Micro- and nanotechnology in cardiovascular tissue engineering

While in nature the formation of complex tissues is gradually shaped by the long journey of development, in tissue engineering constructing complex tissues relies heavily on our ability to directly manipulate and control the micro-cellular environment in vitro. Not surprisingly, advancements in both microfabrication and nanofabrication have powered the field of tissue engineering in many aspects. Focusing on cardiac tissue engineering, this paper highlights the applications of fabrication techniques in various aspects of tissue engineering research: (1) cell responses to micro- and nanopatterned topographical cues, (2) cell responses to patterned biochemical cues, (3) controlled 3D scaffolds, (4) patterned tissue vascularization and (5) electromechanical regulation of tissue assembly and function.

[1]  Keith E. Mostov,et al.  Building epithelial architecture: insights from three-dimensional culture models , 2002, Nature Reviews Molecular Cell Biology.

[2]  J. Vacanti,et al.  Microfabrication Technology for Vascularized Tissue Engineering , 2002 .

[3]  B. Russell,et al.  Micromechanical regulation in cardiac myocytes and fibroblasts: implications for tissue remodeling , 2011, Pflügers Archiv - European Journal of Physiology.

[4]  T. Desai,et al.  Fabrication of microtextured membranes for cardiac myocyte attachment and orientation. , 2000, Journal of biomedical materials research.

[5]  Joe Tien,et al.  Fabrication of Collagen Gels That Contain Patterned, Micrometer‐Scale Cavities , 2004 .

[6]  Lisa E. Freed,et al.  Accordion-Like Honeycombs for Tissue Engineering of Cardiac Anisotropy , 2008, Nature materials.

[7]  Seeram Ramakrishna,et al.  Electrospun nanofiber fabrication as synthetic extracellular matrix and its potential for vascular tissue engineering. , 2004, Tissue engineering.

[8]  Takehiko Kitamori,et al.  A micro-spherical heart pump powered by cultured cardiomyocytes. , 2007, Lab on a chip.

[9]  David J. Mooney,et al.  Active scaffolds for on-demand drug and cell delivery , 2010, Proceedings of the National Academy of Sciences.

[10]  R. Langer,et al.  A tough biodegradable elastomer , 2002, Nature Biotechnology.

[11]  Sean P. Palecek,et al.  3-D microwell culture of human embryonic stem cells. , 2006, Biomaterials.

[12]  Joe Tien,et al.  Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. , 2007, Lab on a chip.

[13]  Kevin Kit Parker,et al.  Nanofiber assembly by rotary jet-spinning. , 2010, Nano letters.

[14]  Eugenia Kumacheva,et al.  Generation of human embryonic stem cell‐derived mesoderm and cardiac cells using size‐specified aggregates in an oxygen‐controlled bioreactor , 2009, Biotechnology and bioengineering.

[15]  D J Mooney,et al.  Open pore biodegradable matrices formed with gas foaming. , 1998, Journal of biomedical materials research.

[16]  M. Radisic,et al.  Engineering surfaces for site-specific vascular differentiation of mouse embryonic stem cells. , 2010, Acta biomaterialia.

[17]  David L Kaplan,et al.  It takes a village to grow a tissue , 2005, Nature Biotechnology.

[18]  Justin S. Weinbaum,et al.  Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. , 2009, Tissue engineering. Part A.

[19]  Robin I. M. Dunbar,et al.  Muscular Thin Films for Building Actuators and Powering Devices , 2007 .

[20]  Jason P. Gleghorn,et al.  Microfluidic scaffolds for tissue engineering. , 2007, Nature materials.

[21]  Tal Dvir,et al.  Nanotechnological strategies for engineering complex tissues. , 2020, Nature nanotechnology.

[22]  Milica Radisic,et al.  Biodegradable collagen patch with covalently immobilized VEGF for myocardial repair. , 2011, Biomaterials.

[23]  G. Whitesides,et al.  Soft lithography in biology and biochemistry. , 2001, Annual review of biomedical engineering.

[24]  T. Desai,et al.  Inhibition of fibroblast proliferation in cardiac myocyte cultures by surface microtopography. , 2003, American journal of physiology. Cell physiology.

[25]  Robert Langer,et al.  Endothelialized microvasculature based on a biodegradable elastomer. , 2005, Tissue engineering.

[26]  Gregory Stephanopoulos,et al.  Effects of substratum morphology on cell physiology , 1994, Biotechnology and bioengineering.

[27]  Milica Radisic,et al.  Scaffolds with covalently immobilized VEGF and Angiopoietin-1 for vascularization of engineered tissues. , 2010, Biomaterials.

[28]  Tejal A Desai,et al.  Microfabricated grooves recapitulate neonatal myocyte connexin43 and N-cadherin expression and localization. , 2003, Journal of biomedical materials research. Part A.

[29]  N. Bursac,et al.  A Method to Replicate the Microstructure of Heart Tissue In Vitro Using DTMRI-Based Cell Micropatterning , 2009, Annals of Biomedical Engineering.

[30]  Younan Xia,et al.  Electrospinning of Nanofibers: Reinventing the Wheel? , 2004 .

[31]  Milica Radisic,et al.  Challenges in cardiac tissue engineering. , 2010, Tissue engineering. Part B, Reviews.

[32]  Milica Radisic,et al.  Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Andre Levchenko,et al.  Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs , 2009, Proceedings of the National Academy of Sciences.

[34]  S. Martinoia,et al.  A new integrated system combining atomic force microscopy and micro-electrode array for measuring the mechanical properties of living cardiac myocytes , 2011, Biomedical microdevices.

[35]  Nobuyuki Magome,et al.  Electrospun nanofibers as a tool for architecture control in engineered cardiac tissue. , 2011, Biomaterials.

[36]  Tejal A Desai,et al.  Microtextured substrata alter gene expression, protein localization and the shape of cardiac myocytes. , 2003, Biomaterials.

[37]  Ravi A. Desai,et al.  Mechanical regulation of cell function with geometrically modulated elastomeric substrates , 2010, Nature Methods.

[38]  D. Mooney,et al.  Growth factor delivery-based tissue engineering: general approaches and a review of recent developments , 2011, Journal of The Royal Society Interface.

[39]  S. H. Lee,et al.  Fabrication of nanostructures of polyethylene glycol for applications to protein adsorption and cell adhesion , 2005, Nanotechnology.

[40]  M. Toner,et al.  Stacks of Microfabricated Structures as Scaffolds for Cell Culture and Tissue Engineering , 2000 .

[41]  T. A. Desai,et al.  Micro- and nanoscale structures for tissue engineering constructs. , 2000, Medical engineering & physics.

[42]  Lauran R. Madden,et al.  Proangiogenic scaffolds as functional templates for cardiac tissue engineering , 2010, Proceedings of the National Academy of Sciences.

[43]  A. Khademhosseini,et al.  Microscale technologies for tissue engineering and biology. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Elisa Cimetta,et al.  Production of arrays of cardiac and skeletal muscle myofibers by micropatterning techniques on a soft substrate , 2009, Biomedical microdevices.

[45]  Milica Radisic,et al.  Influence of substrate stiffness on the phenotype of heart cells , 2010, Biotechnology and bioengineering.

[46]  Harold Bien,et al.  Tension Development and Nuclear Eccentricity in Topographically Controlled Cardiac Syncytium , 2003 .

[47]  Sami Alom Ruiz,et al.  Mechanical tugging force regulates the size of cell–cell junctions , 2010, Proceedings of the National Academy of Sciences.

[48]  A K Harris,et al.  Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations. , 1982, Developmental biology.

[49]  Kyongbum Lee,et al.  Vascularization strategies for tissue engineering. , 2009, Tissue engineering. Part B, Reviews.

[50]  A. Ahluwalia,et al.  Fabrication of PLGA scaffolds using soft lithography and microsyringe deposition. , 2003, Biomaterials.

[51]  Jinchao Xu,et al.  Measuring single cardiac myocyte contractile force via moving a magnetic bead. , 2005, Biophysical journal.

[52]  A. Levchenko,et al.  Guided Cell Migration on Microtextured Substrates with Variable Local Density and Anisotropy , 2009, Advanced functional materials.

[53]  Ning Wang,et al.  Directional control of lamellipodia extension by constraining cell shape and orienting cell tractional forces , 2002, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[54]  K. Woodhouse,et al.  Control of Human Embryonic Stem Cell Colony and Aggregate Size Heterogeneity Influences Differentiation Trajectories , 2008, Stem cells.

[55]  Kevin Kit Parker,et al.  Generation of Functional Ventricular Heart Muscle from Mouse Ventricular Progenitor Cells , 2009, Science.

[56]  Nenad Bursac,et al.  Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues , 2009, Nature Protocols.

[57]  Ali Khademhosseini,et al.  Micro- and nanoscale control of the cardiac stem cell niche for tissue fabrication. , 2009, Tissue engineering. Part B, Reviews.

[58]  Hyoungshin Park,et al.  The significance of pore microarchitecture in a multi-layered elastomeric scaffold for contractile cardiac muscle constructs. , 2011, Biomaterials.

[59]  Yu Sun,et al.  A microfabricated platform for high-throughput unconfined compression of micropatterned biomaterial arrays. , 2010, Biomaterials.

[60]  Ashish Kapoor,et al.  Microtopographically patterned surfaces promote the alignment of tenocytes and extracellular collagen. , 2010, Acta biomaterialia.

[61]  Yu Sun,et al.  Microfabricated arrays for high-throughput screening of cellular response to cyclic substrate deformation. , 2010, Lab on a chip.

[62]  Masayuki Yamato,et al.  Mass preparation of size-controlled mouse embryonic stem cell aggregates and induction of cardiac differentiation by cell patterning method. , 2009, Biomaterials.

[63]  Nenad Bursac,et al.  Novel micropatterned cardiac cell cultures with realistic ventricular microstructure. , 2009, Biophysical journal.

[64]  Robert Langer,et al.  Three‐Dimensional Microfluidic Tissue‐Engineering Scaffolds Using a Flexible Biodegradable Polymer , 2006, Advanced materials.

[65]  Milica Radisic,et al.  A photolithographic method to create cellular micropatterns. , 2006, Biomaterials.

[66]  Ali Khademhosseini,et al.  Microfluidic patterning for fabrication of contractile cardiac organoids , 2007, Biomedical microdevices.

[67]  Tejal A Desai,et al.  Contractility-dependent modulation of cell proliferation and adhesion by microscale topographical cues. , 2008, Small.

[68]  Peter Kohl,et al.  Force-length relations in isolated intact cardiomyocytes subjected to dynamic changes in mechanical load. , 2007, American journal of physiology. Heart and circulatory physiology.

[69]  E Bell,et al.  Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[70]  Y Wang,et al.  Biodegradable Microfluidics , 2004 .

[71]  Sukho Park,et al.  Micro pumping with cardiomyocyte-polymer hybrid. , 2007, Lab on a chip.

[72]  W. Zimmermann,et al.  Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. , 2000, Biotechnology and bioengineering.

[73]  Wesley R. Legant,et al.  Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues , 2009, Proceedings of the National Academy of Sciences.

[74]  J. Vacanti,et al.  Silicon micromachining to tissue engineer branched vascular channels for liver fabrication. , 2000, Tissue engineering.

[75]  Ali Khademhosseini,et al.  Microwell-mediated control of embryoid body size regulates embryonic stem cell fate via differential expression of WNT5a and WNT11 , 2009, Proceedings of the National Academy of Sciences.

[76]  Andrew D McCulloch,et al.  Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. , 2008, Biophysical journal.

[77]  Milica Radisic,et al.  Mathematical model of oxygen distribution in engineered cardiac tissue with parallel channel array perfused with culture medium containing oxygen carriers. , 2005, American journal of physiology. Heart and circulatory physiology.

[78]  Viatcheslav Gurev,et al.  Models of cardiac electromechanics based on individual hearts imaging data , 2011, Biomechanics and modeling in mechanobiology.

[79]  Robert Langer,et al.  Engineering systems for the generation of patterned co-cultures for controlling cell-cell interactions. , 2011, Biochimica et biophysica acta.

[80]  Milica Radisic,et al.  Engineered cardiac tissues. , 2011, Current opinion in biotechnology.

[81]  F. Guilak,et al.  Advanced Material Strategies for Tissue Engineering Scaffolds , 2009, Advanced materials.

[82]  Hyoungshin Park,et al.  Combined technologies for microfabricating elastomeric cardiac tissue engineering scaffolds. , 2010, Macromolecular bioscience.

[83]  Helene Andersson,et al.  Microfabrication and microfluidics for tissue engineering: state of the art and future opportunities. , 2004, Lab on a chip.