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Cardiac Tissue Structure, Properties, and Performance: A Materials Science Perspective

Annals of Biomedical Engineering volume 42, pages 2003–2013 (2014)Cite this article

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

  1. Ait Mou, Y., et al. Differential contribution of cardiac sarcomeric proteins in the myofibrillar force response to stretch. Pflugers Arch. 457:25–36, 2008.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  2. Bers, D. M. Calcium fluxes involved in control of cardiac myocyte contraction. Circ. Res. 87:275–281, 2000.

    CAS  PubMed  Article  Google Scholar 

  3. Bluhm, W. F., A. D. McCulloch, and W. Y. Lew. Active force in rabbit ventricular myocytes. J. Biomech. 28:1119–1122, 1995.

    CAS  PubMed  Article  Google Scholar 

  4. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  5. Brady, A. J. Mechanical properties of isolated cardiac myocytes. Physiol. Rev. 71:413–428, 1991.

    CAS  PubMed  Google Scholar 

  6. 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.

    CAS  PubMed  Article  Google Scholar 

  7. 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.

    PubMed  Article  Google Scholar 

  8. 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.

    CAS  PubMed  Article  Google Scholar 

  9. 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.

    CAS  PubMed  Article  Google Scholar 

  10. Cazorla, O., et al. Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ. Res. 88:1028–1035, 2001.

    CAS  PubMed  Article  Google Scholar 

  11. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  12. 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.

    Article  Google Scholar 

  13. de Tombe, P. P. Altered contractile function in heart failure. Cardiovasc. Res. 37:367–380, 1998.

    PubMed  Article  Google Scholar 

  14. 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.

    PubMed  Google Scholar 

  15. de Tombe, P. P., et al. Myofilament length dependent activation. J. Mol. Cell. Cardiol. 48:851–858, 2010.

    PubMed Central  PubMed  Article  Google Scholar 

  16. 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.

    Google Scholar 

  17. 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.

    CAS  PubMed  Google Scholar 

  18. 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.

    CAS  PubMed  Article  Google Scholar 

  19. Farman, G. P., et al. The role of thin filament cooperativity in cardiac length-dependent calcium activation. Biophys. J. 99:2978–2986, 2010.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  20. Friedberg, M. K., and A. N. Redington. Right versus left ventricular failure: differences, similarities, and interactions. Circulation 129:1033–1044, 2014.

    PubMed  Article  Google Scholar 

  21. Gao, W. D., et al. Myofilament Ca2+ sensitivity in intact versus skinned rat ventricular muscle. Circ. Res. 74:408–415, 1994.

    CAS  PubMed  Article  Google Scholar 

  22. 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.

    CAS  PubMed  Article  Google Scholar 

  23. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  24. Hamdani, N., et al. Sarcomeric dysfunction in heart failure. Cardiovasc. Res. 77:649–658, 2008.

    CAS  PubMed  Article  Google Scholar 

  25. 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.

    PubMed  Article  Google Scholar 

  26. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  27. 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.

    PubMed  Article  Google Scholar 

  28. 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.

    CAS  PubMed  Article  Google Scholar 

  29. 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.

    CAS  PubMed  Google Scholar 

  30. Iwazumi, T. High-speed ultrasensitive instrumentation for myofibril mechanics measurements. Am. J. Physiol. 252:C253–C262, 1987.

    CAS  PubMed  Google Scholar 

  31. Joho, S., et al. Left ventricular pressure–volume relationship in conscious mice. Am. J. Physiol. Heart Circ. Physiol. 292:H369–H377, 2007.

    CAS  PubMed  Article  Google Scholar 

  32. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  33. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  34. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  35. 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.

    PubMed Central  PubMed  Article  Google Scholar 

  36. 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.

    PubMed  Article  Google Scholar 

  37. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  38. LeGrice, I., et al. The architecture of the heart: a data–based model. Philos. Trans. R. Soc. Lond. 359:1217–1232, 2001.

    Article  Google Scholar 

  39. Lin, G., et al. Miniature heart cell force transducer system implemented in MEMS technology. IEEE Trans. Biomed. Eng. 48:996–1006, 2001.

    CAS  PubMed  Article  Google Scholar 

  40. 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.

    CAS  PubMed  Article  Google Scholar 

  41. Nordsletten, D. A., et al. Coupling multi-physics models to cardiac mechanics. Prog. Biophys. Mol. Biol. 104:77–88, 2011.

    CAS  PubMed  Article  Google Scholar 

  42. Pacher, P., et al. Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat. Protoc. 3:1422–1434, 2008.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  43. 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.

    CAS  PubMed  Google Scholar 

  44. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  45. 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.

    CAS  PubMed  Article  Google Scholar 

  46. 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.

    CAS  PubMed  Article  Google Scholar 

  47. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  48. Roche, S. L., and A. N. Redington. The failing right ventricle in congenital heart disease. Can. J. Cardiol. 29:768–778, 2013.

    PubMed  Article  Google Scholar 

  49. 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.

    CAS  PubMed  Article  Google Scholar 

  50. Schwinger, R. H., et al. The failing human heart is unable to use the frank-starling mechanism. Circ. Res. 74:959–969, 1994.

    CAS  PubMed  Article  Google Scholar 

  51. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  52. 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.

    PubMed  Article  Google Scholar 

  53. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  54. 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.

    PubMed  Article  Google Scholar 

  55. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  56. 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.

    CAS  PubMed  Google Scholar 

  57. Trayanova, N. A., and J. J. Rice. Cardiac electromechanical models: from cell to organ. Front. Physiol. 2:43, 2011.

    PubMed Central  PubMed  Article  Google Scholar 

  58. 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.

    CAS  PubMed  Article  Google Scholar 

  59. 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.

    PubMed  Article  Google Scholar 

  60. 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.

    PubMed  Article  Google Scholar 

  61. 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.

    PubMed  Article  Google Scholar 

  62. Walker, L. A., and P. M. Buttrick. The right ventricle: biologic insights and response to disease. Curr. Cardiol. Rev. 5:22–28, 2009.

    PubMed Central  PubMed  Article  Google Scholar 

  63. 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  64. 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.

    Article  Google Scholar 

  65. Washio, T., et al. Approximation for cooperative interactions of a spatially-detailed cardiac sarcomere model. Cell. Mol. Bioeng. 5:113–126, 2012.

    PubMed Central  PubMed  Article  Google Scholar 

  66. Wu, Y., et al. Changes in titin and collagen underlie diastolic stiffness diversity of cardiac muscle. J. Mol. Cell. Cardiol. 32:2151–2162, 2000.

    CAS  PubMed  Article  Google Scholar 

  67. 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.

    Google Scholar 

  68. Zaffran, S., et al. Right ventricular myocardium derives from the anterior heart field. Circ. Res. 95:261–268, 2004.

    CAS  PubMed  Article  Google Scholar 

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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.

Conflict of interest

None declared.

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Affiliations

  1. Department of Biomedical Engineering, UW-Madison College of Engineering, 2146 Engineering Centers Building, 1550 Engineering Drive, Madison, WI, 53706, USA

    Mark Golob & Naomi C. Chesler

  2. Material Science Program, UW-Madison College of Engineering, Madison, WI, 53706, USA

    Mark Golob

  3. Department of Cell and Regenerative Biology, UW-Madison School of Medicine and Public Health, Madison, WI, 53706, USA

    Richard L. Moss

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  1. Mark Golob
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  2. Richard L. Moss
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  3. Naomi C. Chesler
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Correspondence to Naomi C. Chesler.

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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

Keywords

  • Cardiac myocyte mechanics
  • Cardiac sarcomere mechanics
  • Cardiac tissue testing
  • Review