I-Wire Heart-on-a-Chip II: Biomechanical analysis of contractile, three-dimensional cardiomyocyte tissue constructs

Acta Biomaterialia

Volumn 48, Issue , 2017, Pages 79-87

  Schroer, Alison K ^a   Shotwell, Matthew S ^b   Sidorov, Veniamin Y ^a,c   Wikswo, John P ^a,c,d   Merryman, W David ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Auxotonic contraction; Cardiac tissue engineering; Hill model muscle mechanics; Regeneration

Indexed keywords

BIOMECHANICS; CELL CULTURE; CONTROLLED DRUG DELIVERY; HEART; MUSCLE; REGENERATIVE MEDICINE; TISSUE REGENERATION;

AUXOTONIC CONTRACTION; BIOMECHANICAL ANALYSIS; CARDIAC TISSUE ENGINEERING; CARDIOMYOCYTES; HILL MODEL MUSCLE MECHANIC; HILL'S MODEL; MUSCLE MECHANICS; PROPERTY; REGENERATION; TISSUE CONSTRUCTS;

WIRE;

BIOMATERIAL; BLEBBISTATIN; ISOPRENALINE;

ARTICLE; BIOMECHANICS; CARDIAC MUSCLE CELL; CONTROLLED STUDY; HEART; HEART MUSCLE CONTRACTILITY; HEART MUSCLE TENSION; MATHEMATICAL MODEL; MUSCLE ACTION POTENTIAL; PRIORITY JOURNAL; TISSUE ENGINEERING; ACTION POTENTIAL; ANIMAL; CHEMISTRY; COMPUTER SIMULATION; DRUG EFFECTS; HEART CONTRACTION; LAB ON A CHIP; MICROELECTRODE; PHYSIOLOGY; PROCEDURES; RAT; TISSUE SCAFFOLD;

ACTION POTENTIALS; ANIMALS; BIOMECHANICAL PHENOMENA; COMPUTER SIMULATION; ISOPROTERENOL; LAB-ON-A-CHIP DEVICES; MICROELECTRODES; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; RATS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 85006958583     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2016.11.010     Document Type: Article

References (37)

1. [1] Sidorov, V.Y., Samson, P.C., Sidorova, T.N., Davidson, J.M., Lim, C.C., Wikswo, J.P., I-Wire Heart-on-a-Chip I: Three-dimensional cardiac tissue constructs for physiology and pharmacology. Acta Biomater. 48 (2017), 68–78, 10.1016/j.actbio.2016.11.009.
2. [2] Hill, A.V., The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. Lond. B 126 (1938), 136–195.
3. [3] Milani-Nejad, N., Xu, Y., Davis, J.P., Campbell, K.S., Janssen, P.M.L., Effect of muscle length on cross-bridge kinetics in intact cardiac trabeculae at body temperature. J. Gen. Physiol. 141 (2013), 133–139.
4. [4] Shiels, H.A., White, E., The Frank-Starling mechanism in vertebrate cardiac myocytes. J. Exp. Biol. 211 (2008), 2005–2013.
5. [5] Hill, A.V., First and Last Experiments in Muscle Mechanics. 1970, Cambridge University Press, London.
6. [6] Hill, A.V., The mechanics of active muscle. Proc. R. Soc. Lond. B 141 (1953), 104–117.
7. [7] McMahon, T.A., Muscles, Reflexes, and Locomotion. 1984, Princeton University Press, Princeton, NJ.
8. [8] Shadmehr, R.W.S., A Simple Muscle Model (Supplementary Document), The Computational Neurobiology of Reaching and Pointing: A Foundation for Motor Learning. 2005, MIT Press, Cambridge, MA.
9. [9] Chapelle, D., Clement, F., Genot, F., Tallec, P.L., Sorine, M., Urquiza, J.M., A physiologically-based model for the active cardiac muscle contraction. Katila, T., Nenonen, J., Magnin, I.E., Clarysse, P., Montagnat, J., (eds.) Functional Imaging and Modeling of the Heart, 2001, Springer, Berlin, Heidelberg, 128–133.
10. [10] Sermesant, M., Moireau, P., Camara, O., Sainte-Marie, J., Andriantsimiavona, R., Cimrman, R., Hill, D.L.G., Chapelle, D., Razavi, R., Cardiac function estimation from MRI using a heart model and data assimilation: advances and difficulties. Med. Image Anal. 10 (2006), 642–656.
11. [11] Winters, J.M., Hill-based muscle models: a systems engineering perspective. Winters, J.M., Woo, S.L.Y., (eds.) Multiple Muscle Systems: Biomechanics and Movement Organization, 1990, Springer, New York, NY, 69–93.
12. [12] Costa, K.D., Holmes, J.W., McCulloch, A.D., Modelling cardiac mechanical properties in three dimensions. Philos. Trans. R. Soc. Lond. A 359 (2001), 1233–1250.
13. [13] Wang, V.Y., Lam, H.I., Ennis, D.B., Cowan, B.R., Young, A.A., Nash, M.P., Modelling passive diastolic mechanics with quantitative MRI of cardiac structure and function. Med. Image Anal. 13 (2009), 773–784.
14. [14] Sack, K.L., Davies, N.H., Guccione, J.M., Franz, T., Personalised computational cardiology: patient-specific modelling in cardiac mechanics and biomaterial injection therapies for myocardial infarction. Heart Fail. Rev., 2016, 10.1007/s10741-016-9528-9.
15. [15] Sidorov, V.Y., Woods, M.C., Wikswo, J.P., Effects of elevated extracellular potassium on the stimulation mechanism of diastolic cardiac tissue. Biophys. J. 84 (2003), 3470–3479.
16. [16] Straight, A.F., Cheung, A., Limouze, J., Chen, I., Westwood, N.J., Sellers, J.R., Mitchison, T.J., Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299 (2003), 1743–1747.
17. [17] Kovacs, M., Toth, J., Hetenyi, C., Malnasi-Csizmadia, A., Sellers, J.R., Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279 (2004), 35557–35563.
18. [18] Brodde, O.E., Michel, M.C., Adrenergic and muscarinic receptors in the human heart. Pharmacol. Rev. 51 (1999), 651–690.
19. [19] Hazeltine, L.B., Simmons, C.S., Salick, M.R., Lian, X., Badur, M.G., Han, W., Delgado, S.M., Wakatsuki, T., Crone, W.C., Pruitt, B.L., Palecek, S.P., Effects of substrate mechanics on contractility of cardiomyocytes generated from human pluripotent stem cells. Int. J. Cell Biol., 2012, 2012, 508294.
20. [20] Fedorov, V.V., Leonov, S., Optimal Design for Nonlinear Response Models. 2013, CRC Press, Boca Raton, FL.
21. [21] Suard, I., Pery-Man, N., Coirault, C., Pourny, J.C., Lecarpentier, Y., Chemla, D., Relaxant effects of isoproterenol in isolated cardiac muscle: influence of loading patterns. Am. J. Physiol. 267 (1994), H1814–H1823.
22. [22] Campbell, K.B., Chandra, M., Kirkpatrick, R.D., Slinker, B.K., Hunter, W.C., Interpreting cardiac muscle force-length dynamics using a novel functional model. Am. J. Physiol. Heart 286 (2004), H1535–H1545.
23. [23] Beningo, K.A., Hamao, K., Dembo, M., Wang, Y.L., Hosoya, H., Traction forces of fibroblasts are regulated by the Rho-dependent kinase but not by the myosin light chain kinase. Arch. Biochem. Biophys. 456 (2006), 224–231.
24. [24] Allingham, J.S., Smith, R., Rayment, I., The structural basis of blebbistatin inhibition and specificity for myosin II. Nat. Struct. Mol. Biol. 12 (2005), 378–379.
25. [25] Malik, F.I., Hartman, J.J., Elias, K.A., Morgan, B.P., Rodriguez, H., Brejc, K., Anderson, R.L., Sueoka, S.H., Lee, K.H., Finer, J.T., Sakowicz, R., Baliga, R., Cox, D.R., Garard, M., Godinez, G., Kawas, R., Kraynack, E., Lenzi, D., Lu, P.P., Muci, A., Niu, C.R., Qian, X.P., Pierce, D.W., Pokrovskii, M., Suehiro, I., Sylvester, S., Tochimoto, T., Valdez, C., Wang, W.Y., Katori, T., Kass, D.A., Shen, Y.T., Vatner, S.F., Morgans, D.J., Cardiac myosin activation: a potential therapeutic approach for systolic heart failure. Science 331 (2011), 1439–1443.
26. [26] Grood, E.S., Mates, R.E., Falsetti, H., Model of cardiac-muscle dynamics. Circ. Res. 35 (1974), 184–196.
27. [27] Lee, L.C., Zhang, Z.H., Hinson, A., Guccione, J.M., Reduction in left ventricular wall stress and improvement in function in failing hearts using Algisyl-LVR. J. Vis. Exp., 2013 Article UNSP e50096.
28. [28] Wenk, J.F., Ge, L., Zhang, Z.H., Mojsejenko, D., Potter, D.D., Tseng, E.E., Guccione, J.M., Ratcliffe, M.B., Biventricular finite element modeling of the Acorn CorCap cardiac support device on a failing heart. Ann. Thorac. Surg. 95 (2013), 2022–2027.
29. [29] Wenk, J.F., Ge, L., Zhang, Z.H., Soleimani, M., Potter, D.D., Wallace, A.W., Tseng, E., Ratcliffe, M.B., Guccione, J.M., A coupled biventricular finite element and lumped-parameter circulatory system model of heart failure. Comput. Methods Biomech. Biomed. Eng. 16 (2013), 807–818.
30. [30] Wenk, J.F., Sun, K., Zhang, Z.H., Soleimani, M., Ge, L.A., Saloner, D., Wallace, A.W., Ratcliffe, M.B., Guccione, J.M., Regional left ventricular myocardial contractility and stress in a finite element model of posterobasal myocardial infarction. J. Biomech. Eng.-T. ASME, 133, 2011, 044501.
31. [31] Fujiwara, M., Yan, P.S., Otsuji, T.G., Narazaki, G., Uosaki, H., Fukushima, H., Kuwahara, K., Harada, M., Matsuda, H., Matsuoka, S., Okita, K., Takahashi, K., Nakagawa, M., Ikeda, T., Sakata, R., Mummery, C.L., Nakatsuji, N., Yamanaka, S., Nakao, K., Yamashita, J.K., Induction and enhancement of cardiac cell differentiation from mouse and human induced pluripotent stem cells with cyclosporin-A. PLoS One, 6, 2011, e16734.
32. [32] Gauthier, D.J., Resource letter: CC-1: controlling chaos. Am. J. Phys. 71 (2003), 750–759.
33. [33] Vunjak-Novakovic, G., Lui, K.O., Tandon, N., Chien, K.R., Bioengineering heart muscle: a paradigm for regenerative medicine. Annu. Rev. Biomed. Eng. 13 (2011), 245–267.
34. [34] Laflamme, M.A., Murry, C.E., Heart regeneration. Nature 473 (2011), 326–335.
35. [35] Stoyanov, H., Kollosche, M., Risse, S., Wache, R., Kofod, G., Soft conductive elastomer materials for stretchable electronics and voltage controlled artificial muscles. Adv. Mater. 25 (2013), 578–583.
36. [36] Ma, M.M., Guo, L., Anderson, D.G., Langer, R., Bio-inspired polymer composite actuator and generator driven by water gradients. Science 339 (2013), 186–189.
37. [37] Juluri, B.K., Kumar, A.S., Liu, Y., Ye, T., Yang, Y.W., Flood, A.H., Fang, L., Stoddart, J.F., Weiss, P.S., Huang, T.J., A mechanical actuator driven electrochemically by artificial molecular muscles. ACS Nano 3 (2009), 291–300.