I-Wire Heart-on-a-Chip I: Three-dimensional cardiac tissue constructs for physiology and pharmacology

Acta Biomaterialia

Volumn 48, Issue , 2017, Pages 68-78

  Sidorov, Veniamin Y ^a,b   Samson, Philip C ^a   Sidorova, Tatiana N ^c   Davidson, Jeffrey M ^c,d   Lim, Chee C ^c   Wikswo, John P ^a,b,c  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Auxotonic contraction; Cardiac tissue elasticity; Cardiac tissue engineering; Force frequency relationship; Frank Starling relationship

Indexed keywords

BIOMECHANICS; DIAGNOSIS; ELECTROPHYSIOLOGY; HEART; PROBES; PROFESSIONAL ASPECTS; STEM CELLS; TISSUE; TISSUE ENGINEERING;

AUXOTONIC CONTRACTION; CARDIAC TISSUE ELASTICITY; CARDIAC TISSUE ENGINEERING; CARDIAC TISSUES; FORCE-FREQUENCY RELATIONSHIP; FRANK-STARLING RELATIONSHIP; MEASUREMENTS OF; MECHANICAL AND ELECTRICAL; TISSUE CONSTRUCTS; TISSUE ELASTICITY;

WIRE;

BLEBBISTATIN; FIBRIN; FUSED HETEROCYCLIC RINGS; ISOPRENALINE;

ANIMAL CELL; ARTICLE; BETA ADRENERGIC STIMULATION; BIOENERGY; BIOMECHANICS; DRUG SCREENING; ELECTRICAL EQUIPMENT; ELECTROSTIMULATION; ENGINEERED HEART TISSUE; HEART; HEART CELL CULTURE; HEART DISEASE; I WIRE SYSTEM; INDUCED PLURIPOTENT STEM CELL; MEMBRANE POTENTIAL; METABOLOMICS; MICROFLUIDICS; NEWBORN; NONHUMAN; PHARMACOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; RAT; SARCOMERE; STARLING LAW; THREE DIMENSIONAL IMAGING; TISSUE ENGINEERING; ACTION POTENTIAL; ANIMAL; CELL CULTURE; CHEMISTRY; DRUG EFFECTS; ELASTICITY; HEART CONTRACTION; LAB ON A CHIP; PHENOTYPE; PROCEDURES; SPRAGUE DAWLEY RAT; TISSUE SCAFFOLD;

ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; ELASTICITY; HEART; HETEROCYCLIC COMPOUNDS, 4 OR MORE RINGS; ISOPROTERENOL; LAB-ON-A-CHIP DEVICES; MYOCARDIAL CONTRACTION; PHENOTYPE; RATS, SPRAGUE-DAWLEY; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 85006716619     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2016.11.009     Document Type: Article

References (71)

1. [1] Wikswo, J.P., The relevance and potential roles of microphysiological systems in biology and medicine. Exp. Biol. Med. 239 (2014), 1061–1072.
2. [2] Wikswo, J.P., Porter, A.P., Biology coming full circle: joining the whole and the parts. Exp. Biol. Med. 240 (2015), 3–7.
3. [3] van der Meer, A.D., van den Berg, A., Organs-on-chips: breaking the in vitro impasse. Integr. Biol. 4 (2012), 461–470.
4. [4] Ghaemmaghami, A.M., Hancock, M.J., Harrington, H., Kaji, H., Khademhosseini, A., Biomimetic tissues on a chip for drug discovery. Drug Discov. Today 17 (2012), 173–181.
5. [5] Huh, D., Matthews, B.D., Mammoto, A., Montoya-Zavala, M., Hsin, H.Y., Ingber, D.E., Reconstituting organ-level lung functions on a chip. Science 328 (2010), 1662–1668.
6. [6] Vrana, N.E., Lavalle, P., Dokmeci, M.R., Dehghani, F., Ghaemmaghami, A.M., Khademhosseini, A., Engineering functional epithelium for regenerative medicine and in vitro organ models: a review. Tissue Eng. Pt. B: Rev 19 (2013), 529–543.
7. [7] Morin-Brureau, M., De Bock, F., Lerner-Natoli, M., Organotypic brain slices: a model to study the neurovascular unit micro-environment in epilepsies. Fluids Barriers CNS 10 (2013), 1–12.
8. [8] Choi, S.H., Kim, Y.H., Hebisch, M., Sliwinski, C., Lee, S., D'Avanzo, C., Chen, H., Hooli, B., Asselin, C., Muffat, J., Klee, J.B., Zhang, C., Wainger, B.J., Peitz, M., Kovacs, D.M., Woolf, C.J., Wagner, S.L., Tanzi, R.E., Kim, D.Y., A three-dimensional human neural cell culture model of Alzheimer's disease. Nature 515 (2014), 274–278.
9. [9] Maschmeyer, I., Lorenz, A.K., Schimek, K., Hasenberg, T., Ramme, A.P., Hubner, J., Lindner, M., Drewell, C., Bauer, S., Thomas, A., Sambo, N.S., Sonntag, F., Lauster, R., Marx, U., A four-organ-chip for interconnected long-term co-culture of human intestine, liver, skin and kidney equivalents. Lab Chip 15 (2015), 2688–2699.
10. [10] Brown, J.A., Sherrod, S.D., Goodwin, C.R., Brewer, B., Yang, L., Garbett, K.A., Li, D., McLean, J.A., Wikswo, J.P., Mirnics, K., Metabolic consequences of interleukin-6 challenge in developing neurons and astroglia. J. Neuroinflamm., 11, 2014 Article 183.
11. [11] Huh, D., Leslie, D.C., Matthews, B.D., Fraser, J.P., Jurek, S., Hamilton, G.A., Thorneloe, K.S., Mcalexander, M.A., Ingber, D.E., A human disease model of drug toxicity-induced pulmonary edema in a lung-on-a-chip microdevice. Sci. Transl. Med., 4, 2012, 159ra147.
12. [12] Stucki, A.O., Stucki, J.D., Hall, S.R.R., Felder, M., Mermoud, Y., Schmid, R.A., Geiser, T., Guenat, O.T., A lung-on-a-chip array with an integrated bio-inspired respiration mechanism. Lab Chip 15 (2015), 1302–1310.
13. [13] Kim, H.J., Huh, D., Hamilton, G., Ingber, D.E., Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 12 (2012), 2165–2174.
14. [14] Schroer, A.K., Shotwell, M.S., Sidorov, V.Y., Wikswo, J.P., Merryman, W.D., I-Wire Heart-on-a-Chip II: biomechanical analysis of contractile, three-dimensional cardiomyocyte tissue constructs. Acta Biomater. 48 (2017), 79–87, 10.1016/j.actbio.2016.11.010.
15. [15] Huebsch, N., Loskill, P., Mandegar, M.A., Marks, N.C., Sheehan, A.S., Ma, Z., Mathur, A., Nguyen, T.N., Yoo, J.C., Judge, L.M., Spencer, C.I., Chukka, A.C., Russell, C.R., So, P.L., Conklin, B.R., Healy, K.E., Automated video-based analysis of contractility and calcium flux in human-induced pluripotent stem cell-derived cardiomyocytes cultured over different spatial scales. Tissue Eng. Pt. C 21 (2015), 467–479.
16. [16] Mathur, A., Loskill, P., Shao, K.F., Huebsch, N., Hong, S., Marcus, S.G., Marks, N., Mandegar, M., Conklin, B.R., Lee, L.P., Healy, K.E., Human iPSC-based cardiac microphysiological system for drug screening applications. Sci. Rep., 5, 2015 Article 8883.
17. [17] Alford, P.W., Feinberg, A.W., Sheehy, S.P., Parker, K.K., Biohybrid thin films for measuring contractility in engineered cardiovascular muscle. Biomaterials 31 (2010), 3613–3621.
18. [18] Grosberg, A., Alford, P.W., McCain, M.L., Parker, K.K., Ensembles of engineered cardiac tissues for physiological and pharmacological study: heart on a chip. Lab Chip 11 (2011), 4165–4173.
19. [19] Agarwal, A., Goss, J.A., Cho, A., McCain, M.L., Parker, K.K., Microfluidic heart on a chip for higher throughput pharmacological studies. Lab Chip 13 (2013), 3599–3608.
20. [20] Feinberg, A.W., Alford, P.W., Jin, H.W., Ripplinger, C.M., Werdich, A.A., Sheehy, S.P., Grosberg, A., Parker, K.K., Controlling the contractile strength of engineered cardiac muscle by hierarchal tissue architecture. Biomaterials 33 (2012), 5732–5741.
21. [21] Boudou, T., Legant, W.R., Mu, A., Borochin, M.A., Thavandiran, N., Radisic, M., Zandstra, P.W., Epstein, J.A., Margulies, K.B., Chen, C.S., A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues. Tissue Eng. Pt. A 18 (2012), 910–919.
22. 2+ transients in engineered heart tissue. Am. J. Physiol. Heart 306 (2014), H1353–H1363.
23. [23] Godier-Furnemont, A.F.G., Tiburcy, M., Wagner, E., Dewenter, M., Lammle, S., El-Armouche, A., Lehnart, S.E., Vunjak-Novakovic, G., Zimmermann, W.H., Physiologic force-frequency response in engineered heart muscle by electromechanical stimulation. Biomaterials 60 (2015), 82–91.
24. [24] West, A.R., Zaman, N., Cole, D.J., Walker, M.J., Legant, W.R., Boudou, T., Chen, C.S., Favreau, J.T., Gaudette, G.R., Cowley, E.A., Maksym, G.N., Development and characterization of a 3D multicell microtissue culture model of airway smooth muscle. Am. J. Physiol. Lung 304 (2013), L4–L16.
25. [25] Thavandiran, N., Dubois, N., Mikryukov, A., Masse, S., Beca, B., Simmons, C.A., Deshpande, V.S., McGarry, J.P., Chen, C.S., Nanthakumar, K., Keller, G.M., Radisic, M., Zandstra, P.W., Design and formulation of functional pluripotent stem cell-derived cardiac microtissues. PNAS 110 (2013), E4698–E4707.
26. [26] Chen, G.P., Li, S., Karakikes, I., Ren, L.H., Chow, M.Z.Y., Chopra, A., Keung, W., Yan, B., Chan, C.W.Y., Costa, K.D., Kong, C.W., Hajjar, R.J., Chen, C.S., Li, R.A., Phospholamban as a crucial determinant of the inotropic response of human pluripotent stem cell-derived ventricular cardiomyocytes and engineered 3-dimensional tissue constructs. Circ. Arrhythm. Electrophysiol. 8 (2015), 193–202.
27. [27] Sonnenblick, E.H., Force-velocity relations in mammalian heart muscle. Am. J. Physiol. 202 (1962), 931–932.
28. [28] Grood, E.S., Mates, R.E., Falsetti, H., Model of cardiac-muscle dynamics. Circ. Res. 35 (1974), 184–196.
29. [29] 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. 292 (2007), H1487–H1497.
30. [30] Nawroth, J.C., Lee, H., Feinberg, A.W., Ripplinger, C.M., McCain, M.L., Grosberg, A., Dabiri, J.O., Parker, K.K., A tissue-engineered jellyfish with biomimetic propulsion. Nat. Biotechnol. 30 (2012), 792–797.
31. [31] Zhong, L., Chiusa, M., Cadar, A.G., Lin, A., Samaras, S., Davidson, J.M., Lim, C.C., Targeted inhibition of ANKRD1 disrupts sarcomeric ERK-GATA4 signal transduction and abrogates phenylephrine-induced cardiomyocyte hypertrophy. Cardiovasc. Res. 106 (2015), 261–271.
32. [32] Zimmermann, W.H., Fink, C., Kralisch, D., Remmers, U., Weil, J., Eschenhagen, T., Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnol. Bioeng. 68 (2000), 106–114.
33. [33] Banerjee, I., Fuseler, J.W., Price, R.L., Borg, T.K., Baudino, T.A., Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am. J. Physiol. Heart 293 (2007), H1883–H1891.
34. [34] Hansen, A., Eder, A., Bonstrup, M., Flato, M., Mewe, M., Schaaf, S., Aksehirlioglu, B., Schworer, A., Uebeler, J., Eschenhagen, T., Development of a drug screening platform based on engineered heart tissue. Circ. Res. 107 (2010), 35–44.
35. [35] 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.
36. [36] 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.
37. [37] 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.
38. [38] Warren, M.L., Forces. Renz, P., (eds.) Introductory Physics, 1979, W.H. Freeman, San Francisco, 77–92.
39. [39] Katz, A.M., Regulation of Myocardial Contractility (Inotropyn) and Relaxation (Lusitropy), Physiology of the Heart. 2001, Lippincott Williams & Wilkins, Philadelphia, 368–397.
40. [40] Brodde, O.E., Michel, M.C., Adrenergic and muscarinic receptors in the human heart. Pharmacol. Rev. 51 (1999), 651–690.
41. [41] Askeland, D.R., Phule, P.P., Mechanical Properties: Part One. 2006, The Science and Engineering of Materials, Thomson, Toronto, 197–246.
42. [42] Eschenhagen, T., Fink, C., Remmers, U., Scholz, H., Wattchow, J., Weil, J., Zimmermann, W., Dohmen, H.H., Schafer, H., Bishopric, N., Wakatsuki, T., Elson, E.L., Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J. 11 (1997), 683–694.
43. [43] Zimmermann, W.H., Schneiderbanger, K., Schubert, P., Didie, M., Munzel, F., Heubach, J.F., Kostin, S., Neuhuber, W.L., Eschenhagen, T., Tissue engineering of a differentiated cardiac muscle construct. Circ. Res. 90 (2002), 223–230.
44. [44] Asnes, C.F., Marquez, J.P., Elson, E.L., Wakatsuki, T., Reconstitution of the Frank-Starling mechanism in engineered heart tissues. Biophys. J. 91 (2006), 1800–1810.
45. [45] de Lange, W.J., Hegge, L.F., Grimes, A.C., Tong, C.W., Brost, T.M., Moss, R.L., Ralphe, J.C., Neonatal mouse-derived engineered cardiac tissue a novel model system for studying genetic heart disease. Circ. Res. 109 (2011), 8–19.
46. [46] Sakar, M.S., Neal, D., Boudou, T., Borochin, M.A., Li, Y.Q., Weiss, R., Kamm, R.D., Chen, C.S., Asada, H.H., Formation and optogenetic control of engineered 3D skeletal muscle bioactuators. Lab Chip 12 (2012), 4976–4985.
47. [47] Golob, M., Moss, R., Chesler, N., Cardiac tissue structure, properties, and performance: a materials science perspective. Ann. Biomed. Eng. 42 (2014), 2003–2013.
48. [48] Katz, A.M., Energy Utilization: Work and Heat, Physiology of the Heart. 2001, Lippincott Williams & Wilkins, Philadelphia, 101–122.
49. [49] Sniadecki, N.J., Anguelouch, A., Yang, M.T., Lamb, C.M., Liu, Z., Kirschner, S.B., Liu, Y., Reich, D.H., Chen, C.S., From the cover: magnetic microposts as an approach to apply forces to living cells. PNAS 104 (2007), 14553–14558.
50. [50] Hinds, S., Bian, W.N., Dennis, R.G., Bursac, N., The role of extracellular matrix composition in structure and function of bioengineered skeletal muscle. Biomaterials 32 (2011), 3575–3583.
51. [51] Franz, M.R., The electrical restitution curve revisited: steep or flat slope – which is better?. J. Cardiovasc. Electrophysiol. 14 (2003), S140–S147.
52. [52] Bers, D.M., Calcium fluxes involved in control of cardiac myocyte contraction. Circ. Res. 87 (2000), 275–281.
53. [53] Woodworth, R.S., Maximal contraction, “Staircase” contraction, refractory period, and compensatory pause, of the heart. Am. J. Physiol. 8 (1902), 213–248.
54. [54] Szigligeti, P., Pankucsi, C., Banyasz, T., Varro, A., Nanasi, P.P., Action potential duration and force frequency relationship in isolated rabbit, guinea pig and rat cardiac muscle. J. Comp. Physiol. B. 166 (1996), 150–155.
55. [55] Narayan, P., McCune, S.A., Robitaille, P.M.L., Hohl, C.M., Altschuld, R.A., Mechanical alternans and the force-frequency-relationship in failing rat hearts. J. Mol. Cell. Cardiol. 27 (1995), 523–530.
56. [56] Endoh, M., Force-frequency relationship in intact mammalian ventricular myocardium: physiological and pathophysiological relevance. Eur. J. Pharmacol. 500 (2004), 73–86.
57. [57] Redel, A., Baumgartner, W., Golenhofen, K., Drenckhahn, D., Golenhofen, N., Mechanical activity and force-frequency relationship of isolated mouse papillary muscle: effects of extracellular calcium concentration, temperature and contraction type. Pflug. Arch. Eur. J. Phys. 445 (2002), 297–304.
58. [58] Bers, D.M., Control of Cardiac Contraction by SR and Sarcolemmal Ca Fluxes. Excitation-Contraction Coupling and Cardiac Contractile Force. 2001, Kluwer Academic Publishers, Norwell, 245–272.
59. [59] Ponten, A., Li, X.R., Thoren, P., Aase, K., Sjoblom, T., Ostman, A., Eriksson, U., Transgenic overexpression of platelet-derived growth factor-C in the mouse heart induces cardiac fibrosis, hypertrophy, and dilated cardiomyopathy. Am. J. Pathol. 163 (2003), 673–682.
60. [60] Nagueh, S.F., Shah, G., Wu, Y.M., Torre-Amione, G., King, N.M.P., Lahmers, S., Witt, C.C., Becker, K., Labeit, S., Granzier, H.L., Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 110 (2004), 155–162.
61. [61] Berry, M.F., Engler, A.J., Woo, Y.J., Pirolli, T.J., Bish, L.T., Jayasankar, V., Morine, K.J., Gardner, T.J., Discher, D.E., Sweeney, H.L., Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Physiol. Heart 290 (2006), H2196–H2203.
62. [62] Jacot, J.G., McCulloch, A.D., Omens, J.H., Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys. J. 95 (2008), 3479–3487.
63. [63] Engler, A.J., Carag-Krieger, C., Johnson, C.P., Raab, M., Tang, H.Y., Speicher, D.W., Sanger, J.W., Sanger, J.M., Discher, D.E., Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J. Cell Sci. 121 (2008), 3794–3802.
64. [64] Bajaj, P., Tang, X., Saif, T.A., Bashir, R., Stiffness of the substrate influences the phenotype of embryonic chicken cardiac myocytes. J. Biomed. Mater. Res. A 95A (2010), 1261–1269.
65. [65] Bhana, B., Iyer, R.K., Chen, W.L.K., Zhao, R., Sider, K.L., Likhitpanichkul, M., Simmons, C.A., Radisic, M., Influence of substrate stiffness on the phenotype of heart cells. Biotechnol. Bioeng. 105 (2010), 1148–1160.
66. [66] 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.
67. [67] King, N.M.P., Methawasin, M., Nedrud, J., Harrell, N., Chung, C.S., Helmes, M., Granzier, H., Mouse intact cardiac myocyte mechanics: cross-bridge and titin-based stress in unactivated cells. J. Gen. Physiol. 137 (2011), 81–91.
68. [68] Bers, D.M., Cardiac excitation-contraction coupling. Nature 415 (2002), 198–205.
69. [69] Sidorov, V.Y., Holcomb, M.R., Woods, M.C., Gray, R.A., Wikswo, J.P., Effects of unipolar stimulation on voltage and calcium distributions in the isolated rabbit heart. Basic Res. Cardiol. 103 (2008), 537–551.
70. [70] Eklund, S.E., Thompson, R.G., Snider, R.M., Carney, C.K., Wright, D.W., Wikswo, J., Cliffel, D.E., Metabolic discrimination of select list agents by monitoring cellular responses in a multianalyte microphysiometer. Sensors 9 (2009), 2117–2133.
71. [71] Enders, J.R., Marasco, C.C., Kole, A., Nguyen, B., Sundarapandian, S., Seale, K.T., Wikswo, J.P., McLean, J.A., Towards monitoring real-time cellular response using an integrated microfluidics-MALDI/NESI-ion mobility-mass spectrometry platform. IET Syst. Biol. 4 (2010), 416–427.