It's all in the timing: Modeling isovolumic contraction through development and disease with a dynamic dual electromechanical bioreactor system

References

• Morgan KY, Black LD 3rd. Mimicking isovolumic contraction with combined electromechanical stimulation improves the development of engineered cardiac constructs. Tissue Eng Part A 2014; (Forthcoming); PMID:24410342; http://dx.doi.org/10.1089/ten.tea.2013.0355
   PubMedGoogle Scholar
• Zimmermann W-H, Schneiderbanger K, Schubert P, Didié M, Münzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T. Tissue engineering of a differentiated cardiac muscle construct. Circ Res 2002; 90:223-30; PMID:11834716; http://dx.doi.org/10.1161/hh0202.103644
   PubMed Web of Science ®Google Scholar
• Shimko VF, Claycomb WC. Effect of mechanical loading on three-dimensional cultures of embryonic stem cell-derived cardiomyocytes. Tissue Eng Part A 2008; 14:49-58; PMID:18333804; http://dx.doi.org/10.1089/ten.a.2007.0092
   PubMedGoogle Scholar
• Birla RK, Huang YC, Dennis RG. Development of a novel bioreactor for the mechanical loading of tissue-engineered heart muscle. Tissue Eng 2007; 13:2239-48; PMID:17590151; http://dx.doi.org/10.1089/ten.2006.0359
   PubMedGoogle Scholar
• Zhang SJ, Truskey GA, Kraus WE. Effect of cyclic stretch on beta1D-integrin expression and activation of FAK and RhoA. Am J Physiol Cell Physiol 2007; 292:C2057-69; PMID:17267546; http://dx.doi.org/10.1152/ajpcell.00493.2006
   PubMed Web of Science ®Google Scholar
• Akhyari P, Fedak PWM, Weisel RD, Lee TY, Verma S, Mickle DA, Li RK. Mechanical stretch regimen enhances the formation of bioengineered autologous cardiac muscle grafts. Circulation 2002; 106(Suppl 1):I137-42; PMID:12354723
   PubMed Web of Science ®Google Scholar
• Radisic M, Park H, Shing H, Consi T, Schoen FJ, Langer R, Freed LE, Vunjak-Novakovic G. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci U S A 2004; 101:18129-34; PMID:15604141; http://dx.doi.org/10.1073/pnas.0407817101
   PubMed Web of Science ®Google Scholar
• Lasher RA, Pahnke AQ, Johnson JM, Sachse FB, Hitchcock RW. Electrical stimulation directs engineered cardiac tissue to an age-matched native phenotype. J Tissue Eng 2012; 3:2041731412455354; PMID:22919458; http://dx.doi.org/10.1177/2041731412455354
   PubMedGoogle Scholar
• Hsiao C-W, Bai M-Y, Chang Y, Chung M-F, Lee T-Y, Wu C-T, Maiti B, Liao Z-X, Li R-K, Sung H-W. Electrical coupling of isolated cardiomyocyte clusters grown on aligned conductive nanofibrous meshes for their synchronized beating. Biomaterials 2013; 34:1063-72; PMID:23164424; http://dx.doi.org/10.1016/j.biomaterials.2012.10.065
   PubMed Web of Science ®Google Scholar
• Wikswo JP Jr., Lin SF, Abbas RA. Virtual electrodes in cardiac tissue: a common mechanism for anodal and cathodal stimulation. Biophys J 1995; 69:2195-210; PMID:8599628; http://dx.doi.org/10.1016/S0006-3495(95)80115-3
   PubMed Web of Science ®Google Scholar
• Huang C-C, Liao C-K, Yang M-J, Chen C-H, Hwang S-M, Hung Y-W, Chang Y, Sung H-W. A strategy for fabrication of a three-dimensional tissue construct containing uniformly distributed embryoid body-derived cells as a cardiac patch. Biomaterials 2010; 31:6218-27; PMID:20537702; http://dx.doi.org/10.1016/j.biomaterials.2010.04.067
   PubMed Web of Science ®Google Scholar
• Fukuta H, Little WC. The cardiac cycle and the physiologic basis of left ventricular contraction, ejection, relaxation, and filling. Heart Fail Clin 2008; 4:1-11; PMID:18313620; http://dx.doi.org/10.1016/j.hfc.2007.10.004
   PubMedGoogle Scholar
• Weissler AM, Harris WS, Schoenfeld CD. Systolic time intervals in heart failure in man. Circulation 1968; 37:149-59; PMID:5640345; http://dx.doi.org/10.1161/01.CIR.37.2.149
   PubMed Web of Science ®Google Scholar
• Martin CE, Shaver JA, Thompson ME, Reddy PS, Leonard JJ. Direct correlation of external systolic time intervals with internal indices of left ventricular function in man. Circulation 1971; 44:419-31; PMID:5097444; http://dx.doi.org/10.1161/01.CIR.44.3.419
   PubMed Web of Science ®Google Scholar
• Hirschfeld S, Meyer R, Korfhagen J, Kaplan S, Liebman J. The isovolumic contraction time of the left ventricle. An echographic study. Circulation 1976; 54:751-6; PMID:975470; http://dx.doi.org/10.1161/01.CIR.54.5.751
   PubMedGoogle Scholar
• Kensah G, Gruh I, Viering J, Schumann H, Dahlmann J, Meyer H, Skvorc D, Bär A, Akhyari P, Heisterkamp A, et al. A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation. Tissue Eng Part C Methods 2011; 17:463-73; PMID:21142417; http://dx.doi.org/10.1089/ten.tec.2010.0405
   PubMedGoogle Scholar
• Lu L, Mende M, Yang X, Körber H-F, Schnittler HJ, Weinert S, Heubach J, Werner C, Ravens U. Design and validation of a bioreactor for simulating the cardiac niche: a system incorporating cyclic stretch, electrical stimulation, and constant perfusion. Tissue Eng Part A 2013; 19:403-14; PMID:22991978; http://dx.doi.org/10.1089/ten.tea.2012.0135
   PubMed Web of Science ®Google Scholar
• Simmons CS, Petzold BC, Pruitt BL. Microsystems for biomimetic stimulation of cardiac cells. Lab Chip 2012; 12:3235-48; PMID:22782590; http://dx.doi.org/10.1039/c2lc40308k
   PubMedGoogle Scholar
• Wang B, Wang G, To F, Butler JR, Claude A, McLaughlin RM, Williams LN, de Jongh Curry AL, Liao J. Myocardial scaffold-based cardiac tissue engineering: application of coordinated mechanical and electrical stimulations. Langmuir 2013; 29:11109-17; PMID:23923967; http://dx.doi.org/10.1021/la401702w
   PubMedGoogle Scholar
• Calaghan SC, Belus A, White E. Do stretch-induced changes in intracellular calcium modify the electrical activity of cardiac muscle? Prog Biophys Mol Biol 2003; 82:81-95; PMID:12732270; http://dx.doi.org/10.1016/S0079-6107(03)00007-5
   PubMedGoogle Scholar
• Sela G, Landesberg A. The external work-pressure time integral relationships and the afterload dependence of Frank-Starling mechanism. J Mol Cell Cardiol 2009; 47:544-51; PMID:19463830; http://dx.doi.org/10.1016/j.yjmcc.2009.05.007
   PubMedGoogle Scholar
• Iribe G, Helmes M, Kohl P. Force-length relations in isolated intact cardiomyocytes subjected to dynamic changes in mechanical load. Am J Physiol Heart Circ Physiol 2007; 292:H1487-97; PMID:17098830; http://dx.doi.org/10.1152/ajpheart.00909.2006
   PubMedGoogle Scholar
• Allen DG, Kurihara S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol 1982; 327:79-94; PMID:7120151
   PubMed Web of Science ®Google Scholar
• Lab MJ, Allen DG, Orchard CH. The effects of shortening on myoplasmic calcium concentration and on the action potential in mammalian ventricular muscle. Circ Res 1984; 55:825-9; PMID:6499137; http://dx.doi.org/10.1161/01.RES.55.6.825
   PubMedGoogle Scholar
• James RS, Young IS, Cox VM, Goldspink DF, Altringham JD. Isometric and isotonic muscle properties as determinants of work loop power output. Pflugers Arch 1996; 432:767-74; PMID:8772125; http://dx.doi.org/10.1007/s004240050197
   PubMedGoogle Scholar
• Markhasin VS, Solovyova O, Katsnelson LB, Protsenko Y, Kohl P, Noble D. Mechano-electric interactions in heterogeneous myocardium: development of fundamental experimental and theoretical models. Prog Biophys Mol Biol 2003; 82:207-20; PMID:12732280; http://dx.doi.org/10.1016/S0079-6107(03)00017-8
   PubMedGoogle Scholar
• Karabag T, Aydin M, Dogan SM, Sayin MR, Cetiner MA. The influence of circadian variations on echocardiographic parameters in healthy people. Echocardiography 2011; 28:612-8; PMID:21676017; http://dx.doi.org/10.1111/j.1540-8175.2011.01411.x
   PubMedGoogle Scholar
• Tei C, Nishimura RA, Seward JB, Tajik AJ. Noninvasive Doppler-derived myocardial performance index: correlation with simultaneous measurements of cardiac catheterization measurements. J Am Soc Echocardiogr 1997; 10:169-78; PMID:9083973; http://dx.doi.org/10.1016/S0894-7317(97)70090-7
   PubMed Web of Science ®Google Scholar
• Pfeffer MA, Pfeffer JM, Fishbein MC, Fletcher PJ, Spadaro J, Kloner RA, Braunwald E. Myocardial infarct size and ventricular function in rats. Circ Res 1979; 44:503-12; PMID:428047; http://dx.doi.org/10.1161/01.RES.44.4.503
   PubMed Web of Science ®Google Scholar
• Hayward R, Hydock DS. Doxorubicin cardiotoxicity in the rat: an in vivo characterization. J Am Assoc Lab Anim Sci 2007; 46:20-32; PMID:17645292
   PubMed Web of Science ®Google Scholar
• Anderson PAW, Greig A, Mark TM, Malouf NN, Oakeley AE, Ungerleider RM, Allen PD, Kay BK. Molecular basis of human cardiac troponin T isoforms expressed in the developing, adult, and failing heart. Circ Res 1995; 76:681-6; PMID:7534662; http://dx.doi.org/10.1161/01.RES.76.4.681
   PubMed Web of Science ®Google Scholar
• Periasamy M, Huke S. SERCA pump level is a critical determinant of Ca(2+)homeostasis and cardiac contractility. J Mol Cell Cardiol 2001; 33:1053-63; PMID:11444913; http://dx.doi.org/10.1006/jmcc.2001.1366
   PubMed Web of Science ®Google Scholar
• Kim S-J, Abdellatif M, Koul S, Crystal GJ. Chronic treatment with insulin-like growth factor I enhances myocyte contraction by upregulation of Akt-SERCA2a signaling pathway. Am J Physiol Heart Circ Physiol 2008; 295:H130-5; PMID:18456736; http://dx.doi.org/10.1152/ajpheart.00298.2008
   PubMed Web of Science ®Google Scholar
• Chaanine AH, Hajjar RJ. AKT signalling in the failing heart. Eur J Heart Fail 2011; 13:825-9; PMID:21724622; http://dx.doi.org/10.1093/eurjhf/hfr080
   PubMed Web of Science ®Google Scholar
• Tandon N, Marsano A, Maidhof R, Wan L, Park H, Vunjak-Novakovic G. Optimization of electrical stimulation parameters for cardiac tissue engineering. J Tissue Eng Regen Med 2011; 5:e115-25; PMID:21604379; http://dx.doi.org/10.1002/term.377
   PubMedGoogle Scholar
• Black LD 3rd, Meyers JD, Weinbaum JS, Shvelidze YA, Tranquillo RT. Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. Tissue Eng Part A 2009; 15:3099-108; PMID:19338433; http://dx.doi.org/10.1089/ten.tea.2008.0502
   PubMed Web of Science ®Google Scholar
• Stehle R, Iorga B. Kinetics of cardiac sarcomeric processes and rate-limiting steps in contraction and relaxation. J Mol Cell Cardiol 2010; 48:843-50; PMID:20060002; http://dx.doi.org/10.1016/j.yjmcc.2009.12.020
   PubMed Web of Science ®Google Scholar
• Yano M, Ikeda Y, Matsuzaki M. Altered intracellular Ca2+ handling in heart failure. J Clin Invest 2005; 115:556-64; PMID:15765137; http://dx.doi.org/10.1172/JCI24159
   PubMed Web of Science ®Google Scholar
• Pieske B, Houser SR. [Na+]i handling in the failing human heart. Cardiovasc Res 2003; 57:874-86; PMID:12650866; http://dx.doi.org/10.1016/S0008-6363(02)00841-6
   PubMed Web of Science ®Google Scholar
• Pervolaraki E, Anderson RA, Benson AP, Hayes-gill B, Holden AV, Moore BJR, Paley MN, Zhang H. Antenatal architecture and activity of the human heart Antenatal architecture and activity of the human heart. Interface Focus 2013
   Google Scholar
• Sedmera D. Function and form in the developing cardiovascular system. Cardiovasc Res 2011; 91:252-9; PMID:21367775; http://dx.doi.org/10.1093/cvr/cvr062
   PubMedGoogle Scholar
• Hirota A, Kamino K, Komuro H, Sakai T, Yada T. Early events in development of electrical activity and contraction in embryonic rat heart assessed by optical recording. J Physiol 1985; 369:209-27; PMID:4093880
   PubMed Web of Science ®Google Scholar
• Bruch C, Schmermund A, Dagres N, Katz M, Bartel T, Erbel R. Severe aortic valve stenosis with preserved and reduced systolic left ventricular function: diagnostic usefulness of the Tei index. J Am Soc Echocardiogr 2002; 15:869-76; PMID:12221402; http://dx.doi.org/10.1067/mje.2002.120977
   PubMedGoogle Scholar
• Kono M, Kisanuki A, Takasaki K, Nakashiki K, Yuasa T, Kuwahara E, Mizukami N, Uemura T, Kubota K, Ueya N, et al. Left ventricular systolic function is abnormal in diastolic heart failure: re-assessment of systolic function using cardiac time interval analysis. J Cardiol 2009; 53:437-46; PMID:19477388; http://dx.doi.org/10.1016/j.jjcc.2009.02.014
   PubMedGoogle Scholar
• Gaasch WH, Little WC. Assessment of left ventricular diastolic function and recognition of diastolic heart failure. Circulation 2007; 116:591-3; PMID:17679627; http://dx.doi.org/10.1161/CIRCULATIONAHA.107.716647
   PubMed Web of Science ®Google Scholar
• Leiva MC, Tolosa JE, Binotto CN, Weiner S, Huppert L, Denis AL, Huhta JC. Fetal cardiac development and hemodynamics in the first trimester. Ultrasound Obstet Gynecol 1999; 14:169-74; PMID:10550875; http://dx.doi.org/10.1046/j.1469-0705.1999.14030169.x
   PubMed Web of Science ®Google Scholar
• Mäkikallio K, Jouppila P, Räsänen J. Human fetal cardiac function during the first trimester of pregnancy. Heart 2005; 91:334-8; PMID:15710713; http://dx.doi.org/10.1136/hrt.2003.029736
   PubMed Web of Science ®Google Scholar
• Friedman D, Buyon J, Kim M, Glickstein JS. Fetal cardiac function assessed by Doppler myocardial performance index (Tei Index). Ultrasound Obstet Gynecol 2003; 21:33-6; PMID:12528158; http://dx.doi.org/10.1002/uog.11
   PubMed Web of Science ®Google Scholar
• Moreno R, Zamorano J, Almería C, Pérez-González JA, Mataix L, Rodrigo JL, Herrera D, Aubele A, Pérez de Isla L, De Marco E, et al. Isovolumic contraction time by pulsed-wave Doppler tissue imaging in aortic stenosis. Eur J Echocardiogr 2003; 4:279-85; PMID:14611823; http://dx.doi.org/10.1016/S1525-2167(03)00009-X
   PubMedGoogle Scholar
• Dorn GW 2nd, Robbins J, Ball N, Walsh RA. Myosin heavy chain regulation and myocyte contractile depression after LV hypertrophy in aortic-banded mice. Am J Physiol 1994; 267:H400-5; PMID:8048605
   PubMed Web of Science ®Google Scholar
• Ross J Jr. Cardiac function and myocardial contractility: a perspective. J Am Coll Cardiol 1983; 1:52-62; PMID:6826945; http://dx.doi.org/10.1016/S0735-1097(83)80010-2
   PubMedGoogle Scholar
• Duzenli MA, Ozdemir K, Aygul N, Soylu A, Aygul MU, Gök H. Comparison of myocardial performance index obtained either by conventional echocardiography or tissue Doppler echocardiography in healthy subjects and patients with heart failure. Heart Vessels 2009; 24:8-15; PMID:19165562; http://dx.doi.org/10.1007/s00380-008-1069-2
   PubMedGoogle Scholar
• Cutler MJ, Jeyaraj D, Rosenbaum DS. Cardiac electrical remodeling in health and disease. Trends Pharmacol Sci 2011; 32:174-80; PMID:21316769; http://dx.doi.org/10.1016/j.tips.2010.12.001
   PubMedGoogle Scholar
• Porciani MC, Dondina C, Macioce R, Demarchi G, Cappelli F, Lilli A, Pappone A, Ricciardi G, Colombo PC, Padeletti M, et al. Temporal variation in optimal atrioventricular and interventricular delay during cardiac resynchronization therapy. J Card Fail 2006; 12:715-9; PMID:17174233; http://dx.doi.org/10.1016/j.cardfail.2006.08.001
   PubMed Web of Science ®Google Scholar