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      Accordion-Like Honeycombs for Tissue Engineering of Cardiac Anisotropy

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          Abstract

          Tissue engineered grafts may be useful in myocardial repair, however previous scaffolds have been structurally incompatible with recapitulating cardiac anisotropy. Utilizing microfabrication techniques, a novel accordion-like honeycomb microstructure was rendered in poly(glycerol sebacate) to yield porous, elastomeric 3-D scaffolds with controllable stiffness and anisotropy. Accordion-like honeycomb scaffolds with cultured neonatal rat heart cells demonstrated utility via: (1) closely matched mechanical properties compared to native adult rat right ventricular myocardium, with stiffnesses controlled by polymer curing time; (2) heart cell contractility inducible by electric field stimulation with directionally-dependent electrical excitation thresholds (p<0.05); and (3) greater heart cell alignment (p<0.0001) than isotropic control scaffolds. Prototype bilaminar scaffolds with 3-D interconnected pore networks yielded electrically excitable grafts with multi-layered neonatal rat heart cells. Accordion-like honeycombs can thus overcome principal structural-mechanical limitations of previous scaffolds, promoting the formation of grafts with aligned heart cells and mechanical properties more closely resembling native myocardium.

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          Most cited references 53

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          Muscular thin films for building actuators and powering devices.

          We demonstrate the assembly of biohybrid materials from engineered tissues and synthetic polymer thin films. The constructs were built by culturing neonatal rat ventricular cardiomyocytes on polydimethylsiloxane thin films micropatterned with extracellular matrix proteins to promote spatially ordered, two-dimensional myogenesis. The constructs, termed muscular thin films, adopted functional, three-dimensional conformations when released from a thermally sensitive polymer substrate and were designed to perform biomimetic tasks by varying tissue architecture, thin-film shape, and electrical-pacing protocol. These centimeter-scale constructs perform functions as diverse as gripping, pumping, walking, and swimming with fine spatial and temporal control and generating specific forces as high as 4 millinewtons per square millimeter.
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            Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts.

            The concept of regenerating diseased myocardium by implantation of tissue-engineered heart muscle is intriguing, but convincing evidence is lacking that heart tissues can be generated at a size and with contractile properties that would lend considerable support to failing hearts. Here we created large (thickness/diameter, 1-4 mm/15 mm), force-generating engineered heart tissue from neonatal rat heart cells. Engineered heart tissue formed thick cardiac muscle layers when implanted on myocardial infarcts in immune-suppressed rats. When evaluated 28 d later, engineered heart tissue showed undelayed electrical coupling to the native myocardium without evidence of arrhythmia induction. Moreover, engineered heart tissue prevented further dilation, induced systolic wall thickening of infarcted myocardial segments and improved fractional area shortening of infarcted hearts compared to controls (sham operation and noncontractile constructs). Thus, our study provides evidence that large contractile cardiac tissue grafts can be constructed in vitro, can survive after implantation and can support contractile function of infarcted hearts.
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              A tough biodegradable elastomer.

              Biodegradable polymers have significant potential in biotechnology and bioengineering. However, for some applications, they are limited by their inferior mechanical properties and unsatisfactory compatibility with cells and tissues. A strong, biodegradable, and biocompatible elastomer could be useful for fields such as tissue engineering, drug delivery, and in vivo sensing. We designed, synthesized, and characterized a tough biodegradable elastomer from biocompatible monomers. This elastomer forms a covalently crosslinked, three-dimensional network of random coils with hydroxyl groups attached to its backbone. Both crosslinking and the hydrogen-bonding interactions between the hydroxyl groups likely contribute to the unique properties of the elastomer. In vitro and in vivo studies show that the polymer has good biocompatibility. Polymer implants under animal skin are absorbed completely within 60 days with restoration of the implantation sites to their normal architecture.
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                Author and article information

                Journal
                101155473
                30248
                Nat Mater
                Nature materials
                1476-1122
                10 October 2008
                2 November 2008
                December 2008
                1 June 2009
                : 7
                : 12
                : 1003-1010
                Affiliations
                [1 ]Harvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, E25-330, Cambridge, MA 02139, USA
                [2 ]Department of Materials Science and Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, E25-330, Cambridge, MA 02139, USA
                [3 ]Department of Chemical Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, E25-330, Cambridge, MA 02139, USA
                [4 ]Biomedical Engineering Center, Charles Stark Draper Laboratory, 555 Technology Square, Cambridge, MA 02139, USA
                Author notes
                [# ] Correspondence to: Lisa E. Freed, MD, PhD, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Building E25, Room 330, Cambridge, MA 02139, USA, Tel: 617-452-2603, Fax: 617-258-8827, Email: Lfreed@ 123456mit.edu
                Article
                nihpa72112
                10.1038/nmat2316
                2613200
                18978786
                Funding
                Funded by: National Institute of Dental and Craniofacial Research : NIDCR
                Funded by: National Heart, Lung, and Blood Institute : NHLBI
                Award ID: R01 DE013023-09 ||DE
                Funded by: National Institute of Dental and Craniofacial Research : NIDCR
                Funded by: National Heart, Lung, and Blood Institute : NHLBI
                Award ID: R01 DE013023-08 ||DE
                Funded by: National Institute of Dental and Craniofacial Research : NIDCR
                Funded by: National Heart, Lung, and Blood Institute : NHLBI
                Award ID: F32 HL084968-03 ||HL
                Funded by: National Institute of Dental and Craniofacial Research : NIDCR
                Funded by: National Heart, Lung, and Blood Institute : NHLBI
                Award ID: F32 HL084968-02 ||HL
                Funded by: National Institute of Dental and Craniofacial Research : NIDCR
                Funded by: National Heart, Lung, and Blood Institute : NHLBI
                Award ID: F32 HL084968-01 ||HL
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