human embryonic stem cells toward chondrocytes , 2010, Nature Biotechnology.

[22]  Anthony Atala,et al.  Biomaterials for Integration with 3-D Bioprinting , 2014, Annals of Biomedical Engineering.

[23]  J. C. Belmonte,et al.  Diseases in a dish: modeling human genetic disorders using induced pluripotent cells , 2011, Nature Medicine.

[24]  J. Thomson,et al.  Embryonic stem cell lines derived from human blastocysts. , 1998, Science.

[25]  Anthony Atala,et al.  Renal Bioengineering with Scaffolds Generated from Human Kidneys , 2014, Nephron Experimental Nephrology.

[26]  Joseph Suhan,et al.  Bioprinting of Growth Factors onto Aligned Sub-micron Fibrous Scaffolds for Simultaneous Control of Cell Differentiation and Alignment , 2022 .

[27]  Takayuki Takei,et al.  Base structure consisting of an endothelialized vascular-tree network and hepatocytes for whole liver engineering. , 2013, Journal of bioscience and bioengineering.

[28]  Diane Hu,et al.  Injectable hydrogel scaffold from decellularized human lipoaspirate. , 2011, Acta biomaterialia.

[29]  Shaochen Chen,et al.  Digital micromirror device projection printing system for meniscus tissue engineering. , 2013, Acta biomaterialia.

[30]  Igor Tudorache,et al.  Biological vascularized matrix for bladder tissue engineering: matrix preparation, reseeding technique and short-term implantation in a porcine model. , 2005, The Journal of urology.

[31]  Atsushi Yasuda,et al.  Design and validation of a clinical-scale bioreactor for long-term isolated lung culture , 2015, Biomaterials.

[32]  Anthony Callanan,et al.  Comparison of methods for whole-organ decellularization in tissue engineering of bioartificial organs. , 2013, Tissue engineering. Part B, Reviews.

[33]  Shay Soker,et al.  Human liver bioengineering using a whole liver decellularized bioscaffold. , 2013, Methods in molecular biology.

[34]  Jun Liao,et al.  Functional Heart Valve Scaffolds Obtained by Complete Decellularization of Porcine Aortic Roots in a Novel Differential Pressure Gradient Perfusion System. , 2015, Tissue engineering. Part C, Methods.

[35]  Bin Duan,et al.  Bioprinting of Cardiac Tissues , 2015 .

[36]  J. Folkman,et al.  SELF-REGULATION OF GROWTH IN THREE DIMENSIONS , 1973, The Journal of experimental medicine.

[37]  Kyriacos A Athanasiou,et al.  Developing an Articular Cartilage Decellularization Process Toward Facet Joint Cartilage Replacement , 2010, Neurosurgery.

[38]  L. Griffith,et al.  Bioreactor technologies to support liver function in vitro. , 2014, Advanced drug delivery reviews.

[39]  Isabel Moscoso,et al.  Acellular human heart matrix: A critical step toward whole heart grafts. , 2015, Biomaterials.

[40]  Todd C. McDevitt,et al.  Materials as stem cell regulators. , 2014, Nature materials.

[41]  S. Badylak,et al.  The use of xenogeneic small intestinal submucosa as a biomaterial for Achilles tendon repair in a dog model. , 1995, Journal of biomedical materials research.

[42]  P. Cochat,et al.  Et al , 2008, Archives de pediatrie : organe officiel de la Societe francaise de pediatrie.

[43]  Alan Faulkner-Jones,et al.  Bioprinting of human pluripotent stem cells and their directed differentiation into hepatocyte-like cells for the generation of mini-livers in 3D , 2015, Biofabrication.

[44]  Dong-Woo Cho,et al.  Biofabrication: reappraising the definition of an evolving field , 2016, Biofabrication.

[45]  David M Gamm,et al.  Optic Vesicle‐like Structures Derived from Human Pluripotent Stem Cells Facilitate a Customized Approach to Retinal Disease Treatment , 2011, Stem cells.

[46]  Fabien Guillemot,et al.  In vivo bioprinting for computer- and robotic-assisted medical intervention: preliminary study in mice , 2010, Biofabrication.

[47]  Michael L Boninger,et al.  Mechanisms by which acellular biologic scaffolds promote functional skeletal muscle restoration. , 2016, Biomaterials.

[48]  A C Taylor,et al.  RECONSTITUTION OF COMPLETE ORGANS FROM SINGLE-CELL SUSPENSIONS OF CHICK EMBRYOS IN ADVANCED STAGES OF DIFFERENTIATION. , 1960, Proceedings of the National Academy of Sciences of the United States of America.

[49]  P. Vogt,et al.  Tissue Engineered Skin Substitutes Created by Laser-Assisted Bioprinting Form Skin-Like Structures in the Dorsal Skin Fold Chamber in Mice , 2013, PloS one.

[50]  Wim E Hennink,et al.  25th Anniversary Article: Engineering Hydrogels for Biofabrication , 2013, Advanced materials.

[51]  R. Landers,et al.  Rapid prototyping of scaffolds derived from thermoreversible hydrogels and tailored for applications in tissue engineering. , 2002, Biomaterials.

[52]  Michelle E. Scarritt,et al.  A Review of Cellularization Strategies for Tissue Engineering of Whole Organs , 2015, Front. Bioeng. Biotechnol..

[53]  Paolo De Coppi,et al.  Production and Implantation of Renal Extracellular Matrix Scaffolds From Porcine Kidneys as a Platform for Renal Bioengineering Investigations , 2012, Annals of surgery.

[54]  P. McFetridge,et al.  Preparation of ex vivo-based biomaterials using convective flow decellularization. , 2009, Tissue engineering. Part C, Methods.

[55]  Stephen F Badylak,et al.  A whole-organ regenerative medicine approach for liver replacement. , 2011, Tissue engineering. Part C, Methods.

[56]  K Brendel,et al.  Biosynthesis of basement membrane matrix by isolated rat renal glomeruli. , 1979, Kidney international.

[57]  Harald C Ott,et al.  Organ engineering based on decellularized matrix scaffolds. , 2011, Trends in molecular medicine.

[58]  S. Lopes,et al.  Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis , 2015, Nature.

[59]  John B. Shoven,et al.  I , Edinburgh Medical and Surgical Journal.

[60]  J. Lewis,et al.  3D Bioprinting of Vascularized, Heterogeneous Cell‐Laden Tissue Constructs , 2014, Advanced materials.

[61]  Lucas R. Smith,et al.  Method for decellularizing skeletal muscle without detergents or proteolytic enzymes. , 2011, Tissue engineering. Part C, Methods.

[62]  D. Dhar,et al.  Decellularized human liver as a natural 3D-scaffold for liver bioengineering and transplantation , 2015, Scientific Reports.

[63]  Xi Ren,et al.  Engineering pulmonary vasculature in decellularized rat and human lungs , 2015, Nature Biotechnology.

[64]  Wei Sun,et al.  Effects of dispensing pressure and nozzle diameter on cell survival from solid freeform fabrication-based direct cell writing. , 2008, Tissue engineering. Part A.

[65]  Stephen F Badylak,et al.  Decellularization of tissues and organs. , 2006, Biomaterials.

[66]  Richard S Nowakowski,et al.  Differential effects of acellular embryonic matrices on pluripotent stem cell expansion and neural differentiation. , 2015, Biomaterials.

[67]  M Rojkind,et al.  Connective tissue biomatrix: its isolation and utilization for long- term cultures of normal rat hepatocytes , 1980, The Journal of cell biology.

[68]  Kimberly A. Homan,et al.  Bioprinting of 3D Convoluted Renal Proximal Tubules on Perfusable Chips , 2016, Scientific Reports.

[69]  Sailing He,et al.  Rapid Fabrication of Complex 3D Extracellular Microenvironments by Dynamic Optical Projection Stereolithography , 2012, Advanced materials.

[70]  T. Ichisaka,et al.  Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors , 2007, Cell.

[71]  Jeffrey M Karp,et al.  Engineering Stem Cell Organoids. , 2016, Cell stem cell.

[72]  F. Marga,et al.  Toward engineering functional organ modules by additive manufacturing , 2012, Biofabrication.

[73]  R. Stewart,et al.  Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells , 2007, Science.

[74]  Rocky S Tuan,et al.  Enhancement of tenogenic differentiation of human adipose stem cells by tendon-derived extracellular matrix. , 2013, Biomaterials.

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

[76]  Xi Ren,et al.  Perfusion decellularization of whole organs , 2014, Nature Protocols.

[77]  Micaela Liberti,et al.  Electropermeabilization of Inner and Outer Cell Membranes with Microsecond Pulsed Electric Fields: Quantitative Study with Calcium Ions , 2017, Scientific Reports.

[78]  Lay Poh Tan,et al.  Current Status of Bioinks for Micro-Extrusion-Based 3D Bioprinting , 2016, Molecules.

[79]  L. Liotta,et al.  Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. , 1982, Biochemistry.

[80]  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.

[81]  Jean A. Niles,et al.  Influence of acellular natural lung matrix on murine embryonic stem cell differentiation and tissue formation. , 2010, Tissue engineering. Part A.

[82]  Alexander Huber,et al.  The effects of processing methods upon mechanical and biologic properties of porcine dermal extracellular matrix scaffolds. , 2010, Biomaterials.

[83]  Mark A. Skylar-Scott,et al.  Three-dimensional bioprinting of thick vascularized tissues , 2016, Proceedings of the National Academy of Sciences.

[84]  Mark Turmaine,et al.  Discarded human kidneys as a source of ECM scaffold for kidney regeneration technologies. , 2013, Biomaterials.

[85]  Harald C. Ott,et al.  Recellularization of organs: what is the future for solid organ transplantation? , 2014, Current opinion in organ transplantation.

[86]  Richard Tuli,et al.  Adult mesenchymal stem cells and cell-based tissue engineering , 2002, Arthritis research & therapy.

[87]  Anthony Atala,et al.  3D bioprinting of tissues and organs , 2014, Nature Biotechnology.

[88]  P. Armstrong,et al.  Cell sorting out: the self-assembly of tissues in vitro. , 1989, Critical reviews in biochemistry and molecular biology.

[89]  Tal Dvir,et al.  Electric field stimulation integrated into perfusion bioreactor for cardiac tissue engineering. , 2010, Tissue engineering. Part C, Methods.

[90]  Raymond M. Wang,et al.  Decellularized myocardial matrix hydrogels: In basic research and preclinical studies. , 2016, Advanced drug delivery reviews.

[91]  James J. Yoo,et al.  A 3D bioprinting system to produce human-scale tissue constructs with structural integrity , 2016, Nature Biotechnology.

[92]  R. Samanipour,et al.  A simple and high-resolution stereolithography-based 3D bioprinting system using visible light crosslinkable bioinks , 2015, Biofabrication.

[93]  W. Miller,et al.  Bioreactor design for perfusion-based, highly-vascularized organ regeneration. , 2013, Current opinion in chemical engineering.

[94]  W. Bowen,et al.  Hydrogels derived from demineralized and decellularized bone extracellular matrix , 2013, Acta biomaterialia.

[95]  J. Guyette,et al.  Regeneration and Experimental Orthotopic Transplantation of a Bioengineered Kidney , 2013, Nature Medicine.

[96]  John Parkinson,et al.  Sequences and domain structures of mammalian, avian, amphibian and teleost tropoelastins: Clues to the evolutionary history of elastins. , 2006, Matrix biology : journal of the International Society for Matrix Biology.

[97]  Glenn D Prestwich,et al.  Development of a model bladder extracellular matrix combining disulfide cross-linked hyaluronan with decellularized bladder tissue. , 2006, Macromolecular bioscience.

[98]  Anthony Atala,et al.  Tissue specific synthetic ECM hydrogels for 3-D in vitro maintenance of hepatocyte function. , 2012, Biomaterials.

[99]  Xi Ren,et al.  Enhanced lung epithelial specification of human induced pluripotent stem cells on decellularized lung matrix. , 2014, The Annals of thoracic surgery.

[100]  Jörn Hülsmann,et al.  A novel customizable modular bioreactor system for whole-heart cultivation under controlled 3D biomechanical stimulation , 2013, Journal of Artificial Organs.

[101]  Joris Ivens,et al.  Regen , 2018, The City Symphony Phenomenon.

[102]  Andreu M Climent,et al.  Myocardial commitment from human pluripotent stem cells: Rapid production of human heart grafts. , 2016, Biomaterials.

[103]  C. Mason,et al.  A brief definition of regenerative medicine. , 2008, Regenerative medicine.

[104]  Eric D. Miller,et al.  Engineered spatial patterns of FGF-2 immobilized on fibrin direct cell organization. , 2005, Biomaterials.

[105]  Ericka Stricklin-Parker,et al.  Ann , 2005 .

[106]  Stephen F Badylak,et al.  An overview of tissue and whole organ decellularization processes. , 2011, Biomaterials.

[107]  Ali Khademhosseini,et al.  3D biofabrication strategies for tissue engineering and regenerative medicine. , 2014, Annual review of biomedical engineering.

[108]  Brian Derby,et al.  Printing and Prototyping of Tissues and Scaffolds , 2012, Science.

[109]  C. Schmidt,et al.  Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering. , 2000, Biomaterials.

[110]  Sara Conti,et al.  Recellularization of well-preserved acellular kidney scaffold using embryonic stem cells. , 2014, Tissue engineering. Part A.

[111]  Jean A. Niles,et al.  Production and assessment of decellularized pig and human lung scaffolds. , 2013, Tissue engineering. Part A.

[112]  Ricardo Londono,et al.  Biologic Scaffolds for Regenerative Medicine: Mechanisms of In vivo Remodeling , 2014, Annals of Biomedical Engineering.

[113]  D. Navajas,et al.  Local micromechanical properties of decellularized lung scaffolds measured with atomic force microscopy. , 2013, Acta biomaterialia.

[114]  Deok‐Ho Kim,et al.  Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink , 2014, Nature Communications.

[115]  Marco Rasponi,et al.  Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. , 2016, Biomaterials.

[116]  Christopher A. Carruthers,et al.  A hydrogel derived from decellularized dermal extracellular matrix. , 2012, Biomaterials.

[117]  Hiroshi Yagi,et al.  Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix , 2010, Nature Medicine.

[118]  Kevin A Rocco,et al.  Biomimetic Culture Reactor for Whole-Lung Engineering , 2016, BioResearch open access.

[119]  Krishnendu Roy,et al.  Laser-layered microfabrication of spatially patterned functionalized tissue-engineering scaffolds. , 2005, Journal of biomedical materials research. Part B, Applied biomaterials.

[120]  Korkut Uygun,et al.  Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. , 2011, Annual review of biomedical engineering.

[121]  Ibrahim T. Ozbolat,et al.  Bioprinting towards Physiologically Relevant Tissue Models for Pharmaceutics. , 2016, Trends in biotechnology.

[122]  Marc E. Nelson,et al.  Bioresorbable airway splint created with a three-dimensional printer. , 2013, The New England journal of medicine.

[123]  Alessandro Giacomello,et al.  Cardiac tissue engineering using tissue printing technology and human cardiac progenitor cells. , 2012, Biomaterials.

[124]  David J. Mooney,et al.  Regenerative medicine: Current therapies and future directions , 2015, Proceedings of the National Academy of Sciences.

[125]  Yu-Ting Tsai,et al.  Process development of an acellular dermal matrix (ADM) for biomedical applications. , 2004, Biomaterials.

[126]  J. Lahann,et al.  EMBRYONIC STEM CELLS/INDUCED PLURIPOTENT STEM CELLS Concise Review: The Evolution of Human Pluripotent Stem Cell Culture: From Feeder Cells to Synthetic Coatings , 2012 .

[127]  W. Dhert,et al.  Three-dimensional fiber deposition of cell-laden, viable, patterned constructs for bone tissue printing. , 2008, Tissue engineering. Part A.

[128]  Laura E Niklason,et al.  Bioreactor for the Long-Term Culture of Lung Tissue , 2011, Cell transplantation.

[129]  Lei Yang,et al.  Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells , 2013, Nature Communications.

[130]  Anthony Atala,et al.  A hydrogel bioink toolkit for mimicking native tissue biochemical and mechanical properties in bioprinted tissue constructs. , 2015, Acta biomaterialia.

[131]  Christopher D. Batich,et al.  Mouse stem cells seeded into decellularized rat kidney scaffolds endothelialize and remodel basement membranes , 2012, Organogenesis.

[132]  Eric D. Miller,et al.  Microenvironments Engineered by Inkjet Bioprinting Spatially Direct Adult Stem Cells Toward Muscle‐ and Bone‐Like Subpopulations , 2008, Stem cells.