Abstract
From an engineering perspective, many forms of heart disease can be thought of as a reduction in biomaterial performance, in which the biomaterial is the tissue comprising the ventricular wall. In materials science, the structure and properties of a material are recognized to be interconnected with performance. In addition, for most measurements of structure, properties, and performance, some processing is required. Here, we review the current state of knowledge regarding cardiac tissue structure, properties, and performance as well as the processing steps taken to acquire those measurements. Understanding the impact of these factors and their interactions may enhance our understanding of heart function and heart failure. We also review design considerations for cardiac tissue property and performance measurements because, to date, most data on cardiac tissue has been obtained under non-physiological loading conditions. Novel measurement systems that account for these design considerations may improve future experiments and lead to greater insight into cardiac tissue structure, properties, and ultimately performance.
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References
Ait Mou, Y., et al. Differential contribution of cardiac sarcomeric proteins in the myofibrillar force response to stretch. Pflugers Arch. 457:25–36, 2008.
Bers, D. M. Calcium fluxes involved in control of cardiac myocyte contraction. Circ. Res. 87:275–281, 2000.
Bluhm, W. F., A. D. McCulloch, and W. Y. Lew. Active force in rabbit ventricular myocytes. J. Biomech. 28:1119–1122, 1995.
Bollensdorff, C., O. Lookin, and P. Kohl. Assessment of contractility in intact ventricular cardiomyocytes using the dimensionless ‘frank-starling gain’ index. Pflugers Arch. 462:39–48, 2011.
Brady, A. J. Mechanical properties of isolated cardiac myocytes. Physiol. Rev. 71:413–428, 1991.
Brady, A. J., S. T. Tan, and N. V. Ricchiuti. Contractile force measured in unskinned isolated adult rat heart fibres. Nature 282:728–729, 1979.
Brixius, K., et al. Reduced length-dependent cross-bridge recruitment in skinned fiber preparations of human failing myocardium. Eur. J. Appl. Physiol. 89:249–256, 2003.
Bryant, S. M., S. J. Shipsey, and G. Hart. Regional differences in electrical and mechanical properties of myocytes from guinea-pig hearts with mild left ventricular hypertrophy. Cardiovasc. Res. 35:315–323, 1997.
Cazorla, O., J. Y. Le Guennec, and E. White. Length-tension relationships of sub-epicardial and sub-endocardial single ventricular myocytes from rat and ferret hearts. J. Mol. Cell. Cardiol. 32:735–744, 2000.
Cazorla, O., et al. Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ. Res. 88:1028–1035, 2001.
Chung, C. S., and H. L. Granzier. Contribution of titin and extracellular matrix to passive pressure and measurement of sarcomere length in the mouse left ventricle. J. Mol. Cell. Cardiol. 50:731–739, 2011.
Costa, K. D., J. W. Holmes, and A. D. McCulloch. Modelling cardiac mechanical properties in three dimensions. Philos. Trans. R. Soc. Lond. 359:1233–1250, 2001.
de Tombe, P. P. Altered contractile function in heart failure. Cardiovasc. Res. 37:367–380, 1998.
de Tombe, P. P., et al. Right ventricular contractile protein function in rats with left ventricular myocardial infarction. Am. J. Physiol. 271:H73–H79, 1996.
de Tombe, P. P., et al. Myofilament length dependent activation. J. Mol. Cell. Cardiol. 48:851–858, 2010.
Diffee, G. M., and D. F. Nagle. Regional differences in effects of exercise training on contractile and biochemical properties of rat cardiac myocytes. J. Appl. Physiol. 95(35–42):2003, 1985.
Dobesh, D. P., J. P. Konhilas, and P. P. de Tombe. Cooperative activation in cardiac muscle: impact of sarcomere length. Am. J. Physiol. Heart Circ. Physiol. 282:H1055–H1062, 2002.
Edes, I. F., et al. Rate of tension redevelopment is not modulated by sarcomere length in permeabilized human, murine, and porcine cardiomyocytes. Am J. Physiol. Regul. Integr. Comp. Physiol. 293:R20–R29, 2007.
Farman, G. P., et al. The role of thin filament cooperativity in cardiac length-dependent calcium activation. Biophys. J. 99:2978–2986, 2010.
Friedberg, M. K., and A. N. Redington. Right versus left ventricular failure: differences, similarities, and interactions. Circulation 129:1033–1044, 2014.
Gao, W. D., et al. Myofilament Ca2+ sensitivity in intact versus skinned rat ventricular muscle. Circ. Res. 74:408–415, 1994.
Garcia-Webb, M. G., et al. A modular instrument for exploring the mechanics of cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 293:H866–H874, 2007.
Granzier, H. L., and T. C. Irving. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys. J. 68:1027–1044, 1995.
Hamdani, N., et al. Sarcomeric dysfunction in heart failure. Cardiovasc. Res. 77:649–658, 2008.
Han, J. C., et al. A unique micromechanocalorimeter for simultaneous measurement of heat rate and force production of cardiac trabeculae carneae. J. Appl. Physiol. 107:946–951, 2009.
Han, J. C., et al. Interventricular comparison of the energetics of contraction of Trabeculae carneae isolated from the rat heart. J. Physiol. 591:701–717, 2013.
Hand, P. E., and C. S. Peskin. Homogenization of an electrophysiological model for a strand of cardiac myocytes with gap-junctional and electric-field coupling. Bull. Math. Biol. 72:1408–1424, 2010.
Iribe, G., M. Helmes, and P. Kohl. Force-length relations in isolated intact cardiomyocytes subjected to dynamic changes in mechanical load. Am. J. Physiol. Heart Circ. Physiol. 292:H1487–H1497, 2007.
Irving, T. C., et al. Myofilament lattice spacing as a function of sarcomere length in isolated rat myocardium. Am. J. Physiol. Heart Circ. Physiol. 279:H2568–H2573, 2000.
Iwazumi, T. High-speed ultrasensitive instrumentation for myofibril mechanics measurements. Am. J. Physiol. 252:C253–C262, 1987.
Joho, S., et al. Left ventricular pressure–volume relationship in conscious mice. Am. J. Physiol. Heart Circ. Physiol. 292:H369–H377, 2007.
King, N. M. P., et al. Mouse intact cardiac myocyte mechanics: cross-bridge and titin-based stress in unactivated cells. J. Gen. Physiol. 137:81–91, 2011.
Kondo, R. P., et al. Comparison of contraction and calcium handling between right and left ventricular myocytes from adult mouse heart: a role for repolarization waveform. J. Physiol. 571:131–146, 2006.
Konhilas, J. P., et al. Troponin I in the murine myocardium: Influence on length-dependent activation and interfilament spacing. J. Physiol. 547:951–961, 2003.
Korte, F. S., and K. S. McDonald. Sarcomere length dependence of rat skinned cardiac myocyte mechanical properties: dependence on myosin heavy chain. J. Physiol. 581:725–739, 2007.
Le Guennec, J. Y., et al. A new method of attachment of isolated mammalian ventricular myocytes for tension recording: length dependence of passive and active tension. J. Mol. Cell. Cardiol. 22:1083–1093, 1990.
Lee, E.-J., et al. Calcium sensitivity and the frank-starling mechanism of the heart are increased in titin n2b region-deficient mice. J. Mol. Cell. Cardiol. 49:449–458, 2010.
LeGrice, I., et al. The architecture of the heart: a data–based model. Philos. Trans. R. Soc. Lond. 359:1217–1232, 2001.
Lin, G., et al. Miniature heart cell force transducer system implemented in MEMS technology. IEEE Trans. Biomed. Eng. 48:996–1006, 2001.
Nishimura, S., et al. Single cell mechanics of rat cardiomyocytes under isometric, unloaded, and physiologically loaded conditions. Am. J. Physiol. Heart Circ. Physiol. 287:H196–H202, 2004.
Nordsletten, D. A., et al. Coupling multi-physics models to cardiac mechanics. Prog. Biophys. Mol. Biol. 104:77–88, 2011.
Pacher, P., et al. Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat. Protoc. 3:1422–1434, 2008.
Patel, J. R., et al. Pka accelerates rate of force development in murine skinned myocardium expressing α-or β-tropomyosin. Am. J. Physiol. Heart Circ. Physiol. 280:H2732–H2739, 2001.
Patel, J. R., et al. Magnitude of length-dependent changes in contractile properties varies with titin isoform in rat ventricles. Am. J. Physiol. Heart Circ. Physiol. 302:H697–H708, 2012.
Perreault, C. L., et al. Differential effects of cardiac hypertrophy and failure on right vs. left ventricular calcium activation. Circ. Res. 67:707–712, 1990.
Petroff, M. G., et al. Endogenous nitric oxide mechanisms mediate the stretch dependence of Ca2+ release in cardiomyocytes. Nat. Cell Biol. 3:867–873, 2001.
Redington, A. N., et al. Characterisation of the normal right ventricular pressure-volume relation by biplane angiography and simultaneous micromanometer pressure measurements. Br. Heart J. 59:23–30, 1988.
Roche, S. L., and A. N. Redington. The failing right ventricle in congenital heart disease. Can. J. Cardiol. 29:768–778, 2013.
Rundell, V. L. M., et al. Impact of beta-myosin heavy chain isoform expression on cross-bridge cycling kinetics. Am. J. Physiol. Heart Circ. Physiol. 288:H896–H903, 2005.
Schwinger, R. H., et al. The failing human heart is unable to use the frank-starling mechanism. Circ. Res. 74:959–969, 1994.
Shaw, J., L. Izu, and Y. Chen-Izu. Mechanical analysis of single myocyte contraction in a 3d elastic matrix. PLoS ONE 8:e75492–e75492, 2013.
Stevens, C., and P. J. Hunter. Sarcomere length changes in a 3d mathematical model of the pig ventricles. Prog. Biophys. Mol. Biol. 82:229–241, 2003.
Suzuki, M., H. Fujita, and S. Ishiwata. A new muscle contractile system composed of a thick filament lattice and a single actin filament. Biophys. J. 89:321–328, 2005.
Taberner, A. J., et al. An innovative work-loop calorimeter for in vitro measurement of the mechanics and energetics of working cardiac trabeculae. J. Appl. Physiol. 111:1798–1803, 2011.
Tabima, D. M., T. A. Hacker, and N. C. Chesler. Measuring right ventricular function in the normal and hypertensive mouse hearts using admittance-derived pressure-volume loops. Am. J. Physiol. Heart Circ. Physiol. 299:H2069–H2075, 2010.
Tasche, C., E. Meyhofer, and B. Brenner. A force transducer for measuring mechanical properties of single cardiac myocytes. Am. J. Physiol. 277:H2400–H2408, 1999.
Trayanova, N. A., and J. J. Rice. Cardiac electromechanical models: from cell to organ. Front. Physiol. 2:43, 2011.
Umar, S., et al. Allogenic stem cell therapy improves right ventricular function by improving lung pathology in rats with pulmonary hypertension. Am. J. Physiol. Heart Circ. Physiol. 297:H1606–H1616, 2009.
van der Velden, J., et al. Effect of protein kinase a on calcium sensitivity of force and its sarcomere length dependence in human cardiomyocytes. Cardiovasc. Res. 46:487–495, 2000.
van der Velden, J., et al. Increased Ca2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovasc. Res. 57:37–47, 2003.
van der Velden, J., et al. The effect of myosin light chain 2 dephosphorylation on Ca2+-sensitivity of force is enhanced in failing human hearts. Cardiovasc. Res. 57:505–514, 2003.
Walker, L. A., and P. M. Buttrick. The right ventricle: biologic insights and response to disease. Curr. Cardiol. Rev. 5:22–28, 2009.
Walker, L. A., et al. Biochemical and myofilament responses of the right ventricle to severe pulmonary hypertension. Am. J. Physiol. Heart Circ. Physiol. 301:H832–H840, 2011.
Washio, T., J.-I. Okada, and T. Hisada. A parallel multilevel technique for solving the bidomain equation on a human heart with purkinje fibers and a torso model. SIAM Rev. 52:717–743, 2010.
Washio, T., et al. Approximation for cooperative interactions of a spatially-detailed cardiac sarcomere model. Cell. Mol. Bioeng. 5:113–126, 2012.
Wu, Y., et al. Changes in titin and collagen underlie diastolic stiffness diversity of cardiac muscle. J. Mol. Cell. Cardiol. 32:2151–2162, 2000.
Yasuda, S.-I., et al. A novel method to study contraction characteristics of a single cardiac myocyte using carbon fibers. Am. J. Physiol. Heart Circ. Physiol. 281:1442–1446, 2001.
Zaffran, S., et al. Right ventricular myocardium derives from the anterior heart field. Circ. Res. 95:261–268, 2004.
Acknowledgements
Our work was supported by NIH grants 1R01HL086939 (NCC) and 1R37HL82900 (RLM). The authors thank Carol Dizack for preparing the illustrations and Dr. Jitandrakumar Patel for unpublished force-pCa data.
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Associate Editor Jane Grande-Allen oversaw the review of this article.
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Golob, M., Moss, R.L. & Chesler, N.C. Cardiac Tissue Structure, Properties, and Performance: A Materials Science Perspective. Ann Biomed Eng 42, 2003–2013 (2014). https://doi.org/10.1007/s10439-014-1071-z
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DOI: https://doi.org/10.1007/s10439-014-1071-z