Three-dimensional culture alters primary cardiac cell phenotype

Tissue Engineering - Part A

Volumn 16, Issue 2, 2010, Pages 629-641

  Akins, Robert E ^a   Rockwood, Danielle ^a,b   Robinson, Karyn G ^a   Sandusky, Daniel ^a   Rabolt, John ^b   Pizarro, Christian ^a  

^a NEMOURS ALFRED I DUPONT HOSPITAL FOR CHILDREN   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIALS; CELL CULTURE; CELL PROLIFERATION; ENDOTHELIAL CELLS; GENE EXPRESSION; GENE EXPRESSION REGULATION; HEART; TISSUE ENGINEERING;

3D MODELS; 3D STRUCTURE; CARDIAC CELL; CELL DISTRIBUTION; CELL PHENOTYPE; CELL POPULATIONS; CELLULAR PHENOTYPES; CELLULAR STRUCTURE; EXPRESSION PROFILE; GROWTH OF CELLS; IODOTHYRONINE; MRNA EXPRESSION; RE-AGGREGATION; REGENERATIVE MEDICINE; SERUM-FREE MEDIUM; TARGET ORGANS; THREE-DIMENSIONAL (3D); THREE-DIMENSIONAL CULTURE; TISSUE ARCHITECTURE; TISSUE FORMATION; UP-REGULATION; VENTRICULAR CELLS;

THREE DIMENSIONAL;

BIOLOGICAL MARKER; LIOTHYRONINE;

ANIMAL; ARTICLE; CELL ADHESION; CELL AGGREGATION; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CELL PROLIFERATION; CELL SHAPE; CLUSTER ANALYSIS; CULTURE MEDIUM; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECT; ENDOTHELIUM CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HEART MUSCLE; HEART VENTRICLE; METABOLISM; METHODOLOGY; MUSCLE; NEWBORN; PHENOTYPE; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; CELL ADHESION; CELL AGGREGATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; CLUSTER ANALYSIS; CULTURE MEDIA, SERUM-FREE; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEART VENTRICLES; MUSCLES; MYOCARDIUM; PHENOTYPE; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRIIODOTHYRONINE;

EID: 77049106144     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0458     Document Type: Conference Paper

References (67)

1. Jakab, K., Norotte, C., Damon, B., Marga, F., Neagu, A., Besch-Williford, C.L., Kachurin, A., Church, K.H., Park, H., Mironov, V., Markwald, R., Vunjak-Novakovic, G., and Forgacs, G. Tissue engineering by self-assembly of cells printed into topologically defined structures. Tissue Eng Part A 14, 413, 2008.
2. Yildirim, Y., Naito, H., Didie, M., Karikkineth, B.C., Biermann, D., Eschenhagen, T., and Zimmermann, W.H. Development of a biological ventricular assist device: preliminary data from a small animal model. Circulation 116, I16, 2007.
3. Masuda, S., Shimizu, T., Yamato, M., and Okano, T. Cell sheet engineering for heart tissue repair. Adv Drug Deliv Rev 60, 277, 2008.
4. Sekine, H., Shimizu, T., Hobo, K., Sekiya, S., Yang, J., Yamato, M., Kurosawa, H., Kobayashi, E., and Okano, T. Endothelial cell coculture within tissue-engineered cardio-myocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 118, S145, 2008.
5. Akins, R., Gratton, K., Quezada, E., Rutter, H., Tsuda, T., and Soteropoulos, P. Gene expression profile of bioreactor-cultured cardiac cells: activation of morphogenetic pathways for tissue engineering. DNA Cell Biol 26, 425, 2007.
6. Akins, R.E., Boyce, R.A., Madonna, M.L., Schroedl, N.A., Gonda, S.R., McLaughlin, T.A., and Hartzell, C.R. Cardiac organogenesis in vitro: reestablishment of three-dimensional tissue architecture by dissociated neonatal rat ventricular cells. Tissue Eng Part A 5, 103, 1999.
7. Baar, K., Birla, R., Boluyt, M.O., Borschel, G.H., Arruda, E.M., and Dennis, R.G. Self-organization of rat cardiac cells into contractile 3-D cardiac tissue. FASEB J 19, 275, 2005.
8. Birla, R.K., Borschel, G.H., and Dennis, R.G. In vivo conditioning of tissue-engineered heart muscle improves contractile performance. Artif Organs 29, 866, 2005.
9. Birla, R.K., Borschel, G.H., Dennis, R.G., and Brown, D.L. Myocardial engineering in vivo: formation and characterization of contractile, vascularized three-dimensional cardiac tissue. Tissue Eng 11, 803, 2005.
10. Just, L., Kursten, A., Borth-Bruhns, T., Lindenmaier, W., Rohde, M., Dittmar, K., and Bader, A. Formation of three-dimensional fetal myocardial tissue cultures from rat for long-term cultivation. Dev Dyn 235, 2200, 2006.
11. Kelm, J.M., Ehler, E., Nielsen, L.K., Schlatter, S., Perriard, J.C., and Fussenegger, M. Design of artificial myocardial microtissues. Tissue Eng 10, 201, 2004.
12. Watzka, S.B., Steiner, M., Samorapoompichit, P., Gross, K., Coles, J.G., Wolner, E., and Weigel, G. Establishment of vessel-like structures in long-term three-dimensional tissue culture of myocardium: an electron microscopy study. Tissue Eng 10, 1684, 2004.
13. Griffith, L.G., and Swartz, M.A. Capturing complex 3D tissue physiology in vitro. Nat Rev 7, 211, 2006.
14. Lee, G.Y., Kenny, P.A., Lee, E.H., and Bissell, M.J. Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 4, 359, 2007.
15. Harding, S.E., Davies, C.H., Wynne, D.G., and Poole-Wilson, P.A. Contractile function and response to agonists in myo-cytes from failing human heart. Eur Heart J 15 Suppl D, 35, 1994.
16. Wollenberger, A. Isolated heart cells as a model of the myocardium. Basic Res Cardiol 80 Suppl 2, 9, 1985.
17. Speicher, D.W., Peace, J.N., and McCarl, R.L. Effects of plating density and age in culture on growth and cell division of neonatal rat heart primary cultures. In Vitro 17, 863, 1981.
18. Millart, H., and Seraydarian, M.W. Influence of plating density on individual cell growth, cell division and differentiation of neonatal rat heart primary cultures. Tissue Cell 18, 209, 1986.
19. Akins, R.E. Cardiac tissue. In: Atala, A., and Lanza, R., eds. Methods of Tissue Engineering. San Diego, CA: Academic Press, 2002, pp. 915-925.
20. Vunjak-Novakovic, G. Cardiac tissue engineering: effects of bioreactor flow environment on tissue constructs. J Chem Technol Biotechnol 81, 485, 2006.
21. Akins, R., McLaughlin, T., Boyce, B., Gilmour, L., and Gratton, K. Exogenous metalloporphyrins alter the organization and function of cultured neonatal rat heart cells via modulation of heme oxygenase activity. J Cell Physiol 201, 26, 2004.
22. Holshek, J., and Akins, R. Acetonitrile is better than ethanol as a dehydrating agent for cells prepared for SEM. Proc Microsc Soc Am 52, 324, 1994.
23. Akins, R., Schroedl, N., Gonda, S., and Hartzell, C. Neonatal rat heart cells cultured in simulated microgravity. In Vitro Cell Dev Biol Anim 33, 337, 1997.
24. Schroedl, N.A., Bacon, C.R., Huang, Y.C., and Hartzell, C.R. Protein metabolism during nutrient deprivation and re-feeding of neonatal heart cells. Am J Physiol 257 (5 Pt 1), C913, 1989.
25. Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kos-tukovich, E., Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., and Quackenbush, J. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374, 2003.
26. Rockwood, D.N., Akins, R.E., Jr., Parrag, I.C., Woodhouse, K.A., and Rabolt, J.F. Culture on electrospun polyurethane scaffolds decreases atrial natriuretic peptide expression by cardiomyocytes in vitro. Biomaterials 29, 4783, 2008.
27. Zou, Y., Evans, S., Chen, J., Kuo, H.C., Harvey, R.P., and Chien, K.R. CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. Development 124, 793, 1997.
28. Sperelakis, N. Cultured heart cell reaggregate model for studying cardiac toxicology. Environ Health Perspect 26, 243, 1978.
29. Kasten, F.H. Rat myocardial cells in vitro: mitosis and differentiated properties. In Vitro 8, 128, 1972.
30. Polinger, I.S. Separation of cell types in embryonic heart cell cultures. Exp Cell Res 63, 78, 1970.
31. Gharaibeh, B., Lu, A., Tebbets, J., Zheng, B., Feduska, J., Crisan, M., Peault, B., Cummins, J., and Huard, J. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Prot 3, 1501, 2008.
32. Rando, T.A., and Blau, H.M. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J Cell Biol 125, 1275, 1994.
33. Richler, C., and Yaffe, D. The in vitro cultivation and differentiation capacities of myogenic cell lines. Dev Biol 23, 1, 1970.
34. Benezra, R., Rafii, S., and Lyden, D. The Id proteins and angiogenesis. Oncogene 20, 8334, 2001.
35. Glienke, J., Schmitt, A.O., Pilarsky, C., Hinzmann, B., Weiss, B., Rosenthal, A., and Thierauch, K.H. Differential gene expression by endothelial cells in distinct angiogenic states. Eur J Biochem 267, 2820, 2000.
36. Valdimarsdottir, G., Goumans, M.J., Rosendahl, A., Brug-man, M., Itoh, S., Lebrin, F., Sideras, P., and ten Dijke, P. Stimulation of Id1 expression by bone morphogenetic protein is sufficient and necessary for bone morphogenetic protein-induced activation of endothelial cells. Circulation 106, 2263, 2002.
37. van Wijk, B., Moorman, A.F., and van den Hoff, M.J. Role of bone morphogenetic proteins in cardiac differentiation. Cardiovasc Res 74, 244, 2007.
38. Bhattacharya, S., Macdonald, S.T., and Farthing, C.R. Molecular mechanisms controlling the coupled development of myocardium and coronary vasculature. Clin Sci (Lond) 111, 35, 2006.
39. Tirziu, D., Chorianopoulos, E., Moodie, K.L., Palac, R.T., Zhuang, Z.W., Tjwa, M., Roncal, C., Eriksson, U., Fu, Q., Elfenbein, A., Hall, A.E., Carmeliet, P., Moons, L., and Simons, M. Myocardial hypertrophy in the absence of external stimuli is induced by angiogenesis in mice. J Clin Investig 117, 3188, 2007.
40. Tirziu, D., and Simons, M. Endothelium as master regulator of organ development and growth. Vasc Pharm 50, 1, 2008.
41. Bloch, K.D., Seidman, J.G., Naftilan, J.D., Fallon, J.T., and Seidman, C.E. Neonatal atria and ventricles secrete atrial natriuretic factor via tissue-specific secretory pathways. Cell 47, 695, 1986.
42. Irons, C.E., Sei, C.A., and Glembotski, C.C. Regulated secretion of atrial natriuretic factor from cultured ventricular myocytes. Am J Physiol 257 (5 Pt 1), C913, 1989.
43. Jeyaseelan, R., Poizat, C., Baker, R.K., Abdishoo, S., Ister-abadi, L.B., Lyons, G.E., and Kedes, L. A novel cardiac-restricted target for doxorubicin. CARP, a nuclear modulator of gene expression in cardiac progenitor cells and cardio-myocytes. J Biol Chem 272, 22800, 1997.
44. Kuo, H., Chen, J., Ruiz-Lozano, P., Zou, Y., Nemer, M., and Chien, K.R. Control of segmental expression of the cardiac-restricted ankyrin repeat protein gene by distinct regulatory pathways in murine cardiogenesis. Development 126, 4223, 1999.
45. Wei, Y.J., Cui, C.J., Huang, Y.X., Zhang, X.L., Zhang, H., and Hu, S.S. Upregulated expression of cardiac ankyrin repeat protein in human failing hearts due to arrhythmogenic right ventricular cardiomyopathy. Eur J Heart Fail 11, 559, 2009.
46. Zolk, O., Frohme, M., Maurer, A., Kluxen, F.W., Hentsch, B., Zubakov, D., Hoheisel, J.D., Zucker, I.H., Pepe, S., and Es-chenhagen, T. Cardiac ankyrin repeat protein, a negative regulator of cardiac gene expression, is augmented in human heart failure. Biochem Biophys Res Commun 293, 1377, 2002.
47. Armstrong, M.T., Lee, D.Y., and Armstrong, P.B. Regulation of proliferation of the fetal myocardium. Dev Dyn 219, 226, 2000.
48. Chizzonite, R.A., and Zak, R. Regulation of myosin isoen-zyme composition in fetal and neonatal rat ventricle by endogenous thyroid hormones. J Biol Chem 259, 12628, 1984.
49. Dillmann, W.H., Rohrer, D., Popovich, B., and Barrieux, A. Thyroid hormone induced changes in cardiac proteins and mRNAs. Horm Metab Res Suppl 17, 26, 1987.
50. Andries, L.J., Sys, S.U., and Brutsaert, D.L. Morphor-egulatory interactions of endocardial endothelium and extracellular material in the heart. Herz 20, 135, 1995.
51. Yamazaki, T., Komuro, I., Kudoh, S., Zou, Y., Shiojima, I., Hiroi, Y., Mizuno, T., Maemura, K., Kurihara, H., Aikawa, R., Takano, H., and Yazaki, Y. Endothelin-1 is involved in mechanical stress-induced cardiomyocyte hypertrophy. J Biol Chem 271, 3221-3228, 1996. (Pubitemid 26055625)
52. Swynghedauw, B. Developmental and functional adaptation of contractile proteins in cardiac and skeletal muscles. Phy-siol Rev 66, 710, 1986.
53. Sadoshima, J., and Izumo, S. Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes: potential involvement of an autocrine=paracrine mechanism. EMBO J 12, 1681, 1993.
54. Dzau, V.J. The role of mechanical and humoral factors in growth regulation of vascular smooth muscle and cardiac myocytes. Curr Opin Nephrol Hypertens 2, 27, 1993.
55. Goodwin, T.J., Prewett, T.L., Wolf, D.A., and Spaulding, G.F. Reduced shear stress: a major component in the ability of mammalian tissues to form three-dimensional assemblies in simulated microgravity. J Cell Biochem 51, 301, 1993.
56. Hammond, T.G., and Hammond, J.M. Optimized suspension culture: the rotating-wall vessel. Am J Physiol 281, F12, 2001.
57. Csiszar, A., Labinskyy, N., Smith, K.E., Rivera, A., Bakker, E.N., Jo, H., Gardner, J., Orosz, Z., and Ungvari, Z. Down-regulation of bone morphogenetic protein 4 expression in coronary arterial endothelial cells: role of shear stress and the cAMP=protein kinase A pathway. Arterioscler Thromb Vasc Biol 27, 776, 2007.
58. Bartman, T., Walsh, E.C., Wen, K.K., McKane, M., Ren, J., Alexander, J., Rubenstein, P.A., and Stainier, D.Y. Early myocardial function affects endocardial cushion development in zebrafish. PLoS Biol 2, E129, 2004.
59. Dennis, G., Jr., Sherman, B.T., Hosack, D.A., Yang, J., Gao, W., Lane, H.C., and Lempicki, R.A. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 4, P3, 2003.
60. Huang da, W., Sherman, B.T., and Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Prot 4, 44, 2009.
61. Pandey, K.N. Biology of natriuretic peptides and their receptors. Peptides 26, 901, 2005.
62. McGrath, M.F., and de Bold, A.J. Determinants of natriuretic peptide gene expression. Peptides 26, 933, 2005.
63. Arber, S., Hunter, J.J., Ross, J., Jr., Hongo, M., Sansig, G., Borg, J., Perriard, J.C., Chien, K.R., and Caroni, P. MLP-deficient mice exhibit a disruption of cardiac cytoarchi-tectural organization, dilated cardiomyopathy, and heart failure. Cell 88, 393, 1997.
64. Xin, M., Small, E.M., van Rooij, E., Qi, X., Richardson, J.A., Srivastava, D., Nakagawa, O., and Olson, E.N. Essential roles of the bHLH transcription factor Hrt2 in repression of atrial gene expression and maintenance of postnatal cardiac function. Proc Natl Acad Sci USA 104, 7975, 2007.
65. Koibuchi, N., and Chin, M.T. CHF1=Hey2 plays a pivotal role in left ventricular maturation through suppression of ectopic atrial gene expression. Circ Res 100, 850, 2007.
66. Mikhailov, A.T., and Torrado, M. The enigmatic role of the ankyrin repeat domain 1 gene in heart development and disease. Int J Dev Biol 52, 811, 2008.
67. Haddad, F., Qin, A.X., Bodell, P.W., Jiang, W., Giger, J.M., and Baldwin, K.M. Intergenic transcription and developmental regulation of cardiac myosin heavy chain genes. Am J Physiol. 257 (5 Pt 1), C913, 1989.