Design and validation of a bioreactor for simulating the cardiac niche: A system incorporating cyclic stretch, electrical stimulation, and constant perfusion

Tissue Engineering - Part A

Volumn 19, Issue 3-4, 2013, Pages 403-414

  Lu, Liang ^a   Mende, Matthias ^a   Yang, Xuegeng ^b   Körber, Heinz Felix ^c   Schnittler, Hans Joachim ^b   Weinert, Sönke ^d   Heubach, Jürgen ^a   Werner, Carsten ^e   Ravens, Ursula ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c FORTECH UG   (Germany)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

^e LEIBNIZ INSTITUTE OF POLYMER RESEARCH DRESDEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCOMPATIBILITY; BROMINE COMPOUNDS; CELL CULTURE; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; ENDOTHELIAL CELLS; FIBROBLASTS;

BIOREACTOR SYSTEM; CARBON ELECTRODE; CARDIAC CELL; CELL CULTURE SUBSTRATE; CORROSIVE REACTIONS; CYCLIC STRETCH; CYTOTOXICITY ASSAYS; DEFORMATION ANALYSIS; ELECTRICAL STIMULATION SYSTEM; ELECTRICAL STIMULATIONS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; INPUT VOLTAGES; NOVEL DEVICES; PULSE DURATIONS; SURFACE STRAINS; VENTRICULAR MYOCYTES;

BIOREACTORS;

RATTUS;

ACTION POTENTIAL; ANIMAL; ARTICLE; BATCH CELL CULTURE; BIOREACTOR; CELL CULTURE; ELECTROSTIMULATION; EQUIPMENT; EQUIPMENT DESIGN; EQUIPMENT FAILURE; EVALUATION; HEART CONTRACTION; HEART MUSCLE CELL; HUMAN; MALE; MECHANICAL STRESS; MECHANOTRANSDUCTION; PHYSIOLOGY; RAT; STEM CELL NICHE; STIMULATION; TISSUE ENGINEERING; VALIDATION STUDY; WISTAR RAT; YOUNG MODULUS;

ACTION POTENTIALS; ANIMALS; BATCH CELL CULTURE TECHNIQUES; BIOREACTORS; CELLS, CULTURED; ELASTIC MODULUS; ELECTRIC STIMULATION; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; HUMANS; MALE; MECHANOTRANSDUCTION, CELLULAR; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHYSICAL STIMULATION; RATS; RATS, WISTAR; STEM CELL NICHE; STRESS, MECHANICAL; TISSUE ENGINEERING;

MLCS; MLOWN;

EID: 84872098790     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0135     Document Type: Article

References (35)

1. Leychenko, A., Konorev, E., Jijiwa, M., and Matter, M. L. Stretch-induced hypertrophy activates NFkB-mediated VEGF secretion in adult cardiomyocytes. PLos One 6, 2011.
2. Tsai, C.T., Chiang, F.T., Tseng, C.D., Yu, C.C., Wang, Y.C., Lai, L.P., Hwang, J.J., and Lin, J.L. Mechanical stretch of atrial myocyte monolayer decreases sarcoplasmic reticulum calcium adenosine triphosphatase expression and increases susceptibility to repolarization alternans. J Am Coll Cardiol 58, 2106, 2011.
3. Husse, B., Briest, W., Homagk, L., Isenberg, G., and Gekle, M. Cyclical mechanical stretch modulates expression of collagen I and collagen III by PKC and tyrosine kinase in cardiac fibro-blasts. Am J Physiol Regul Integr Comp Physiol 293, R1898,2007.
4. Lee, A.A., Delhaas, T., McCulloch, A.D., and Villarreal, F.J. Differential responses of adult cardiac fibroblasts to in vitro biaxial strain patterns. J Mol Cell Cardiol 31, 1833, 1999.
5. Berger, H.J., Prasad, S.K., Davidoff, A.J., Pimental, D., El-lingsen, O., Marsh, J.D., Smith, T.W., and Kelly, RA. Con-tinual electric-field stimulation preserves contractile function of adult ventricular myocytes in primary culture. Am J Physiol 266, H341, 1994.
6. Holt, E., Lunde, P.K., Sejersted, O.M., and Christensen, G. Electrical stimulation of adult rat cardiomyocytes in culture improves contractile properties and is associated with altered calcium handling. Basic Res Cardiol 92, 289, 1997.
7. Zimmermann, W.H., Melnychenko, I., and Eschenhagen, T. Engineered heart tissue for regeneration of diseased hearts. Biomaterials 25, 1639, 2004.
8. Radisic, M., Park, H., Shing, H., Consi, T., Schoen, F.J., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Func-tional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci U S A 101, 18129, 2004.
9. Feng, Z.G., Matsumoto, T., Nomura, Y., and Nakamura, T. An electro-tensile bioreactor for 3-D culturing of cardio-myocytes - a bioreactor system that simulates the myo-cordium's electrical and mechanical response in vivo. IEEE Eng Med Biol Mag 24, 73, 2005.
10. Carrier, R.L., Rupnick, M., Langer, R., Schoen, F.J., Freed, L.E., and Vunjak-Novakovic, G. Perfusion improves tissue archi-tecture of engineered cardiac muscle. Tissue Eng 8,175, 2002.
11. Radisic, M., Yang, L.M., Boublik, J., Cohen, R.J., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Medium perfusion enables engineering of compact and contractile cardiac tis-sue. Am J Physiol Heart Circ Physiol 286, H507, 2004.
12. Radisic, M., Marsano, A., Maidhof, R., Wang, Y., and Vunjak-Novakovic, G. Cardiac tissue engineering using perfusion bioreactor systems. Nat Protoc 3, 719, 2008.
13. Maidhof, R., Tandon, N., Lee, E.J., Luo, J., Duan, Y., Yeager, K., Konofogou, E., and Vunjak-Novakovic, G. Biomimetic perfusion and electrical stimulation applied in concert im-proved the assembly of engineered cardiac tissue. J Tissue Eng Regen Med 6, e12,2011.
14. Tandon, N., Cannizzaro, C., Chao, P.H.G., Maidhof, R., Marsano, A., Au, H.T.H., Radisic, M., and Vunjak-Nova-kovic, G. Electrical stimulation systems for cardiac tissue engineering. Nat Protoc 4, 155, 2009.
15. Tandon, N., Marsano, A., Maidhof, R., Wan, L., Park, H., and Vunjak-Novakovic, G. Optimization of electrical stim-ulation parameters for cardiac tissue engineering. J Tissue Eng Regen Med 5, E115, 2011.
16. Merrill, D.R., Bikson, M., and Jefferys, J.G.R. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosci Methods 141, 171, 2005.
17. Tandon, N., Cannizzaro, C., Figallo, E., Voldman, J., and Vunjak-Novakovic, G. Characterization of electrical stimulation electrodes for cardiac tissue engineering. Abstract presented at the Proceedings of the 28th IEEE EMBS Annual International Conference, New York City, 2006. Abstract no. 259747.
18. Schnittler, H.J., Franke, R.P., Akbay, U., Mrowietz, C., and Drenckhahn, D. Improved in-vitro rheological system for studying the effect of fluid shear-stress on cultured-cells. Am J Phys 265, C289, 1993.
19. Villarreal, F.J., Bahnson, T., and Kim, NN. Human cardiac fibroblasts and receptors for angiotensin II and bradykinin: a potential role for bradykinin in the modulation of cardiac extracellular matrix. Basic Res Cardiol 93, 4, 1998.
20. Christ, T., Wettwer, E., Dobrev, D., Adolph, E., Knaut, M., Wallukat, G., and Ravens, U. Autoantibodies against the beta(1)-adrenoceptor from patients with dilated cardiomyo-pathy prolong action potential duration and enhance con-tractility in isolated cardiomyocytes. J Mol Cell Cardiol 33, 1515, 2001.
21. Neidlinger-Wilke, C., Grood, E., Claes, L., and Brand, R. Fibroblast orientation to stretch begins within three hours. J Orthop Res 20, 953, 2002.
22. Berry, J.L., Steen, J.A., Williams, J.K., Jordan, J.E., Atala, A., and Yoo, J.J. Bioreactors for development of tissue en-gineered heart valves. Ann Biomed Eng 38, 3272, 2010.
23. Gandaglia, A., Bagno, A., Naso, F., Spina, M., and Gerosa, G. Cells, scaffolds and bioreactors for tissue-engineered heart valves: a journey from basic concepts to contemporary de-velopmental innovations. Eur J Cardiothorac Surg 39, 523, 2011.
24. Colombo, A., Cahill, P.A., and Lally, C. An analysis of the strain field in biaxial Flexcell membranes for different wave-forms and frequencies. Proc Inst Mech Eng H 222,1235,2008.
25. Boerboom, R.A., Rubbens, M.P., Driessen, N.J.B., Bouten, CV.C., and Baaijens, F.P.T. Effect of strain magnitude on the tissue properties of engineered cardiovascular constructs. Ann Biomed Eng 36, 244, 2008.
26. Tulloch, N.L., Muskheli, V., Razumova, M.V., Korte, F.S., Regnier, M., Hauch, K.D., Pabon, L., Reinecke, H., and Murry, C.E. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res 109, 47, 2011.
27. Caspi, O., Lesman, A., Basevitch, Y., Gepstein, A., Arbel, G., Huber, I., Habib, M., Gepstein, L., and Levenberg, S. Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 100, 263, 2007.
28. Radisic, M., Park, H., Martens, T.P., Salazar-Lazaro, J.E., Geng, W.L., Wang, Y.D., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Pre-treatment of synthetic elastomeric scaffolds by cardiac fibroblasts improves engineered heart tissue. J Biomed Mater Res A 86A, 713, 2008.
29. Yang, G.G., Crawford, R.C., and Wang, J.H.C. Proliferation and collagen production of human patellar tendon fibro-blasts in response to cyclic uniaxial stretching in serum-free conditions. J Biomech 37, 1543, 2004.
30. Wang, J.H.C., and Grood, E.S. The strain magnitude and contact guidance determine orientation response of fibroblasts to cyclic substrate strains. Connect Tissue Res 41,29,2000.
31. Wang, J.H.C. Substrate deformation determines actin cyto-skeleton reorganization: a mathematical modeling and ex-perimental study. J Theor Biol 202, 33, 2000.
32. Wang, J.H.C., Goldschmidt-Clermont, P., Wille, J., and Yin, F.C.P. Specificity of endothelial cell reorientation in response to cyclic mechanical stretching. J Biomech 34, 1563, 2001.
33. Zhou, J.W., Ellis, A.V., and Voelcker, N.H. Recent develop-ments in PDMS surface modification for microfluidic de-vices. Electrophoresis 31, 2, 2010.
34. Bokenes, J., Sjaastad, I., and Sejersted, O.M. Artifactual contractions triggered by field stimulation of cardiomyo-cytes. J Appl Physiol 98, 1712, 2005.
35. Zimmermann, W.H., Schneiderbanger, K., Schubert, P., Di-die, M., Munzel, F., Heubach, J.F., Kostin, S., Neuhuber, W.L., and Eschenhagen, T. Tissue engineering of a differ-entiated cardiac muscle construct. Circ Res 90, 223, 2002.