Dynamic culture yields engineered myocardium with near-adult functional output

Biomaterials - Tập 111 - Trang 66-79 - 2016
Christopher P. Jackman1, Aaron L. Carlson1, Nenad Bursac1
1Department of Biomedical Engineering, Duke University, Durham, NC, United States

Tài liệu tham khảo

Tiburcy, 2011, Terminal differentiation, advanced organotypic maturation, and modeling of hypertrophic growth in engineered heart tissue, Circ. Res., 109, 1105, 10.1161/CIRCRESAHA.111.251843 Liau, 2012, Functional cardiac tissue engineering, Regen. Med., 7, 187, 10.2217/rme.11.122 Hirt, 2015, Deciphering the microrna signature of pathological cardiac hypertrophy by engineered heart tissue- and sequencing-technology, J. Mol. Cell. Cardiol., 81, 1, 10.1016/j.yjmcc.2015.01.008 Wang, 2014, Modeling the mitochondrial cardiomyopathy of barth syndrome with ipsc and heart-on-chip technologies, Nat. Med., 20, 616, 10.1038/nm.3545 Thompson, 2011, Mechanical coupling between myofibroblasts and cardiomyocytes slows electric conduction in fibrotic cell monolayers, Circulation, 123, 10.1161/CIRCULATIONAHA.110.015057 Eder, 2014, Effects of proarrhythmic drugs on relaxation time and beating pattern in rat engineered heart tissue, Basic Res. Cardiol., 109, 1, 10.1007/s00395-014-0436-7 Mathur, 2015, Human ipsc-based cardiac microphysiological system for drug screening applications, Sci. Rep., 5, 8883, 10.1038/srep08883 Eschenhagen, 2012, Physiological aspects of cardiac tissue engineering, Am. J. Physiol. Heart Circ. Physiol., 303, H133, 10.1152/ajpheart.00007.2012 Jackman, 2015, Human cardiac tissue engineering: from pluripotent stem cells to heart repair, Curr. Opin. Chem. Eng., 7, 57, 10.1016/j.coche.2014.11.004 Hirt, 2014, Cardiac tissue engineering: state of the art, Circ. Res., 114, 354, 10.1161/CIRCRESAHA.114.300522 Yang, 2014, Engineering adolescence: maturation of human pluripotent stem cell–derived cardiomyocytes, Circ. Res., 114, 511, 10.1161/CIRCRESAHA.114.300558 Hsieh, 2006, Endothelial-cardiomyocyte interactions in cardiac development and repair, Annu. Rev. Physiol., 68, 51, 10.1146/annurev.physiol.68.040104.124629 Sekine, 2014, Oxygen consumption of human heart cells in monolayer culture, Biochem. Biophys. Res. Commun., 452, 834, 10.1016/j.bbrc.2014.09.018 Kagawa, 2015, Direct measurement of local dissolved oxygen concentration spatial profiles in a cell culture environment, Biotechnol. Bioeng., 112, 1263, 10.1002/bit.25531 Vollert, 2014, In vitro perfusion of engineered heart tissue through endothelialized channels, Tissue Eng. Part A, 20, 854 Radisic, 2004, Medium perfusion enables engineering of compact and contractile cardiac tissue, Am. J. Phys. Heart Circ. Physiol., 286, H507, 10.1152/ajpheart.00171.2003 Dvir, 2007, Activation of the erk1/2 cascade via pulsatile interstitial fluid flow promotes cardiac tissue assembly, Tissue Eng., 13, 2185, 10.1089/ten.2006.0364 Carrier, 1999, Cardiac tissue engineering: cell seeding, cultivation parameters, and tissue construct characterization, Biotechnol. Bioeng., 64, 580, 10.1002/(SICI)1097-0290(19990905)64:5<580::AID-BIT8>3.0.CO;2-X Bursac, 1999, Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies, Am. J. Physiol. Heart Circ. Physiol., 277, H433, 10.1152/ajpheart.1999.277.2.H433 Papadaki, 2001, Tissue engineering of functional cardiac muscle: molecular, structural, and electrophysiological studies, Am. J. Physiol. Heart Circ. Physiol., 280, H168, 10.1152/ajpheart.2001.280.1.H168 Vunjak-Novakovic, 2009, Challenges in cardiac tissue engineering, Tissue Eng. Part B Rev., 16, 169, 10.1089/ten.teb.2009.0352 Nunes, 2013, Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes, Nat. Methods, 10, 781, 10.1038/nmeth.2524 Zhang, 2013, Tissue-engineered cardiac patch for advanced functional maturation of human esc-derived cardiomyocytes, Biomaterials, 34, 5813, 10.1016/j.biomaterials.2013.04.026 Godier-Furnémont, 2015, Physiologic force-frequency response in engineered heart muscle by electromechanical stimulation, Biomaterials, 60, 82, 10.1016/j.biomaterials.2015.03.055 Tulloch, 2011, Growth of engineered human myocardium with mechanical loading and vascular coculture, Circ. Res., 109, 47, 10.1161/CIRCRESAHA.110.237206 Bian, 2009, Mesoscopic hydrogel molding to control the 3d geometry of bioartificial muscle tissues, Nat. Protoc., 4, 1522, 10.1038/nprot.2009.155 Naito, 2006, Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle, Circulation, 114, 10.1161/CIRCULATIONAHA.105.001560 Juhas, 2014, Roles of adherent myogenic cells and dynamic culture in engineered muscle function and maintenance of satellite cells, Biomaterials, 35, 9438, 10.1016/j.biomaterials.2014.07.035 Lian, 2012, Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical wnt signaling, Proc. Natl. Acad. Sci. U. S. A., 109, 1848, 10.1073/pnas.1200250109 Tohyama, 2013, Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes, Cell Stem Cell., 12, 127, 10.1016/j.stem.2012.09.013 Burridge, 2014, Chemically defined generation of human cardiomyocytes, Nat. Meth., 11, 855, 10.1038/nmeth.2999 McSpadden, 2009, Electrotonic loading of anisotropic cardiac monolayers by unexcitable cells depends on connexin type and expression level, Am. J. Pysiol. Cell Physiol., 297, C339, 10.1152/ajpcell.00024.2009 Bian, 2014, Controlling the structural and functional anisotropy of engineered cardiac tissues, Biofabrication, 6, 024109, 10.1088/1758-5082/6/2/024109 Madden, 2015, Bioengineered human myobundles mimic clinical responses of skeletal muscle to drugs, eLife, 4, e04885, 10.7554/eLife.04885 Liau, 2011, Pluripotent stem cell-derived cardiac tissue patch with advanced structure and function, Biomaterials, 32, 9180, 10.1016/j.biomaterials.2011.08.050 Schödel, 2009, Hif-prolyl hydroxylases in the rat kidney : physiologic expression patterns and regulation in acute kidney injury, Am. J. Pathol., 174, 1663, 10.2353/ajpath.2009.080687 Appelhoff, 2004, Differential function of the prolyl hydroxylases phd1, phd2, and phd3 in the regulation of hypoxia-inducible factor, J. Biol. Chem., 279, 38458, 10.1074/jbc.M406026200 Schäfer, 2001, Beta-adrenoceptor stimulation attenuates the hypertrophic effect of alpha-adrenoceptor stimulation in adult rat ventricular cardiomyocytes, J. Am. Coll. Cardiol., 37, 300, 10.1016/S0735-1097(00)01065-2 Zimmer, 1995, Response of the rat heart to catecholamines and thyroid hormones, Mol. Cell Biochem., 147, 105, 10.1007/BF00944790 Millar, 1994, Neuropeptide y stimulates hypertrophy of adult ventricular cardiomyocytes, Am. J. Physiol., 266, C1271, 10.1152/ajpcell.1994.266.5.C1271 Bolter, 1988, Maximum heart rate responses to exercise and isoproterenol in the trained rat. American Journal of Physiology - Regulatory, Integr. Comp. Physiol., 254, R834, 10.1152/ajpregu.1988.254.5.R834 Howell, 2011, Mtor couples cellular nutrient sensing to organismal metabolic homeostasis, Trends Endocrinol. Metab., 22, 94, 10.1016/j.tem.2010.12.003 Kim D-H, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, et al. Mtor interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell.110:163–175. Salameh, 2010, Cyclic mechanical stretch induces cardiomyocyte orientation and polarization of the gap junction protein connexin43, Circ. Res., 106, 1592, 10.1161/CIRCRESAHA.109.214429 Kudoh, 1998, Mechanical stretch induces hypertrophic responses in cardiac myocytes of angiotensin ii type 1a receptor knockout mice, J. Biol. Chem., 273, 24037, 10.1074/jbc.273.37.24037 Dvir, 2007, Activation of the erk1/2 cascade via pulsatile interstitial fluid flow promotes cardiac tissue assembly, Tissue Eng., 13, 2185, 10.1089/ten.2006.0364 Thompson, 2011, Mechanical coupling between myofibroblasts and cardiomyocytes slows electric conduction in fibrotic cell monolayers, Circulation, 123, 2083, 10.1161/CIRCULATIONAHA.110.015057 Hirt, 2012, Increased afterload induces pathological cardiac hypertrophy: a new in vitro model, Basic Res. Cardiol., 107, 1, 10.1007/s00395-012-0307-z Saadane, 1999, Expression of immediate early genes, gata-4, and nkx-2.5 in adrenergic-induced cardiac hypertrophy and during regression in adult mice, Br. J. Pharmacol., 127, 1165, 10.1038/sj.bjp.0702676 Kensah, 2013, Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue in vitro, Eur. Heart J., 34, 1134, 10.1093/eurheartj/ehs349 Thavandiran, 2013, Design and formulation of functional pluripotent stem cell-derived cardiac microtissues, Proc. Natl. Acad. Sci., 110, E4698, 10.1073/pnas.1311120110 Schaaf, 2011, Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology, PLoS ONE, 6, e26397, 10.1371/journal.pone.0026397 Turnbull, 2014, Advancing functional engineered cardiac tissues toward a preclinical model of human myocardium. FASEB journal, Off. Publ. Fed. Am. Soc. Exp. Biol., 28, 644 Black, 2009, Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification, Tissue Eng. Part A, 15, 3099, 10.1089/ten.tea.2008.0502 Boudou, 2012, A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues, Tissue Eng. Part A, 18, 910, 10.1089/ten.tea.2011.0341 Sondergaard, 2012, Contractile and electrophysiologic characterization of optimized self-organizing engineered heart tissue, Ann. Thorac. Surg., 94, 1241, 10.1016/j.athoracsur.2012.04.098 Layland, 1999, Positive force- and [ca2+]i-frequency relationships in rat ventricular trabeculae at physiological frequencies, Am. J. Physiol. Heart Circ. Physiol., 276, H9, 10.1152/ajpheart.1999.276.1.H9 Hiranandani, 2006, Frequency-dependent contractile response of isolated cardiac trabeculae under hypo-, normo-, and hyperthermic conditions, J. Appl. Physiol., 100, 1727, 10.1152/japplphysiol.01244.2005 Raman, 2006, Effect of muscle dimensions on trabecular contractile performance under physiological conditions, Pflug. Arch. Eur. J. Physiol., 451, 625, 10.1007/s00424-005-1500-9 Bartel, 1996, Protein phosphorylation in isolated trabeculae from nonfailing and failing human hearts, Mol. Cell Biochem., 157, 171, 10.1007/BF00227896 Cheng, 2008, Insulin-like growth factor-i and slow, bi-directional perfusion enhance the formation of tissue-engineered cardiac grafts, Tissue Eng. Part A, 15, 645, 10.1089/ten.tea.2008.0077 Brown, 2008, Pulsatile perfusion bioreactor for cardiac tissue engineering, Biotechnol. Prog., 24, 907, 10.1002/btpr.11 Sun, 1993, Sympathetic innervation modulates ventricular impulse propagation and repolarization in the immature rat-heart, Cardiovasc. Res., 27, 459, 10.1093/cvr/27.3.459 Nygren, 2003, Voltage-sensitive dye mapping in langendorff-perfused rat hearts, Am. J. Physiol. Heart Circ. Physiol., 284, H892, 10.1152/ajpheart.00648.2002 Zimmermann, 2006, Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts, Nat. Med., 12, 452, 10.1038/nm1394 Spach, 2001, Changes in anisotropic conduction caused by remodeling cell size and the cellular distribution of gap junctions and na(+) channels, J. Electrocardiol., 34, 69, 10.1054/jelc.2001.28833 Guyette, 2016, Bioengineering human myocardium on native extracellular matrix, Circ. Res., 118, 56, 10.1161/CIRCRESAHA.115.306874 Solaro, 1988, Effects of acidosis on ventricular muscle from adult and neonatal rats, Circ. Res., 63, 779, 10.1161/01.RES.63.4.779 Hasenfuss, 1991, Energetics of isometric force development in control and volume- overload human myocardium. Comparison with animal species, Circ. Res., 68, 836, 10.1161/01.RES.68.3.836 Sciarretta, 2014, Mammalian target of rapamycin signaling in cardiac physiology and disease, Circ. Res., 114, 549, 10.1161/CIRCRESAHA.114.302022 Kemi, 2008, Activation or inactivation of cardiac akt/mtor signaling diverges physiological from pathological hypertrophy, J. Cell. Physiol., 214, 316, 10.1002/jcp.21197 Laplante, 2013, Regulation of mtorc1 and its impact on gene expression at a glance, J. Cell Sci., 126, 1713, 10.1242/jcs.125773 Yokogami, 2000, Serine phosphorylation and maximal activation of stat3 during cntf signaling is mediated by the rapamycin target mtor, Curr. Biol., 10, 47, 10.1016/S0960-9822(99)00268-7 Alessi, 1996, Mechanism of activation of protein kinase b by insulin and igf-1, EMBO J., 15, 6541, 10.1002/j.1460-2075.1996.tb01045.x Zheng, 2006, Insulin-like growth factor-1 (igf-1) induces the activation/phosphorylation of akt kinase and camp response element-binding protein (creb) by activating different signaling pathways in pc12 cells, BMC Neurosci., 7, 1, 10.1186/1471-2202-7-51 Maillet, 2013, Molecular basis of physiological heart growth: fundamental concepts and new players, Nat. Rev. Mol. Cell Biol., 14, 38, 10.1038/nrm3495 McMullen, 2007, Differences between pathological and physiological cardiac hypertrophy: novel therapeutic strategies to treat heart failure, Clin. Exp. Pharmacol. Physiol., 34, 255, 10.1111/j.1440-1681.2007.04585.x Dibble, 2009, Characterization of rictor phosphorylation sites reveals direct regulation of mtor complex 2 by s6k1, Mol. Cell. Biol., 29, 5657, 10.1128/MCB.00735-09 Harrington, 2005, Restraining pi3k: mtor signalling goes back to the membrane, Trends Biochem. Sci., 30, 35, 10.1016/j.tibs.2004.11.003 Manning, 2004, Balancing akt with s6k: implications for both metabolic diseases and tumorigenesis, J. Cell Biol., 167, 399, 10.1083/jcb.200408161 Rodrik-Outmezguine, 2011, Mtor kinase inhibition causes feedback-dependent biphasic regulation of akt signaling, Cancer Discov., 1, 248, 10.1158/2159-8290.CD-11-0085 Aksamitiene, 2012, Kholodenko Boris N. Cross-talk between mitogenic ras/mapk and survival pi3k/akt pathways: a fine balance, Biochem. Soc. Trans., 40, 139, 10.1042/BST20110609 Rosner, 2010, Mtor phosphorylated at s2448 binds to raptor and rictor, Amino Acids, 38, 223, 10.1007/s00726-008-0230-7 Sarbassov, 2005, Phosphorylation and regulation of akt/pkb by the rictor-mtor complex, Science, 307, 1098, 10.1126/science.1106148 Laplante, 2012, Mtor signaling in growth control and disease, Cell, 149, 274, 10.1016/j.cell.2012.03.017 Bracho-Valdés, 2011, Mtorc1- and mtorc2-interacting proteins keep their multifunctional partners focused, IUBMB Life, 63, 896, 10.1002/iub.558 Anversa, 1980, Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. I. Hypertrophy, hyperplasia, and binucleation of myocytes, Circ. Res., 46, 495, 10.1161/01.RES.46.4.495 Laflamme, 2011, Heart regeneration, Nature, 473, 326, 10.1038/nature10147 Lasher, 2012, Electrical stimulation directs engineered cardiac tissue to an age-matched native phenotype, J. tissue Eng., 3 Qin, 1996, Cellular and ionic basis of arrhythmias in postinfarction remodeled ventricular myocardium, Circ. Res., 79, 461, 10.1161/01.RES.79.3.461 Gerdes, 1996, Myocyte remodeling during the progression to failure in rats with hypertension, Hypertension, 28, 609, 10.1161/01.HYP.28.4.609 Taylor, 2000, A role for focal adhesion kinase in phenylephrine-induced hypertrophy of rat ventricular cardiomyocytes, J. Biol. Chem., 275, 10.1074/jbc.M909099199 Tigchelaar, 2016, Hypertrophy induced kif5b controls mitochondrial localization and function in neonatal rat cardiomyocytes, J. Mol. Cell. Cardiol., 97, 70, 10.1016/j.yjmcc.2016.04.005