Hypertrophic phenotype in cardiac cell assemblies solely by structural cues and ensuing self-organization

FASEB Journal

Volumn 25, Issue 3, 2011, Pages 851-862

  Chung, Chiung Yin ^a   Bien, Harold ^a   Sobie, Eric A ^c   Dasari, Vikram ^a   McKinnon, David ^b   Rosati, Barbara ^b   Entcheva, Emilia ^a,b  

^a St Francis Hospital The Heart Center   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiomyocytes; Cell culture; Electrophysiology; Natriuretic peptides

Indexed keywords

ATRIAL NATRIURETIC FACTOR; ATRIAL NATRIURETIC FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL NUCLEUS; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; EXCITATION CONTRACTION COUPLING; GAP JUNCTION; GENE EXPRESSION; HEART ELECTROPHYSIOLOGY; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; MECHANICAL STRESS; MULTINUCLEAR CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; ATRIAL NATRIURETIC FACTOR; CARDIOMEGALY; CELL ADHESION; CELL SHAPE; CELLS, CULTURED; ELECTRIC STIMULATION; GENETIC MARKERS; MECHANOTRANSDUCTION, CELLULAR; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; NATRIURETIC PEPTIDE, BRAIN; PHENOTYPE; PHYSICAL STIMULATION; RATS; SIGNAL TRANSDUCTION; STIMULATION, CHEMICAL; TISSUE SCAFFOLDS;

RATTUS;

EID: 79954615188     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-168625     Document Type: Article

References (61)

1. Engler, A. J., Sen, S., Sweeney, H. L., and Discher, D. E. (2006) Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (Pubitemid 44233625)
2. Rosenberg, S. S., Kelland, E. E., Tokar, E., De la Torre, A. R., and Chan, J. R. (2008) The geometric and spatial constraints of the microenvironment induce oligodendrocyte differentiation. Proc. Natl. Acad. Sci. U. S. A. 105, 14662-14667
3. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M., and Ingber, D. E. (1997) Geometric control of cell life and death. Science 276, 1425-1428 (Pubitemid 27235413)
4. Geiger, B. (2001) Cell biology. Encounters in space. Science 294, 1661-1663
5. Folch, A., and Toner, M. (2000) Microengineering of cellular interactions. Annu. Rev. Biomed. Eng. 2, 227-256
6. Balaban, N. Q., Schwarz, U. S., Riveline, D., Goichberg, P., Tzur, G., Sabanay, I., Mahalu, D., Safran, S., Bershadsky, A., Addadi, L., and Geiger, B. (2001) Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3, 466-472 (Pubitemid 32422082)
7. Swynghedauw, B. (1999) Molecular mechanisms of myocardial remodeling. Physiol. Rev. 79, 215-262 (Pubitemid 29056953)
8. Hardt, S. E., and Sadoshima, J. (2004) Negative regulators of cardiac hypertrophy. Cardiovasc. Res. 63, 500-509 (Pubitemid 38970194)
9. Tomaselli, G. F., and Marban, E. (1999) Electrophysiological remodeling in hypertrophy and heart failure. Cardiovasc. Res. 42, 270-283 (Pubitemid 29243156)
10. Hill, J. A. (2003) Electrical remodeling in cardiac hypertrophy. Trends Cardiovasc. Med. 13, 316-322 (Pubitemid 37338563)
11. Wolk, R. (2000) Arrhythmogenic mechanisms in left ventricular hypertrophy. Europace 2, 216-223
12. Cadre, B. M., Qi, M., Eble, D. M., Shannon, T. R., Bers, D. M., and Samarel, A. M. (1998) Cyclic stretch down-regulates calcium transporter gene expression in neonatal rat ventricular myocytes. J. Mol. Cell. Cardiol. 30, 2247-2259 (Pubitemid 28549977)
13. McDonough, P. M., and Glembotski, C. C. (1992) Induction of atrial natriuretic factor and myosin light chain-2 gene expression in cultured ventricular myocytes by electrical stimulation of contraction. J. Biol. Chem. 267, 11665-11668
14. 2+-dependent calcineurin activation in mechanical stretch-induced hypertrophy. Cardiology 107, 281-290 (Pubitemid 46788245)
15. Horio, T., Nishikimi, T., Yoshihara, F., Matsuo, H., Takishita, S., and Kangawa, K. (2000) Inhibitory regulation of hypertrophy by endogenous atrial natriuretic peptide in cultured cardiac myocytes. Hypertension 35, 19-24 (Pubitemid 30054231)
16. Entcheva, E., and Bien, H. (2003) Tension development and nuclear eccentricity in topographically controlled cardiac syncytium. J. Biomed. Microdev. 5, 163-168 (Pubitemid 36986748)
17. Bien, H., Yin, L., and Entcheva, E. (2003) Cardiac cell networks on elastic microgrooved scaffolds. IEEE Eng. Med. Biol. Mag. 22, 108-112 (Pubitemid 38005038)
18. Yin, L., Bien, H., and Entcheva, E. (2004) Scaffold topography alters intracellular calcium dynamics in cultured cardiomyocyte networks. Am. J. Physiol. Heart Circ. Physiol. 287, H1276-H1285 (Pubitemid 39096677)
19. Entcheva, E., and Bien, H. (2005) Acoustic micromachining of three-dimensional surfaces for biological applications. Lab Chip 5, 179-183 (Pubitemid 40260860)
20. Dunn, A. K., Smithpeter, C, Welch, A. J., and Richards-Kortum, R (1996) Sources of contrast in confocal reflectance imaging. Applied Optics 35, 3441-3446 (Pubitemid 126622157)
21. Chung, C. Y, Bien, H., and Entcheva, E. (2007) The role of cardiac tissue alignment in modulating electrical function. J. Cardiovasc. Electrophysiol. 18, 1323-1329 (Pubitemid 350115781)
22. Bien, H., Yin, L., and Entcheva, E. (2006) Calcium instabilities in mammalian cardiomyocyte networks. Biophys. J. 90, 2628-2640
23. Bay, B. K. (1995) Texture correlation: a method for the measurement of detailed strain distributions within trabecular bone. J. Orthop. Res. 13, 258-267
24. Lau, Y. H., Braun, M., and Hutton, B. F. (2001) Non-rigid image registration using a median-filtered coarse-to-fine displacement field and a symmetric correlation ratio. Phys. Med. Biol. 46, 1297-1319 (Pubitemid 32366619)
25. Sobie, E. A. (2009) Parameter sensitivity analysis in electrophysiological models using multivariable regression. Biophys. J. 96, 1264-1274
26. Geladi, P., and Kowalski, B. R. (1986) Partial least-squares regression: a tutorial. Analyt. Chim. Acta 185, 1-17
27. Zhuang, J., Yamada, K. A., Saffitz, J. E., and Kleber, A. G. (2000) Pulsatile stretch remodels cell-to-cell communication in cultured myocytes. Circ. Res. 87, 316-322 (Pubitemid 30655973)
28. Anversa, P., Olivetti, G., and Loud, A. V. (1980) Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. I. Hypertrophy, hyperplasia, and binucleation of myocytes. Circ. Res. 46, 495-502 (Pubitemid 10107370)
29. Ahuja, P., Sdek, P., and MacLellan, W. R. (2007) Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol. Rev. 87, 521-544 (Pubitemid 47086282)
30. Lalevee, N., Rebsamen, M. C., Barrere-Lemaire, S., Perrier, E., Nargeot, J., Benitah, J. P., and Rossier, M. F. (2005) Aldosterone increases T-type calcium channel expression and in vitro beating frequency in neonatal rat cardiomyocytes. Cardiovasc. Res. 67, 216-224 (Pubitemid 40943614)
31. + currents via transcriptional up-regulation of Kv4.2 channel subunits. J. Biol. Chem. 281, 38498-38506 (Pubitemid 46041974)
32. Gaughan, J. P., Hefner, C. A., and Houser, S. R. (1998) Electrophysiological properties of neonatal rat ventricular myocytes with alpha-adrenergic-induced hypertrophy. Am. J. Physiol. 275, 577-590
33. Walsh, K. B., Sweet, J. K., Parks, G. E., and Long, K. J. (2001) Modulation of outward potassium currents in aligned cultures of neonatal rat ventricular myocytes during phorbol esterinduced hypertrophy. J. Mol. Cell. Cardiol. 33, 1233-1247 (Pubitemid 32579288)
34. Strait, J. B., and Samarel, A. M. (2000) Isoenzyme-specific protein kinase C and c-Jun. N-terminal kinase activation by electrically stimulated contraction of neonatal rat ventricular myocytes. J. Mol. Cell. Cardiol. 32, 1553-1566
35. Makhlouf, A. A., and McDermott, P. J. (1998) Increased expression of eukaryotic initiation factor 4E during growth of neonatal rat cardiocytes in vitro. Am. J. Physiol. Heart Circ. Physiol. 274, H2133-H2142
36. Adachi, S., Ito, H., Ohta, Y., Tanaka, M., Ishiyama, S., Nagata, M., Toyozaki, T., Hirata, Y, Marumo, F., and Hiroe, M. (1995) Distribution of mRNAs for natriuretic peptides in RV hypertrophy after pulmonary arterial banding. Am. J. Physiol. Heart Circ. Physiol. 268, H162-H169
37. Kinnunen, P., Taskinen, T., Leppaluoto, J., and Ruskoaho, H. (1990) Release of atrial natriuretic peptide from rat myocardium in vitro: effect of minoxidil-induced hypertrophy. Br. J. Pharmacol. 99, 701-708 (Pubitemid 20111309)
38. Koyanagi, T., Wong, L. Y., Inagaki, K., Petrauskene, O. V., and Mochly-Rosen, D. (2008) Alteration of gene expression during progression of hypertension-induced cardiac dysfunction in rats. Am. J. Physiol. Heart Circ. Physiol. 295, H220-H226
39. Bodi, I., Muth, J. N., Hahn, H. S., Petrashevskaya, N. N., Rubio, M., Koch, S. E., Varadi, G., and Schwartz, A. (2003) Electrical remodeling in hearts from a calcium-dependent mouse model of hypertrophy and failure: complex nature of K+ current changes and action potential duration. J. Am. Coll. Cardiol. 41, 1611-1622 (Pubitemid 36543383)
40. + channel genes in left ventricular remodeled myocardium after experimental myocardial infarction. Circ. Res. 79, 669-675 (Pubitemid 26317814)
41. + channels in the rat. Mol. Cell. Biochem. 237, 1-10 (Pubitemid 34965787)
42. + current in spontaneously hypertensive rats. Cardiovasc. Res. 74, 85-95 (Pubitemid 46366947)
43. Zhang, T. T., Cui, B., and Dai, D. Z. (2004) Downregulation of Kv4.2 and Kv4.3 channel gene expression in right ventricular hypertrophy induced by monocrotaline in rat. Acta Pharmacol. Sin. 25, 226-230 (Pubitemid 38186175)
44. Lee, J. K., Nishiyama, A., Kambe, F., Seo, H., Takeuchi, S., Kamiya, K, Kodama, I., and Toyama, J. (1999) Downregulation of voltagegated K+ channels in rat heart with right ventricular hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 277, H1725-H1731
45. Wang, Z., Kutschke, W., Richardson, K. E., Karimi, M., and Hill, J. A. (2001) Electrical remodeling in pressure-overload cardiac hypertrophy: role of calcineurin. Circulation 104, 1657-1663 (Pubitemid 32947530)
46. Domenighetti, A. A., Boixel, C, Cefai, D., Abriel, H., and Pedrazzini, T. (2007) Chronic angiotensin II stimulation in the heart produces an acquired long QT syndrome associated with IK1 potassium current downregulation. J. Mol. Cell. Cardiol. 42, 63-70 (Pubitemid 44958628)
47. Shi, W., Wymore, R., Yu, H., Wu, J., Wymore, R. T., Pan, Z., Robinson, R. B., Dixon, J. E., McKinnon, D., and Cohen, I. S. (1999) Distribution and prevalence of hyperpolarization-activated cation channel (HCN) mRNA expression in cardiac tissues. Circ. Res. 85, e1-e6
48. Fernandez-Velasco, M., Goren, N., Benito, G., Blanco-Rivero, J., Bosca, L., and Delgado, C. (2003) Regional distribution of hyperpolarization-activated current (If) and hyperpolarizationactivated cyclic nucleotide-gated channel mRNA expression in ventricular cells from control and hypertrophied rat hearts. J. Physiol. 553, 395-405 (Pubitemid 37527543)
49. Fernandez-Velasco, M., Ruiz-Hurtado, G., and Delgado, C. (2006) I K1 and If in ventricular myocytes isolated from control and hypertrophied rat hearts. Pflügers Arch. 452, 146-154 (Pubitemid 44029839)
50. Hiramatsu, M., Furukawa, T., Sawanobori, T., and Hiraoka, M. (2002) Ion channel remodeling in cardiac hypertrophy is prevented by blood pressure reduction without affecting heart weight increase in rats with abdominal aortic banding. J. Cardiovasc. Pharmacol. 39, 866-874 (Pubitemid 34538817)
51. Hesse, M., Kondo, C. S., Clark, R. B., Su, L., Allen, F. L., Geary-Joo, C. T., Kunnathu, S., Severson, D. L., Nygren, A., Giles, W. R., and Cross, J. C. (2007) Dilated cardiomyopathy is associated with reduced expression of the cardiac sodium channel Scn5a. Cardiovasc. Res. 75, 498-509 (Pubitemid 47082512)
52. Eghbali, M., Deva, R., Alioua, A., Minosyan, T. Y, Ruan, H., Wang, Y, Toro, L., and Stefani, E. (2005) Molecular and functional signature of heart hypertrophy during pregnancy. Circ. Res. 96, 1208-1216 (Pubitemid 40827697)
53. Yasui, K., Liu, W., Opthof, T., Kada, K., Lee, J. K., Kamiya, K., and Kodama, I. (2001) I (f) current and spontaneous activity in mouse embryonic ventricular myocytes. Circ. Res. 88, 536-542 (Pubitemid 32240918)
54. 2+ channel activity by human natriuretic peptide in rabbit heart cells. Br. J. Pharmacol. 114, 1076-1082
55. 2+ efflux from freshly isolated adult rat cardiomyocytes. FEBS Lett. 419, 255-258 (Pubitemid 28010821)
56. Kecskemeti, V., Pacher, P., Pankucsi, C, and Nanasi, P. (1996) Comparative study of cardiac electrophysiological effects of atrial natriuretic peptide. Mol. Cell Biochem. 160-161, 53-59 (Pubitemid 26336335)
57. McGrath, M. F., de Bold, M. L., and de Bold, A. J. (2005) The endocrine function of the heart. Trends Endocrinol. Metab. 16, 469-477 (Pubitemid 41660863)
58. Kitashiro, S., Sugiura, T., Takayama, Y, Tsuka, Y, Izuoka, T., Tokunaga, S., and Iwasaka, T. (1999) Long-term administration of atrial natriuretic peptide in patients with acute heart failure. J. Cardiovasc. Pharmacol. 33, 948-952 (Pubitemid 29242778)
59. Suwa, M., Seino, Y, Nomachi, Y, Matsuki, S., and Funahashi, K (2005) Multicenter prospective investigation on efficacy and safety of carperitide for acute heart failure in the 'real world' of therapy. Circ. J. 69, 283-290 (Pubitemid 40410182)
60. Hayashi, M., Tsutamoto, T., Wada, A., Maeda, K., Mabuchi, N., Tsutsui, T., Horie, H., Ohnishi, M., and Kinoshita, M. (2001) Intravenous atrial natriuretic peptide prevents left ventricular remodeling in patients with first anterior acute myocardial infarction. J. Am. Coll. Cardiol. 37, 1820-1826 (Pubitemid 32499965)
61. Kuga, H., Ogawa, K., Oida, A., Taguchi, I., Nakatsugawa, M., Hoshi, T., Sugimura, H., Abe, S., and Kaneko, N. (2003) Administration of atrial natriuretic peptide attenuates reperfusion phenomena and preserves left ventricular regional wall motion after direct coronary angioplasty for acute myocardial infarction. Circ. J. 67, 443-448 (Pubitemid 36554068)